Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis

Stilling, R. M.; Dinan, T. G.; Cryan, J. F.

doi:10.1111/gbb.12109

Cited by 637Gut microbiota and healthEpigenetics and DNA MethylationTryptophan and brain disorders

Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis

Stilling, R. M., Dinan, T. G., Cryan, J. F.·2014·Genes, Brain and Behavior

DOI 10.1111/gbb.12109

Open this paper in CoChat — free account

Abstract

To date, there is rapidly increasing evidence for host-microbe interaction at virtually all levels of complexity, ranging from direct cell-to-cell communication to extensive systemic signalling, and involving various organs and organ systems, including the central nervous system. As such, the discovery that differential microbial composition is associated with alterations in behaviour and cognition has significantly contributed to establishing the microbiota-gut-brain axis as an extension of the well-accepted gut-brain axis concept. Many efforts have been focused on delineating a role for this axis in health and disease, ranging from stress-related disorders such as depression, anxiety and irritable bowel syndrome to neurodevelopmental disorders such as autism. There is also a growing appreciation of the role of epigenetic mechanisms in shaping brain and behaviour. However, the role of epigenetics in informing host-microbe interactions has received little attention to date. This is despite the fact that there are many plausible routes of interaction between epigenetic mechanisms and the host-microbiota dialogue. From this new perspective we put forward novel, yet testable, hypotheses. Firstly, we suggest that gut-microbial products can affect chromatin plasticity within their host's brain that in turn leads to changes in neuronal transcription and eventually alters host behaviour. Secondly, we argue that the microbiota is an important mediator of gene-environment interactions. Finally, we reason that the microbiota itself may be viewed as an epigenetic entity. In conclusion, the fields of (neuro)epigenetics and microbiology are converging at many levels and more interdisciplinary studies are necessary to unravel the full range of this interaction.

Integrity signals

Registry

Crossref · 10.1111/gbb.12109

Cites

191 of 191 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Preclinical evidence suggests that GM-mediated mechanisms are likely involved in modulating brain processes, including brain biochemistry, response to stress, pain interpretation, feeding, emotional behaviors, and cognition.
“Preclinical evidence suggests that GM-mediated mechanisms are likely involved in modulating brain processes, including brain biochemistry, response to stress, pain interpretation, feeding, emotional behaviors, and cognition (57–64).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [57]
Gut bacteria play a vital role in regulating important aspects of brain development and function, along with other host physiology.
“Studies have since shown that gut bacteria play a vital role in regulating important aspects of brain development and function, along with other host physiology [5, 7].”
From Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review (2020) · cites this paper as [7]
Butyrate and, to a lesser extent, other SCFAs can act as potent inhibitors of histone deacetylases.
“Lastly, butyrate and, to a lesser extent, other SCFAs can also act as a potent inhibitor of histone deacetylases (HDACs) (357).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [357]

