Bacterial Peptidoglycans from Microbiota in Neurodevelopment and Behavior
Open accessAbstract
It is increasingly recognized that the gut microbiota profoundly influences many aspects of host development and physiology, including the modulation of brain development and behavior. However, the precise molecular mechanisms and signaling pathways involved in communication between the microbiota and the developing brain remain to be fully elucidated. Germline-encoded pattern-recognition receptors (PRRs) that recognize conserved microbial molecular signatures such as bacterial surface molecules (e.g., peptidoglycans, PGNs) have emerged as potential key regulators of gut microbiota-brain interactions. We highlight current evidence supporting multiple and essential roles for PGNs and their sensing molecules beyond innate immunity, extending to neurodevelopment and behavior. In addition, the possible implications of the PGN signaling pathway for the pathogenesis of neurodevelopmental disorders such as autism spectrum disorder (ASD) are considered.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Peptidoglycan may directly impact neuronal function.
“These findings suggest that PGN may directly impact neuronal function [83,84].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [84]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
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 · cited 1× · see citing works
“[33]).”
Host microbiota constantly control maturation and function of microglia in the CNS
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4030 · Cited by 3,569 · see citing works
The human microbiome: at the interface of health and disease
Cho, I., & Blaser, M. J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3182 · Cited by 3,449 · see citing works
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283 · 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
Self-citationThe Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication
Silva, Y. P., Bernardi, A., & Frozza, R. L. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00025 · Cited by 3,043 · see citing works
Gut microbiota functions: metabolism of nutrients and other food components
Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., & Tuohy, K. (2018) · European Journal of Nutrition · doi