Structure, function and diversity of the healthy human microbiome
The Human Microbiome Project Consortium (2012) · Nature · doi:10.1038/nature11234 · Cited by 11,726 · see citing works
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624 · see citing works
Enterotypes of the human gut microbiome
MetaHIT Consortium (additional members), Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., et al. (2011) · Nature · doi:10.1038/nature09944 · Cited by 7,548 · see citing works
Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
The human microbiome project
Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., & Gordon, J. I. (2007) · Nature · doi:10.1038/nature06244 · Cited by 6,091 · see citing works
Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002601107 · Cited by 4,774 · see citing works
Host-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
Vaginal microbiome of reproductive-age women
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002611107 · Cited by 4,254 · see citing works
Interactions Between the Microbiota and the Immune System
Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012) · Science · doi:10.1126/science.1223490 · Cited by 4,173 · see citing works
Ingestion of <i>Lactobacillus</i> strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
The gut microbiota--masters of host development and physiology
Sommer, F., & Bäckhed, F. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2974 · Cited by 3,681 · see citing works
Gut microbiota composition correlates with diet and health in the elderly
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O’Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O’Sullivan, O., et al. (2012) · Nature · doi:10.1038/nature11319 · Cited by 3,314 · see citing works
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228 · see citing works
Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria
Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J.-P., & Ricciardi‐Castagnoli, P. (2001) · Nature Immunology · doi:10.1038/86373 · Cited by 2,554 · see citing works
Gut–brain axis: How the microbiome influences anxiety and depression
Foster, J. A., & McVey Neufeld, K.-A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.005 · Cited by 2,460 · cited 2× · see citing works
“…Genes, Brain and Behavior (2014) 13: 69–86 T ab le 2: B io ch em ic al an d m ol ec ul ar al te ra tio ns w ith di ff er en tia lm ic ro bi ot a co m po si tio n Genes, Brain and Behavior (2014) 13: 69–86 73 a critical time window during adolescence (Clarke et al. 2013; Foster & Neufeld 2013).”
Background
The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner
Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.77 · Cited by 1,893 · see citing works
Self-citation
Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action
Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. (2006) · Nature Neuroscience · doi:10.1038/nn1659 · Cited by 1,780 · see citing works
The ageing systemic milieu negatively regulates neurogenesis and cognitive function
Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A., et al. (2011) · Nature · doi:10.1038/nature10357 · Cited by 1,763 · see citing works
The Intestinal Microbiota Affect Central Levels of Brain-Derived Neurotropic Factor and Behavior in Mice
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Gut feelings: the emerging biology of gut-brain communication
Mayer, E. A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3071 · Cited by 1,726 · see citing works
Induction of autophagy by spermidine promotes longevity
Eisenberg, T., Knauer, H., Schauer, A., Büttner, S., Ruckenstuhl, C., Carmona-Gutierrez, D., Ring, J., Schroeder, S., Magnes, C., Antonacci, L., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1975 · Cited by 1,680 · see citing works
The interplay between the intestinal microbiota and the brain
Collins, S. M., Surette, M., & Bercik, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2876 · Cited by 1,611 · cited 3× · see citing works
“…on different aspects ranging from basic microbiology to translational applications (e.g. see Bercik et al. 2012; Berer & Krishnamoorthy 2012; Collins et al. 2012b, 2013; Cryan & Dinan 2012; Cryan & O’Mahony 2011; Forsythe & Kunze 2013; Lyte 2011, 2013; Nicholson et al. 2012; Rhee et al.…”
Background
Inhibition of Histone Deacetylase Activity by Butyrate
Davie, J. R. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.7.2485s · Cited by 1,515 · see citing works
The role of microorganisms in coral health, disease and evolution
ROSENBERG, E. B., Koren, O., Reshef, L., Efrony, R., & Zilber‐Rosenberg, I. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1635 · Cited by 1,507 · see citing works
Reduced anxiety-like behavior and central neurochemical change in germ-free mice: Behavior in germ-free mice
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392 · see citing works
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · cited 3× · see citing works
“…ranging from basic microbiology to translational applications (e.g. see Bercik et al. 2012; Berer & Krishnamoorthy 2012; Collins et al. 2012b, 2013; Cryan & Dinan 2012; Cryan & O’Mahony 2011; Forsythe & Kunze 2013; Lyte 2011, 2013; Nicholson et al. 2012; Rhee et al. 2009; Sommer & Bäckhed 2013).”
Background
Psychobiotics: A novel class of psychotropic
Dinan, T. G., Stanton, C., & Cryan, J. F. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.05.001 · Cited by 1,287 · see citing works
Gut immune maturation depends on colonization with a host-specific microbiota
Chung, H., Pamp, S. J., Hill, J. A., Surana, N. K., Edelman, S. M., Troy, E. B., Reading, N. C., Villablanca, E. J., Wang, S., Mora, J. R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.037 · Cited by 1,241 · see citing works
Recovery of learning and memory is associated with chromatin remodelling
Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., & Tsai, L.-H. (2007) · Nature · doi:10.1038/nature05772 · Cited by 1,227 · see citing works
Consumption of fermented milk product with probiotic modulates brain activity
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.043 · Cited by 1,192 · see citing works
Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123 · see citing works
The Inheritance of Epigenetic Defects
Holliday, R. (1987) · Science · doi:10.1126/science.3310230 · Cited by 1,078 · see citing works
Sodium butyrate inhibits histone deacetylation in cultured cells
Candido, E. (1978) · Cell · doi:10.1016/0092-8674(78)90305-7 · Cited by 1,036 · see citing works
The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication
Bercik, P., Park, A. J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P. A., Fahnestock, M., Moine, D., et al. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01796.x · Cited by 1,018 · see citing works
Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression
Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999 · see citing works
The microbiome-gut-brain axis: from bowel to behavior
Cryan, J. F., & O’Mahony, S. M. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01664.x · Cited by 990 · see citing works
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952 · see citing works
Self-citation
Altered Histone Acetylation Is Associated with Age-Dependent Memory Impairment in Mice
Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R. C., Cota, P., Wittnam, J. L., Gogol-Doering, A., Opitz, L., et al. (2010) · Science · doi:10.1126/science.1186088 · Cited by 951 · see citing works
Bacteria activate sensory neurons that modulate pain and inflammation
Chiu, I. M., Heesters, B. A., Ghasemlou, N., Von Hehn, C. A., Zhao, F., Tran, J., Wainger, B., Strominger, A., Muralidharan, S., Horswill, A. R., et al. (2013) · Nature · doi:10.1038/nature12479 · Cited by 949 · see citing works
MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system
Mellén, M., Ayata, P., Dewell, S., Kriaucionis, S., & Heintz, N. (2012) · Cell · doi:10.1016/j.cell.2012.11.022 · Cited by 943 · see citing works
Genomic variation landscape of the human gut microbiome
Schloissnig, S., Arumugam, M., Sunagawa, S., Mitreva, M., Tap, J., Zhu, A., Waller, A., Mende, D. R., Kultima, J. R., Martin, J., et al. (2013) · Nature · doi:10.1038/nature11711 · Cited by 907 · see citing works
Microbiota is essential for social development in the mouse
Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.65 · Cited by 866 · see citing works
An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota
Jeffery, I. B., O'Toole, P. W., Öhman, L., Claesson, M. J., Deane, J., Quigley, E. M. M., & Simrén, M. (2012) · Gut · doi:10.1136/gutjnl-2011-301501 · Cited by 835 · see citing works
5-hmC–mediated epigenetic dynamics during postnatal neurodevelopment and aging
Szulwach, K. E., Li, X., Li, Y., Song, C., Wu, H., Dai, Q., Irier, H. A., Upadhyay, A. K., Gearing, M., Levey, A. I., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2959 · Cited by 819 · see citing works
Influences of microbiota on intestinal immune system development.
Cebra, J. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.5.1046s · Cited by 819 · see citing works
Mom Knows Best: The Universality of Maternal Microbial Transmission
Funkhouser-Jones, L. J., & Bordenstein, S. R. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001631 · Cited by 806 · see citing works
Fatal attraction in rats infected with Toxoplasma gondii
Berdoy, M., Webster, J. P., & Macdonald, D. W. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1182 · Cited by 731 · see citing works
Therapeutic Potential of Fecal Microbiota Transplantation
Smits, L. P., Bouter, K. E. C., de Vos, W. M., Borody, T. J., & Nieuwdorp, M. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.08.058 · Cited by 717 · see citing works
Histone acetylation: molecular mnemonics on the chromatin
Gräff, J., & Tsai, L.-H. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3427 · Cited by 680 · see citing works
Chronic Gastrointestinal Inflammation Induces Anxiety-Like Behavior and Alters Central Nervous System Biochemistry in Mice
Bercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674 · see citing works
Control of Inducible Gene Expression by Signal-Dependent Transcriptional Elongation
Hargreaves, D. C., Horng, T., & Medzhitov, R. M. (2009) · Cell · doi:10.1016/j.cell.2009.05.047 · Cited by 649 · see citing works
Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon
Waldecker, M., Kautenburger, T., Daumann, H., Busch, C., & Schrenk, D. (2008) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2007.08.002 · Cited by 615 · see citing works
Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats
Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.024 · Cited by 612 · see citing works
Histone Deacetylase 5 Epigenetically Controls Behavioral Adaptations to Chronic Emotional Stimuli
Renthal, W., Maze, I., Krishnan, V., Covington, H. E., Xiao, G., Kumar, A., Russo, S. J., Graham, A., Tsankova, N., Kippin, T. E., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.032 · Cited by 599 · see citing works
Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors
Vyas, A., Kim, S.-K., Giacomini, N., Boothroyd, J. C., & Sapolsky, R. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608310104 · Cited by 571 · see citing works
New insights into brain BDNF function in normal aging and Alzheimer disease
Tapia‐Arancibia, L., Aliaga, E., Silhol, M., & Arancibia, S. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.07.007 · Cited by 571 · see citing works
Carpenter's Human Neuroanatomy
Parent, A., & Carpenter, M. B. (1996) · Medical Entomology and Zoology · Cited by 561 · see citing works
The Host Genotype Affects the Bacterial Community in the Human Gastronintestinal Tract
Zoetendal, A. D. L. A. E. G. (2001) · Microbial Ecology in Health and Disease · doi:10.1080/089106001750462669 · Cited by 558 · see citing works
Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design, and use of probiotics.
Lyte, M. (2011) · BioEssays · doi:10.1002/bies.201100024 · Cited by 549 · see citing works
Human gut microbiome: the second genome of human body
Zhu, B., Wang, X., & Li, L. (2010) · Protein & Cell · doi:10.1007/s13238-010-0093-z · Cited by 535 · see citing works
Cesarean Versus Vaginal Delivery: Long-term Infant Outcomes and the Hygiene Hypothesis
Neu, J., & Rushing, J. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.03.008 · Cited by 528 · see citing works
Epigenetic mechanisms in cognition
Day, J. J., & Sweatt, J. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.019 · Cited by 510 · see citing works
Histamine Derived from Probiotic Lactobacillus reuteri Suppresses TNF via Modulation of PKA and ERK Signaling
Thomas, C. M., Hong, T., van Pijkeren, J. P., Hemarajata, P., Trinh, D. V., Hu, W., Britton, R. A., Kalkum, M., & Versalovic, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031951 · Cited by 491 · see citing works
DNA methylation and memory formation
Day, J. J., & Sweatt, J. D. (2010) · Nature Neuroscience · doi:10.1038/nn.2666 · Cited by 488 · see citing works
II. Stress and intestinal barrier function
Söderholm, J. D., & Perdue, M. H. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.1.g7 · Cited by 467 · see citing works
Increased IgA and IgM responses against gut commensals in chronic depression: Further evidence for increased bacterial translocation or leaky gut
Maes, M., Kubera, M., Leunis, J.-C., & Berk, M. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.02.023 · Cited by 446 · see citing works
Tet1 Is Critical for Neuronal Activity-Regulated Gene Expression and Memory Extinction
Rudenko, A., Dawlaty, M. M., Seo, J., Cheng, A. W., Meng, J., Le, T. T., Faull, K. F., Jaenisch, R., & Tsai, L. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.003 · Cited by 435 · see citing works
Short-chain fatty acid fermentation products of the gut microbiome: implications in autism spectrum disorders
MacFabe, D. F. (2012) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v23i0.19260 · Cited by 432 · see citing works
Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress
Zareie, M., Johnson‐Henry, K. C., Jury, J., Yang, P.-C., Ngan, B., McKay, D. M., Söderholm, J. D., Perdue, M. H., & Sherman, P. M. (2006) · Gut · doi:10.1136/gut.2005.080739 · Cited by 423 · see citing works
Microbes and the gut‐brain axis
Bercik, P., Collins, S. M., & Verdu, E. F. (2012) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2012.01906.x · Cited by 417 · see citing works
Maternal separation as a model of brain-gut axis dysfunction
O’Mahony, S. M., Hyland, N. P., Dinan, T. G., & Cryan, J. F. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2010-9 · Cited by 415 · see citing works
The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality
Montiel-Castro, A. J., González-Cervantes, R. M., Bravo-Ruiseco, G., & Pacheco-López, G. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00070 · Cited by 413 · see citing works
TET1 Controls CNS 5-Methylcytosine Hydroxylation, Active DNA Demethylation, Gene Transcription, and Memory Formation
Kaas, G. A., Zhong, C., Eason, D. E., Ross, D. L., Vachhani, R., Ming, G., King, J. R., Song, H., & Sweatt, J. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.032 · Cited by 411 · see citing works
Sodium butyrate improves memory function in an Alzheimer's disease mouse model when administered at an advanced stage of disease progression
Govindarajan, N., Agis-Balboa, R. C., Walter, J., Sananbenesi, F., & Fischer, A. (2011) · Journal of Alzheimer's Disease · doi:10.3233/jad-2011-110080 · Cited by 405 · see citing works
Gastrointestinal microbiology enters the metagenomics era
Frank, D. N., & Pace, N. R. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f2b0e8 · Cited by 405 · see citing works
Restoring polyamines protects from age-induced memory impairment in an autophagy-dependent manner
Gupta, V., Scheunemann, L., Eisenberg, T., Mertel, S., Bhukel, A., Koemans, T. S., Kramer, J. M., Liu, K. S. Y., Schroeder, S., Stunnenberg, H. G., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3512 · Cited by 374 · see citing works
The Double Bromodomain Proteins Brd2 and Brd3 Couple Histone Acetylation to Transcription
LeRoy, G., Rickards, B., & Flint, S. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.01.018 · Cited by 374 · see citing works
Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity.
Cowansage, K., LeDoux, J., & Monfils, M.-H. (2010) · Current Molecular Pharmacology · doi:10.2174/1874467211003010012 · Cited by 372 · cited 2× · see citing works
“a number of psychiatric and neurodegenerative diseases (Cowansage et al. 2010; Tapia-Arancibia et al. 2008; Walker et al. 2012).”
Background
Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder
MacFabe, D. F., Cain, N. E., Boon, F., Ossenkopp, K.-P., & Cain, D. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.005 · Cited by 365 · see citing works
Epigenetics and Bacterial InfectionsPreprint
Bierne, H., Hamon, M. A., & Cossart, P. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a010272 · Cited by 363 · see citing works
Bacterial Neuroactive Compounds Produced by Psychobiotics
Wall, R., Cryan, J. F., Ross, R. P., Fitzgerald, G. F., Dinan, T. G., & Stanton, C. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4_10 · Cited by 362 · see citing works
Targeting the correct HDAC(s) to treat cognitive disorders
Fischer, A., Sananbenesi, F., Mungenast, A. E., & Tsai, L. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.09.003 · Cited by 355 · see citing works
The human gut microbiome: current knowledge, challenges, and future directions
Dave, M., Higgins, P., Middha, S., & Rioux, K. P. (2012) · Translational research · doi:10.1016/j.trsl.2012.05.003 · Cited by 338 · see citing works
Voices from within: gut microbes and the CNS
Forsythe, P., & Kunze, W. A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1028-z · Cited by 336 · see citing works
Epigenetic sources of behavioral differences in mice
Francis, D. D., Szegda, K. L., Campbell, G., Martin, W. D., & Insel, T. R. (2003) · Nature Neuroscience · doi:10.1038/nn1038 · Cited by 333 · see citing works
Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression
Latham, T., Mackay, C. L., Sproul, D., Karim, M., Culley, J., Harrison, D. J., Hayward, L., Langridge‐Smith, P. R. R., Gilbert, N., & Ramsahoye, B. H. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks066 · Cited by 331 · see citing works
The Emerging Field of Neuroepigenetics
Sweatt, J. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.023 · Cited by 324 · see citing works
Chemokines: a new class of neuromodulator?
Rostène, W. H., Kitabgi, P., & Parsadaniantz, S. M. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2255 · Cited by 321 · see citing works
Programming infant gut microbiota: influence of dietary and environmental factors
Marques, T. M., Wall, R., Ross, R. P., Fitzgerald, G. F., Ryan, C. A., & Stanton, C. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.03.020 · Cited by 314 · see citing works
Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat
Santos, J., Yang, P.-C., Söderholm, J. D., Benjamin, M., & Perdue, M. H. (2001) · Gut · doi:10.1136/gut.48.5.630 · Cited by 313 · see citing works
Suppression of the antiviral response by an influenza histone mimic
Marazzi, I., Ho, J., Kim, J., Manicassamy, B., Dewell, S. B., Albrecht, R. A., Seibert, C. W., Schaefer, U., Jeffrey, K. L., Prinjha, R. K., et al. (2012) · Nature · doi:10.1038/nature10892 · Cited by 312 · see citing works
Long noncoding RNAs in development and disease of the central nervous system
Ng, S., Lin, L., Soh, B.-S., & Stanton, L. W. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.03.002 · Cited by 308 · see citing works
Distinct antimicrobial peptide expression determines host species-specific bacterial associations
Franzenburg, S., Walter, J., Künzel, S., Wang, J., Baines, J. F., Bosch, T. C. G., & Fraune, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304960110 · Cited by 308 · see citing works
Two Time Periods of Hippocampal mRNA Synthesis Are Required for Memory Consolidation of Fear-Motivated Learning
Igaz, L. M., Vianna, M. R. M. R., Medina, J. H., & Izquierdo, I. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06781.2002 · Cited by 305 · see citing works
The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse
McVey Neufeld, K. A., Mao, Y. K., Bienenstock, J., Foster, J. A., & Kunze, W. A. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12049 · Cited by 299 · see citing works
Brain function and chromatin plasticity
Dulac, C. G. (2010) · Nature · doi:10.1038/nature09231 · Cited by 299 · see citing works
Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease
Collins, L., Toulouse, A., Connor, T. J., & Nolan, Y. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.028 · Cited by 298 · see citing works
The Potential of HDAC Inhibitors as Cognitive Enhancers
Gräff, J., & Tsai, L. (2013) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-011112-140216 · Cited by 297 · see citing works
Altered colonic function and microbiota profile in a mouse model of chronic depression
Park, A. J., Collins, J., Blennerhassett, P. A., Ghia, J., Verdu, E. F., Berčík, P., & Collins, S. M. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12153 · Cited by 291 · see citing works
Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome–gut–brain axis
Davari, S., Talaei, S. A., Alaei, H., & salami, M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.02.055 · Cited by 290 · see citing works
The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation
Weng, N.-P., Araki, Y., & Subedi, K. (2012) · Nature Reviews Immunology · doi:10.1038/nri3173 · Cited by 290 · see citing works
Introduction to intestinal microecology
Luckey, T. D. (1972) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/25.12.1292 · Cited by 288 · see citing works
Innate Immunity in the CNS: Redefining the Relationship between the CNS and Its Environment
Lampron, A., ElAli, A., & Rivest, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.005 · Cited by 282 · see citing works
A Role for SIRT2-Dependent Histone H3K18 Deacetylation in Bacterial Infection
Eskandarian, H. A., Impens, F., Nahori, M., Soubigou, G., Coppée, J., Cossart, P., & Hamon, M. A. (2013) · Science · doi:10.1126/science.1238858 · Cited by 270 · see citing works
The gut microbiome: the role of a virtual organ in the endocrinology of the host
Evans, J. M., Morris, L. S., & Marchesi, J. R. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0131 · Cited by 264 · see citing works
Legionella pneumophila Effector RomA Uniquely Modifies Host Chromatin to Repress Gene Expression and Promote Intracellular Bacterial Replication
Rolando, M., Sanulli, S., Rusniok, C., Gómez-Valero, L., Bertholet, C., Sahr, T., Margueron, R., & Buchrieser, C. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.03.004 · Cited by 262 · see citing works
The Gut Microbiome: A New Frontier in Autism Research
Mulle, J. G., Sharp, W. G., & Cubells, J. F. (2013) · Current Psychiatry Reports · doi:10.1007/s11920-012-0337-0 · Cited by 262 · see citing works
Epigenetics of Host–Pathogen Interactions: The Road Ahead and the Road Behind
Gómez-Díaz, E., Jordà, M., Peinado, M., & Rivero, A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003007 · Cited by 259 · see citing works
ASSOCIATION OF GERMFREE MICE WITH BACTERIA ISOLATED FROM NORMAL MICE
Schaedler, R. W., Dubos, R. J., & Costello, R. L. (1965) · The Journal of Experimental Medicine · doi:10.1084/jem.122.1.77 · Cited by 258 · see citing works
Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis
Alenghat, T., Osborne, L. C., Saenz, S. A., Kobuley, D. E., Ziegler, C. G. K., Mullican, S. E., Choi, I., Grunberg, S., Sinha, R., Wynosky-Dolfi, M. A., et al. (2013) · Nature · doi:10.1038/nature12687 · Cited by 248 · see citing works
Long Noncoding RNAs Usher In a New Era in the Biology of Enhancers
Ørom, U. A., & Shiekhattar, R. (2013) · Cell · doi:10.1016/j.cell.2013.08.028 · Cited by 243 · see citing works
Autism Spectrum Disorders and Epigenetics
Grafodatskaya, D., Chung, B., Szatmari, P., & Weksberg, R. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.05.005 · Cited by 235 · see citing works
How and why Toxoplasma makes us crazy
Jaroslav Flegr, A. (2013) · Trends in Parasitology · doi:10.1016/j.pt.2013.01.007 · Cited by 235 · see citing works
Metabolic Perturbance in Autism Spectrum Disorders: A Metabolomics Study
Ming, X., Stein, T. P., Barnes, V., Rhodes, N., & Guo, L. (2012) · Journal of Proteome Research · doi:10.1021/pr300910n · Cited by 234 · see citing works
Genotype Is a Stronger Determinant than Sex of the Mouse Gut Microbiota
Kovacs, A., Ben-Jacob, N., Tayem, H., Halperin, E., Iraqi, F. A., & Gophna, U. (2010) · Microbial Ecology · doi:10.1007/s00248-010-9787-2 · Cited by 226 · see citing works
Review article: probiotics for the treatment of irritable bowel syndrome – focus on lactic acid bacteria
Clarke, G. A., Cryan, J. F., Dinan, T. G., & Quigley, E. M. M. (2012) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2011.04965.x · Cited by 217 · see citing works
The Distribution of Toxoplasma gondii Cysts in the Brain of a Mouse with Latent Toxoplasmosis: Implications for the Behavioral Manipulation Hypothesis
Berenreiterová, M., Jaroslav Flegr, A., Kuběna, A. A., & Němec, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028925 · Cited by 216 · see citing works
Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour
Webster, J. P. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(01)01459-9 · Cited by 216 · see citing works
The immunology of neurodegeneration
Czirr, E., & Wyss‐Coray, T. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58656 · Cited by 211 · see citing works
Histone Modifications and Chromatin Remodeling during Bacterial Infections
Hamon, M. A., & Cossart, P. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.07.009 · Cited by 211 · see citing works
Molecular Characterisation of Gastrointestinal Microbiota of Children With Autism (With and Without Gastrointestinal Dysfunction) and Their Neurotypical Siblings
Gondalia, S. V., Palombo, E. A., Knowles, S. R., Cox, S. B., Meyer, D., & Austin, D. W. (2012) · Autism Research · doi:10.1002/aur.1253 · Cited by 208 · see citing works
Effect of Intestinal Microbial Ecology on the Developing Brain
Douglas‐Escobar, M., Elliott, E., & Neu, J. (2013) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2013.497 · Cited by 207 · see citing works
The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications
Collins, S. M., Kassam, Z., & Berčík, P. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.004 · Cited by 206 · see citing works
Deep Sequencing Identifies Ethnicity-Specific Bacterial Signatures in the Oral Microbiome
Mason, M. R., Nagaraja, H. N., Camerlengo, T., Joshi, V., & Kumar, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077287 · Cited by 205 · see citing works
The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat
McKernan, D. P., Fitzgerald, P., Dinan, T. G., & Cryan, J. F. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01520.x · Cited by 205 · see citing works
Pathways underlying the gut-to-brain connection in autism spectrum disorders as future targets for disease management
de Theije, C. G. M., Wu, J., da Silva, S. L., Kamphuis, P. J. G. H., Garssen, J., Korte, S. M., & Kraneveld, A. D. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.07.013 · Cited by 203 · see citing works
MicroRNAs in learning, memory, and neurological diseases: Figure 1.Preprint
Wang, W., Kwon, E. J., & Tsai, L. (2012) · Learning & Memory · doi:10.1101/lm.026492.112 · Cited by 203 · see citing works
Manipulation of Host Behavior by Parasitic Insects and Insect Parasites
Libersat, F., Delago, A., & Gal, R. (2008) · Annual Review of Entomology · doi:10.1146/annurev.ento.54.110807.090556 · Cited by 202 · see citing works
The enteric bacterial metabolite propionic acid alters brain and plasma phospholipid molecular species: Further development of a rodent model of autism spectrum disorders
Thomas, R. H., Meeking, M. M., Mepham, J. R., Tichenoff, L., Possmayer, F., Liu, S., & MacFabe, D. F. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-153 · Cited by 200 · see citing works
Histone Methylation by NUE, a Novel Nuclear Effector of the Intracellular Pathogen Chlamydia trachomatis
Pennini, M. E., Perrinet, S., Dautry‐Varsat, A., & Subtil, A. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000995 · Cited by 195 · see citing works
The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework
Rosenberg, E., Sharon, G., & Zilber‐Rosenberg, I. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.01995.x · Cited by 189 · see citing works
THE ROLES OF HOST EVOLUTIONARY RELATIONSHIPS (GENUS: NASONIA) AND DEVELOPMENT IN STRUCTURING MICROBIAL COMMUNITIES
Brucker, R. M., & Bordenstein, S. R. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01454.x · Cited by 181 · see citing works
Host manipulation by parasites: a multidimensional phenomenon
Frédéric Thomas, A., Poulin, R., & Jacques Brodeur, B. (2010) · Oikos · doi:10.1111/j.1600-0706.2009.18077.x · Cited by 178 · see citing works
Bacteroides fragilis polysaccharide A is necessary and sufficient for acute activation of intestinal sensory neurons
Mao, Y.-K., Kasper, D. L., Wang, B., Forsythe, P., Bienenstock, J., & Kunze, W. A. (2013) · Nature Communications · doi:10.1038/ncomms2478 · Cited by 178 · see citing works
The Potential Role of Probiotics in the Management of Childhood Autism Spectrum Disorders
Critchfield, J. W., van Hemert, S., Ash, M. E., Mulder, L. H. C., & Ashwood, P. (2011) · Gastroenterology Research and Practice · doi:10.1155/2011/161358 · Cited by 175 · see citing works
Antidepressant-Like Properties of Novel HDAC6-Selective Inhibitors with Improved Brain Bioavailability
Jochems, J., Boulden, J., Lee, B. G., Blendy, J. A., Jarpe, M. B., Mazitschek, R., van Duzer, J. H., Jones, S. S., & Berton, O. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.207 · Cited by 168 · see citing works
Toxoplasma gondiiinfection, from predation to schizophrenia: can animal behaviour help us understand human behaviour?
Webster, J. P., Kaushik, M., Bristow, G. C., & McConkey, G. A. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.074716 · Cited by 168 · see citing works
When bacteria target the nucleus: the emerging family of nucleomodulins
Bierne, H., & Cossart, P. (2012) · Cellular Microbiology · doi:10.1111/j.1462-5822.2012.01758.x · Cited by 163 · see citing works
HDAC6 Regulates Glucocorticoid Receptor Signaling in Serotonin Pathways with Critical Impact on Stress Resilience
Espallergues, J., Teegarden, S. L., Veerakumar, A., Boulden, J., Challis, C., Jochems, J., Chan, M., Petersen, T. L., Deneris, E. S., Matthias, P., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5634-11.2012 · Cited by 147 · see citing works
SLC5A8 Triggers Tumor Cell Apoptosis through Pyruvate-Dependent Inhibition of Histone Deacetylases
Thangaraju, M., Gopal, E., Martin, P. M., Ananth, S., Smith, S. B., Prasad, P. D., Sterneck, E., & Ganapathy, V. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1950 · Cited by 140 · see citing works
Transgenerational Epigenetic Effects on Brain Functions
Bohacek, J., Gapp, K., Saab, B. J., & Mansuy, I. M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.019 · Cited by 137 · see citing works
Epigenetics and Evolution
Mendizabal, I., Keller, T. E., Zeng, J., & Yi, S. V. (2014) · Integrative and Comparative Biology · doi:10.1093/icb/icu040 · Cited by 136 · see citing works
The role of histone acetylation in age-associated memory impairment and Alzheimer’s disease
Stilling, R. M., & Fischer, A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.04.002 · Cited by 136 · see citing works
Little things on which happiness depends: microRNAs as novel therapeutic targets for the treatment of anxiety and depression
O’Connor, R. M., Dinan, T. G., & Cryan, J. F. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.162 · Cited by 133 · see citing works
Cognitive neuroepigenetics: A role for epigenetic mechanisms in learning and memory
Day, J. J., & Sweatt, J. D. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.12.008 · Cited by 130 · see citing works
Importance of epigenetic mechanisms in visceral pain induced by chronic water avoidance stress
Tran, L., Chaloner, A., Sawalha, A. H., & van-Meerveld, B. G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.016 · Cited by 124 · see citing works
HDAC3 and the molecular brake pad hypothesis
McQuown, S. C., & Wood, M. A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.04.005 · Cited by 122 · see citing works
Host-manipulation by parasites with complex life cycles: adaptive or not?
Cézilly, F., Frédéric Thomas, A., Médoc, V., & Perrot‐Minnot, M. (2010) · Trends in Parasitology · doi:10.1016/j.pt.2010.03.009 · Cited by 114 · see citing works
Reversible epigenetic histone modifications and Bdnf expression in neurons with aging and from a mouse model of Alzheimer’s disease
Walker, M. P., LaFerla, F. M., Oddo, S., & Brewer, G. J. (2012) · AGE · doi:10.1007/s11357-011-9375-5 · Cited by 106 · see citing works
Cognitive performance in irritable bowel syndrome: evidence of a stress-related impairment in visuospatial memory
Kennedy, P. J., Clarke, G., O‘Neill, A., Groeger, J. A., Quigley, E. M. M., Shanahan, F., Cryan, J. F., & Dinan, T. G. (2014) · Psychological Medicine · doi:10.1017/s0033291713002171 · Cited by 106 · see citing works
Ingestion of mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice
Matthews, D. M., & Jenks, S. M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.02.007 · Cited by 105 · see citing works
The Human Gut Bacteria Bacteroides thetaiotaomicron and Fusobacterium varium Produce Putrescine and Spermidine in Cecum of Pectin-Fed Gnotobiotic Rats
Noack, J., Dongowski, G., Hartmann, L., & Blaut, M. (2000) · Journal of Nutrition · doi:10.1093/jn/130.5.1225 · Cited by 101 · see citing works
The gut microbiota—a clinical perspective on lessons learned
Shanahan, F. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.145 · Cited by 100 · see citing works
Microbes' roadmap to neurons
Kristensson, K. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3029 · Cited by 100 · see citing works
New mechanisms in memory storage: piRNAs and epigenetics
Landry, C. D., Kandel, E. R., & Rajasethupathy, P. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.05.004 · Cited by 95 · see citing works
IBS: an epigenetic perspective
Dinan, T. G., Cryan, J. F., Shanahan, F., Keeling, P. W. N., & Quigley, E. M. M. (2010) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2010.99 · Cited by 90 · see citing works
Gene, environment, and brain‐gut interactions in irritable bowel syndrome
Fukudo, S., & Kanazawa, M. (2011) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2011.06631.x · Cited by 87 · see citing works
Physicochemical analysis of electrostatic foundation for DNA–protein interactions in chromatin transformations
Korolev, N., Vorontsova, O. V., & Nordenskiöld, L. (2006) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2006.11.003 · Cited by 84 · see citing works
Modulation of inflammatory cytokines and mitogen-activated protein kinases by acetate in primary astrocytes
Soliman, M. L., Combs, C. K., & Rosenberger, T. A. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9426-4 · Cited by 84 · see citing works
Commensal gut flora and brain autoimmunity: a love or hate affair?
Berer, K., & Krishnamoorthy, G. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-0949-9 · Cited by 82 · see citing works
Does the Human Gut Microbiota Contribute to the Etiology of Autism Spectrum Disorders?
Louis, P. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2286-1 · Cited by 81 · see citing works
Basic Pathophysiologic Mechanisms in Irritable Bowel Syndrome
Mayer, E. A., Naliboff, B. D., & Chang, L. (2001) · Digestive Diseases · doi:10.1159/000050682 · Cited by 81 · see citing works
Language: Disputed definitions
Ledford, H. K. (2008) · Nature · doi:10.1038/4551023a · Cited by 75 · see citing works
Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines
Moal, V. L.-L., & Servin, A. L. (2013) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00064-12 · Cited by 75 · see citing works
Epigenetic regulation of genomic integrity
Deem, A. K., Li, X., & Tyler, J. K. (2012) · Chromosoma · doi:10.1007/s00412-011-0358-1 · Cited by 75 · see citing works
Microbe-induced epigenetic alterations in host cells: The coming era of patho-epigenetics of microbial infections
Minárovits, J. (2009) · Acta Microbiologica et Immunologica Hungarica · doi:10.1556/amicr.56.2009.1.1 · Cited by 73 · see citing works
Inhibition of mRNA synthesis in the hippocampus impairs consolidation and reconsolidation of spatial memory
da Silva, W. C. F. N., Bonini, J. S., Bevilaqua, L. R., Medina, J. H., Izquierdo, I., & Cammarota, M. (2007) · Hippocampus · doi:10.1002/hipo.20362 · Cited by 68 · see citing works
Mechanisms of Age-Related Cognitive Change and Targets for Intervention: Epigenetics
Kosik, K. S., Rapp, P. R., Raz, N., Small, S. A., Sweatt, J. D., & Tsai, L. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls110 · Cited by 66 · see citing works
An observational study of cognitive function in patients with irritable bowel syndrome and inflammatory bowel disease
Berrill, J. W., Gallacher, J., Hood, K., Green, J. T., Matthews, S. B., Campbell, A. K., & Smith, A. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12219 · Cited by 62 · see citing works
THE PURE‐CULTURE CONCEPT AND GNOTOBIOTICS
Reyniers, J. A. (1959) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1959.tb53091.x · Cited by 56 · see citing works
Microbial Endocrinology
Lyte, M., & Freestone, P. P. E. (2010) · Springer eBooks · doi:10.1007/978-1-4419-5576-0 · Cited by 55 · see citing works
Interplay of bromodomain and histone acetylation in the regulation of p300-dependent genes
Chen, J., Ghazawi, F. M., & Li, Q. (2010) · Epigenetics · doi:10.4161/epi.5.6.12224 · Cited by 50 · see citing works
Neural parasitology: how parasites manipulate host behaviour
Adamo, S. A., & Webster, J. P. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.082511 · Cited by 49 · see citing works
Epigenomic control of the innate immune response
Stender, J. D., & Glass, C. K. (2013) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2013.06.002 · Cited by 49 · see citing works
Epigenetics and Evolution
Saunders, P. T. (2017) · Human Development · doi:10.1159/000477993 · Cited by 48 · see citing works
The capacious hologenome
Brucker, R. M., & Bordenstein, S. R. (2013) · Zoology · doi:10.1016/j.zool.2013.08.003 · Cited by 46 · see citing works
Microbial–immune cross‐talk and regulation of the immune system
Cahenzli, J., Balmer, M. L., & McCoy, K. D. (2012) · Immunology · doi:10.1111/j.1365-2567.2012.03624.x · Cited by 40 · see citing works
Gene expression during memory formation
Igaz, L. M., Bekinschtein, P., Vianna, M. R. M. R., Izquierdo, I., & Medina, J. H. (2004) · Neurotoxicity Research · doi:10.1007/bf03033221 · Cited by 40 · see citing works
Microbial endocrinology and nutrition: A perspective on new mechanisms by which diet can influence gut-to-brain communication
Lyte, M. (2013) · PharmaNutrition · doi:10.1016/j.phanu.2012.11.002 · Cited by 40 · see citing works
Do gut microbial communities differ in pediatric IBS and health?
Shankar, V., Agans, R., Holmes, B., Raymer, M. G., & Paliy, O. (2013) · Gut Microbes · doi:10.4161/gmic.24827 · Cited by 36 · see citing works
Effects of polyamines on in vitro phosphorylation and acetylation of histones of the cerebral cortex of rats of various ages
Das, R., & Kanungo, M. S. (1979) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(79)91885-0 · Cited by 25 · see citing works
Nuclear microbiology—bacterial assault on the nucleolus
Bierne, H. (2013) · EMBO Reports · doi:10.1038/embor.2013.105 · Cited by 15 · see citing works
Treatment of Severe Constipation Improves Parkinsonʼs Disease (PD) Symptoms
Borody, T. J., Torres, M., Campbell, J., Hills, L., & Ketheeswaran, S. (2009) · The American Journal of Gastroenterology · doi:10.14309/00000434-200910003-00999 · Cited by 15 · see citing works
Role of probiotics as memory enhancer
Medhi, B., & Misra, S. (2013) · Indian Journal of Pharmacology · doi:10.4103/0253-7613.111917 · Cited by 11 · see citing works
Germfrec Vertebrates
Reyniers, J. A. (1960) · The American Journal of the Medical Sciences · doi:10.1097/00000441-196003000-00073 · Cited by 9 · see citing works
[Observations of the behavior of gnotobiotic piglets].
Kh, B. (1970) · PubMed · Cited by 6 · see citing works
Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health
Lyte, M., & Lambris, J. D. (2016) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-20215-0 · Cited by 4 · see citing works
Clinical Vignettes - Functional Bowel Disorders
(2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.492_14 · Cited by 2 · see citing works
Untitled work
Bailey (1999) · doi:10.1002/(sici)1098-2302(199909)35:2

Flagged first, then by citations

Sorted by citations

The Microbiota-Gut-Brain Axis
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.
(2015) · PubMed Central · Cited by 2,540 · see citing works
Gut/brain axis and the microbiota
Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
Butyrate: A Double-Edged Sword for Health?
Liu, H., Wang, J., He, T., Becker, S. R., Zhang, G., Li, D., & Ma, X. (2018) · Advances in Nutrition · doi:10.1093/advances/nmx009 · Cited by 1,158 · see citing works
The microbiome-gut-brain axis in health and disease
Dinan, T. G., & Cryan, J. F. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.09.007 · Cited by 1,111 · see citing works
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089 · see citing works
Control of brain development, function, and behavior by the microbiome
Sampson, T. R., & Mazmanian, S. K. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.011 · Cited by 1,093 · see citing works
Psychobiotics and the manipulation of bacteria–gut–brain signals
Sarkar, A., Lehto, S. M., Harty, S., Dinan, T. G., Cryan, J. F., & Burnet, P. W. J. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.09.002 · Cited by 1,068 · see citing works
Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033 · see citing works
The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis
Stilling, R. M., van de Wouw, M., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.06.011 · Cited by 891 · see citing works
The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders
Socała, K., Doboszewska, U., Szopa, A., Serefko, A., Włodarczyk, M., Zielińska, A., Poleszak, E., Fichna, J., & Wlaź, P. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105840 · Cited by 857 · see citing works
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour
Desbonnet, L., Clarke, G., Traplin, A., O’Sullivan, O., Crispie, F., Moloney, R. D., Cotter, P. D., Dinan, T. G., & Cryan, J. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.04.004 · Cited by 760 · see citing works
Kynurenine pathway metabolism and the microbiota-gut-brain axis
Kennedy, P. J., Cryan, J. F., Dinan, T. G., & Clarke, G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.002 · Cited by 724 · see citing works
Cognitive impairment by antibiotic-induced gut dysbiosis: analysis of gut microbiota-brain communication
Fröhlich, E. E., Farzi, A., Mayerhofer, R., Reichmann, F., Jačan, A., Wagner, B., Zinser, E., Bordag, N., Magnes, C., Fröhlich, E., et al. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.02.020 · Cited by 720 · see citing works
Biological embedding of childhood adversity: from physiological mechanisms to clinical implications
Berens, A. E., Jensen, S. K. G., & Nelson, C. A. (2017) · BMC Medicine · doi:10.1186/s12916-017-0895-4 · Cited by 657 · see citing works
“lites or molecular patterns, heightened inflammation with downstream neural effects, and induction of epigenetic changes [77, 79, 80].”
Background
Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior
Luczynski, P., McVey Neufeld, K.-A., Oriach, C. S., Clarke, G., Dinan, T. G., & Cryan, J. F. (2016) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw020 · Cited by 632 · see citing works
Gastrointestinal microbiota in children with autism in Slovakia
Tomova, A., Husarova, V., Lakatosova, S., Bakos, J., Vlkova, B., Babinska, K., & Ostatnikova, D. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.10.033 · Cited by 632 · see citing works
Butyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health?
Bourassa, M. W., Alim, I., Bultman, S. J., & Ratan, R. R. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.02.009 · Cited by 636 · see citing works
The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis?
Houser, M. C., & Tansey, M. G. (2017) · npj Parkinson's Disease · doi:10.1038/s41531-016-0002-0 · Cited by 588 · see citing works
Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes
Clark, A., & Mach, N. (2016) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-016-0155-6 · Cited by 583 · see citing works
“Given the gut microbiota’s diverse role in GI function, enteric immunity [70], endocrinology [11] as well as regulating oxidative stress [71–73] and hydration levels, it is not surprising that efforts to identify the mechanisms by which gut microbiota improves intestinal barrier function of elite athletes are increasi…”
Background
Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease
Pistollato, F., Sumalla Cano, S., Elio, I., Masias Vergara, M., Giampieri, F., & Battino, M. (2016) · Nutrition Reviews · doi:10.1093/nutrit/nuw023 · Cited by 496 · see citing works
Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown
Colston, T. J., & Jackson, C. R. (2016) · Molecular Ecology · doi:10.1111/mec.13730 · Cited by 508 · see citing works
Feeding the microbiota–gut–brain axis: Diet, microbiome, and neuropsychiatry
Sandhu, K. V., Sherwin, E., Schellekens, H., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Translational Research · doi:10.1016/j.trsl.2016.10.002 · Cited by 491 · see citing works
Microbiota-gut-brain axis: Modulator of host metabolism and appetite
van de Wouw, M., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Nutrition · doi:10.3945/jn.116.240481 · Cited by 461 · see citing works
Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
Self-citation
Influence of gut microbiota on neuropsychiatric disorders
Cénit, M. C., Sanz, Y., & Codoñer‐Franch, P. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i30.5486 · Cited by 418 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
The Possible Role of the Microbiota-Gut-Brain-Axis in Autism Spectrum Disorder
Srikantha, P., & Mohajeri, M. H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092115 · Cited by 400 · see citing works
Short-Chain Fatty Acids and Human Health: From Metabolic Pathways to Current Therapeutic Implications
Facchin, S., Bertin, L., Bonazzi, E., Lorenzon, G., Barba, C. D., Barberio, B., Zingone, F., Maniero, D., Scarpa, M., Ruffolo, C., et al. (2024) · Life · doi:10.3390/life14050559 · Cited by 422 · see citing works
Stress and the Microbiota–Gut–Brain Axis in Visceral Pain: Relevance to Irritable Bowel Syndrome
Moloney, R. D., Johnson, A. C., O’Mahony, S. M., Dinan, T. G., Meerveld, B. G., & Cryan, J. F. (2015) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12490 · Cited by 396 · see citing works
Secretory Products of the Human GI Tract Microbiome and Their Potential Impact on Alzheimer's Disease (AD): Detection of Lipopolysaccharide (LPS) in AD Hippocampus
Zhao, Y., Jaber, V., & Lukiw, W. J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00318 · Cited by 379 · see citing works
Stress, immunity, and the management of calves
Hulbert, L. E., & Moisá, S. J. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10198 · Cited by 370 · see citing works
Has the time come for a staging model to map the course of eating disorders from high risk to severe enduring illness? An examination of the evidence
Treasure, J., Stein, D., & Maguire, S. (2015) · Early Intervention in Psychiatry · doi:10.1111/eip.12170 · Cited by 353 · see citing works
Molecular insights into transgenerational non-genetic inheritance of acquired behaviours
Bohacek, J., & Mansuy, I. M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3964 · Cited by 318 · see citing works
Irritable bowel syndrome: A microbiome-gut-brain axis disorder?
Kennedy, P. J. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i39.14105 · Cited by 335 · see citing works
Sperm epigenetics and influence of environmental factors
Donkin, I., & Barrès, R. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.02.006 · Cited by 331 · see citing works
The Impact of Microbiota on Brain and Behavior: Mechanisms & Therapeutic Potential
Borre, Y. E., Moloney, R. D., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_17 · Cited by 329 · see citing works
Brain-Gut-Microbiota Axis and Mental Health
Dinan, T. G., & Cryan, J. F. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000519 · Cited by 325 · see citing works
Self-citation
Autism spectrum disorders and intestinal microbiota
De Angelis, M., Francavilla, R., Piccolo, M., De Giacomo, A., & Gobbetti, M. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1035855 · Cited by 311 · see citing works
Gut microbiota in neurodegenerative disorders
Sarkar, S. R., & Banerjee, S. (2019) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2019.01.004 · Cited by 319 · see citing works
Association Between Gut Microbiota and Autism Spectrum Disorder: A Systematic Review and Meta-Analysis
Xu, M., Xu, X., Li, J., & Li, F. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00473 · Cited by 309 · see citing works
Microbiota-gut-brain axis and the central nervous system
Zhu, X., Han, Y., Du, J., Liu, R., Jin, K., & Yi, W. (2017) · Oncotarget · doi:10.18632/oncotarget.17754 · Cited by 308 · see citing works
The Role of the Microbial Metabolites Including Tryptophan Catabolites and Short Chain Fatty Acids in the Pathophysiology of Immune-Inflammatory and Neuroimmune Disease
Morris, G., Berk, M., Carvalho, A. F., Caso, J. R., Sanz, Y., Walder, K. R., & Maes, M. H. J. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0004-2 · Cited by 307 · see citing works
Microbiota regulation of the mammalian gut-brain axis
Burokas, A., Moloney, R. D., Dinan, T. G., & Cryan, J. F. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2015.02.001 · Cited by 300 · see citing works
May the Force Be With You: The Light and Dark Sides of the Microbiota–Gut–Brain Axis in Neuropsychiatry
Sherwin, E., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2016) · CNS Drugs · doi:10.1007/s40263-016-0370-3 · Cited by 297 · see citing works
Gut Microbiota Dysbiosis, Oxidative Stress, Inflammation, and Epigenetic Alterations in Metabolic Diseases
Abdolmaleky, H. M., & Zhou, J. (2024) · Antioxidants · doi:10.3390/antiox13080985 · Cited by 311 · see citing works
Enteric Bacterial Metabolites Propionic and Butyric Acid Modulate Gene Expression, Including CREB-Dependent Catecholaminergic Neurotransmission, in PC12 Cells - Possible Relevance to Autism Spectrum Disorders
Nankova, B. B., Agarwal, R., MacFabe, D. F., & La Gamma, E. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103740 · Cited by 294 · see citing works
Sex differences in the gut microbiome–brain axis across the lifespan
Jašarević, E., Morrison, K. E., & Bale, T. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0122 · Cited by 295 · see citing works
Towards a systems view of IBS
Mayer, E. A., Labus, J. S., Tillisch, K., Cole, S. W., & Baldi, P. (2015) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.121 · Cited by 282 · see citing works
Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats
O’Mahony, S. M., Felice, V. D., Nally, K., Savignac, H. M., Claesson, M. J., Scully, P., Woznicki, J., Hyland, N. P., Shanahan, F., Quigley, E. M., et al. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.054 · Cited by 272 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat
Hoban, A. E., Moloney, R. D., Golubeva, A. V., McVey Neufeld, K. A., O’Sullivan, O., Patterson, E., Stanton, C., Dinan, T. G., Clarke, G., & Cryan, J. F. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.003 · Cited by 270 · see citing works
Enteric short-chain fatty acids: microbial messengers of metabolism, mitochondria, and mind: implications in autism spectrum disorders
MacFabe, D. F. (2015) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v26.28177 · Cited by 260 · see citing works
Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review
Chinna Meyyappan, A., Forth, E., Wallace, C. J. K., & Milev, R. (2020) · BMC Psychiatry · doi:10.1186/s12888-020-02654-5 · Cited by 254 · see citing works
Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome
Dinan, T. G., & Cryan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.103 · Cited by 246 · see citing works
Autoimmune diseases, gastrointestinal disorders and the microbiome in schizophrenia: more than a gut feeling
Severance, E. G., Yolken, R. H., & Eaton, W. W. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.027 · Cited by 256 · see citing works
Gut microbiota–brain axis in depression: the role of neuroinflammation
Carlessi, A. S., Borba, L. A., Zugno, A. I., Quevedo, J., & Réus, G. Z. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14631 · Cited by 243 · see citing works
Microbiome, inflammation, epigenetic alterations, and mental diseases
Alam, R., Abdolmaleky, H. M., & Zhou, J. (2017) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32567 · Cited by 240 · see citing works
Microbes & neurodevelopment – Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala
Stilling, R. M., Ryan, F. J., Hoban, A. E., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.07.009 · Cited by 233 · see citing works
Metabolites of Dietary Protein and Peptides by Intestinal Microbes and their Impacts on Gut
Fan, P. F., Li, L., Rezaei, A., Eslamfam, S., Che, D., & Ma, X. (2015) · Current Protein and Peptide Science · doi:10.2174/1389203716666150630133657 · Cited by 235 · see citing works
Gut Microbiota and Their Neuroinflammatory Implications in Alzheimer’s Disease
Giau, V. V., Wu, S., Jamerlan, A., An, S. S. A., Kim, S., & Hulme, J. (2018) · Nutrients · doi:10.3390/nu10111765 · Cited by 235 · see citing works
Microbiome disturbances and autism spectrum disorders
Rosenfeld, C. S. (2015) · Drug Metabolism and Disposition · doi:10.1124/dmd.115.063826 · Cited by 229 · see citing works
Dietary metabolites derived from gut microbiota: critical modulators of epigenetic changes in mammals
Bhat, M. I., & Kapila, R. (2017) · Nutrition Reviews · doi:10.1093/nutrit/nux001 · Cited by 227 · see citing works
The Potential Role of Gut Microbiota in Alzheimer’s Disease: From Diagnosis to Treatment
Varesi, A., Pierella, E., Romeo, M., Piccini, G. B., Alfano, C., Bjørklund, G., Oppong, A., Ricevuti, G., Esposito, C., Chirumbolo, S., et al. (2022) · Nutrients · doi:10.3390/nu14030668 · Cited by 225 · see citing works
Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish
Borrelli, L., Aceto, S., Agnisola, C., De Paolo, S., Dipineto, L., Stilling, R. M., Dinan, T. G., Cryan, J. F., Menna, L. F., & Fioretti, A. (2016) · Scientific Reports · doi:10.1038/srep30046 · Cited by 225 · see citing works
“As such, it has been shown that absence or modification of the enteric microbiota affects stress-associated anxiety-like and depressive-like behaviours 4,5 .”
Self-citation
Epigenetic Matters: The Link between Early Nutrition, Microbiome, and Long-term Health Development
Indrio, F., Martini, S., Francavilla, R., Corvaglia, L., Cristofori, F., Mastrolia, S. A., Neu, J., Rautava, S., Spena, G. R., Raimondi, F., et al. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00178 · Cited by 232 · see citing works
Cytotoxicity of Nanoparticles Contained in Food on Intestinal Cells and the Gut Microbiota
Fröhlich, E. E., & Fröhlich, E. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040509 · Cited by 223 · see citing works
The Gut-Brain Axis, BDNF, NMDA and CNS Disorders
Maqsood, R., & Stone, T. W. (2016) · Neurochemical Research · doi:10.1007/s11064-016-2039-1 · Cited by 223 · see citing works
Intestinal microbiota in early life and its implications on childhood health
Zhuang, L., Chen, H., Zhang, S., Zhuang, J., Li, Q., & Feng, Z. (2019) · Genomics, Proteomics & Bioinformatics · doi:10.1016/j.gpb.2018.10.002 · Cited by 219 · see citing works
The function of gut microbiota in immune-related neurological disorders: a review
Sittipo, P., Choi, J., Lee, S., & Lee, Y. K. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02510-1 · Cited by 221 · see citing works
Gut Microbiota: The Conductor in the Orchestra of Immune–Neuroendocrine Communication
El Aidy, S., Dinan, T. G., & Cryan, J. F. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.03.002 · Cited by 215 · see citing works
Mind-altering with the gut: Modulation of the gut-brain axis with probiotics
Kim, N., Yun, M., Oh, Y. J., & Choi, H.-J. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-8032-4 · Cited by 210 · see citing works
Gut Dysbiosis in Animals Due to Environmental Chemical Exposures
Rosenfeld, C. S. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00396 · Cited by 207 · see citing works
Microbiota Signaling Pathways that Influence Neurologic Disease
Cox, L. M., & Weiner, H. L. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0598-8 · Cited by 208 · see citing works
Gut Microbiome and Obesity: A Plausible Explanation for Obesity
Sanmiguel, C. P., Gupta, A., & Mayer, E. A. (2015) · Current Obesity Reports · doi:10.1007/s13679-015-0152-0 · Cited by 203 · see citing works
Brain-gut-microbiota axis: challenges for translation in psychiatry
Kelly, J. R., Clarke, G. A., Cryan, J. F., & Dinan, T. G. (2016) · Annals of Epidemiology · doi:10.1016/j.annepidem.2016.02.008 · Cited by 200 · see citing works
The microbiome regulates amygdala-dependent fear recall
Hoban, A. E., Stilling, R. M., Moloney, G., Shanahan, F., Dinan, T. G., Clarke, G., & Cryan, J. F. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.100 · Cited by 197 · see citing works
Gastroenterology Issues in Schizophrenia: Why the Gut Matters
Severance, E. G., Prandovszky, E., Castiglione, J., & Yolken, R. H. (2015) · Current Psychiatry Reports · doi:10.1007/s11920-015-0574-0 · Cited by 196 · see citing works
Gut microbiota in atherosclerosis: focus on trimethylamine N‐oxide
Zhu, Y., Li, Q., & Jiang, H. (2020) · Apmis · doi:10.1111/apm.13038 · Cited by 204 · see citing works
Gut microbiota in hypertension
José, P. A., & Raj, D. S. (2015) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000149 · Cited by 187 · see citing works
Gut Microbiota: The Brain Peacekeeper
Mu, C., Yang, Y., & Zhu, W. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00345 · Cited by 188 · see citing works
Gastrointestinal symptoms and autism spectrum disorder: links and risks – a possible new overlap syndrome
Wasilewska, J., & Klukowski, M. (2015) · Pediatric Health Medicine and Therapeutics · doi:10.2147/phmt.s85717 · Cited by 184 · see citing works
The Gut–Brain Axis and Its Relation to Parkinson’s Disease: A Review
Klann, E. M., Dissanayake, U., Gurrala, A., Farrer, M. J., Shukla, A. W., Ramirez‐Zamora, A., Mai, V., & Vedam‐Mai, V. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.782082 · Cited by 191 · see citing works
Microbial regulation of microRNA expression in the amygdala and prefrontal cortex
Hoban, A. E., Stilling, R. M., M. Moloney, G., Moloney, R. D., Shanahan, F., Dinan, T. G., Cryan, J. F., & Clarke, G. (2017) · Microbiome · doi:10.1186/s40168-017-0321-3 · Cited by 177 · see citing works
Evidence for interplay among antibacterial-induced gut microbiota disturbance, neuro-inflammation, and anxiety in mice
Jang, H.-M., Lee, H.-J., Jang, S.-E., Han, M. J., & Kim, D.-H. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0042-3 · Cited by 181 · see citing works
Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour
Clarke, G., O'Mahony, S., Dinan, T., & Cryan, J. (2014) · Acta Paediatrica · doi:10.1111/apa.12674 · Cited by 179 · see citing works
Impacts of foodborne inorganic nanoparticles on the gut microbiota-immune axis: potential consequences for host health
Lamas, B., Breyner, N. M., & Houdeau, É. (2020) · Particle and Fibre Toxicology · doi:10.1186/s12989-020-00349-z · Cited by 177 · see citing works
Genomics of schizophrenia: time to consider the gut microbiome?
Dinan, T. G., Borre, Y. E., & Cryan, J. F. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.93 · Cited by 175 · see citing works
Gut microbiota and dietary patterns in children with attention-deficit/hyperactivity disorder
Wang, L., Yang, C., Chou, W., Lee, M., Chou, M., Kuo, H., Yeh, Y., Lee, S.-Y., Huang, L., & Li, S. (2019) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-019-01352-2 · Cited by 174 · see citing works
Gut Microbiota, Nitric Oxide, and Microglia as Prerequisites for Neurodegenerative Disorders
Tse, J. K. Y. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00176 · Cited by 172 · see citing works
The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
Malan-Muller, S., Valles-Colomer, M., Raes, J., Lowry, C. A., Seedat, S., & Hemmings, S. M. J. (2018) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2017.0077 · Cited by 161 · see citing works
From Probiotics to Psychobiotics: Live Beneficial Bacteria Which Act on the Brain-Gut Axis
Bermúdez‐Humarán, L. G., Salinas, E., Ortíz, G. G., Ramírez-Jirano, L. J., Morales, J. A., & Bitzer-Quintero, O. K. (2019) · Nutrients · doi:10.3390/nu11040890 · Cited by 172 · see citing works
The Role of Gut Dysbiosis in the Pathophysiology of Neuropsychiatric Disorders
Anand, N., Gorantla, V. R., & Chidambaram, S. B. (2022) · Cells · doi:10.3390/cells12010054 · Cited by 185 · see citing works
Bacterial Metabolites of Human Gut Microbiota Correlating with Depression
Averina, O. V., Zorkina, Y., Yunes, R. А., Kovtun, A. S., Ushakova, V. M., Morozova, A. Y., Kostyuk, G. P., Даниленко, В. Н., & Chekhonin, V. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239234 · Cited by 166 · see citing works
Effects of exposure to bisphenol A and ethinyl estradiol on the gut microbiota of parents and their offspring in a rodent model
Javurek, A. B., Spollen, W. G., Johnson, S. A., Bivens, N. J., Bromert, K. H., Givan, S. A., & Rosenfeld, C. S. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1234657 · Cited by 160 · see citing works
Gut microbiota and attention deficit hyperactivity disorder: new perspectives for a challenging condition
Cenit, M. C., Nuevo, I. C., Codoñer-Franch, P., Dinan, T. G., & Sanz, Y. (2017) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-0969-z · Cited by 163 · see citing works
Self-citation
Mental health and periodontal and peri‐implant diseases
Ball, J., & Darby, I. B. (2022) · Periodontology 2000 · doi:10.1111/prd.12452 · Cited by 180 · see citing works
Stress-Induced Visceral Pain: Toward Animal Models of Irritable-Bowel Syndrome and Associated Comorbidities
Moloney, R. D., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00015 · Cited by 167 · see citing works

EPIGENETIC IMPACT OF GUT MICROBIOTA ON HOST NEUROBIOLOGY AND BRIDGING THE GUT BRAIN AXIS
Risha Shiny, T., & Punitha, S. C. (2026) · Iterative International Publishers eBooks · doi:10.58532/nbennur3174c4
The microbiota-gut-brain axis: An emerging role for the epigenome
Louwies, T., Johnson, A. C., Orock, A. M., Yuan, T., & Meerveld, B. G. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219891690 · Cited by 66 · see citing works
Microbiota, the brain and epigenetics
Louwies, T., Johnson, A. C., Orock, A. M., Yuan, T., & Meerveld, B. G. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816843-1.00026-6
The gut–brain–epigenetic axis in brain health
Louwies, T. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-15572-7.00057-7
The brain’s Geppetto—microbes as puppeteers of neural function and behaviour?
Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2015) · Journal of NeuroVirology · doi:10.1007/s13365-015-0355-x · Cited by 41 · see citing works

Authors: Stilling, R. M., Dinan, T. G., & Cryan, J. F.
Affiliations: APC Microbiome Institute (IE)
University College Cork (IE)
Corresponding author: Cryan, J. F.
ORCID: Stilling, R. M.
Dinan, T. G.
Cryan, J. F.
Venue: Genes, Brain and Behavior
Publisher: Wiley
Published: 2013-12-27
Volume: 13
Issue: 1
Pages: 69-86
ISSN: 1601-183X (ISSN-L)
1601-1848
DOI: 10.1111/gbb.12109
OpenAlex: W1490861410
Cited by: 637
References: 191
Citations by year: 2026: 36 · 2025: 44 · 2024: 46 · 2023: 47 · 2022: 65 · 2021: 59 · 2020: 68 · 2019: 45 · 2018: 50 · 2017: 55 · 2016: 50 · 2015: 47 · 2014: 25
FWCI: 3.83
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Genes Brain & Behavior (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: microbiota-gut-brain axis, gut-brain axis, epigenetics, host-microbe interactions, chromatin plasticity, gene-environment interaction, depression, anxiety, irritable bowel syndrome, autism spectrum disorder, neurodevelopmental disorders, microbial metabolites, behavior
MeSH terms: Animals, Brain, Genes, Bacterial, Humans, Intestines, Stress, Psychological, Chromatin Assembly and Disassembly, Epigenesis, Genetic, Host-Pathogen Interactions, Gene-Environment Interaction, Microbiota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks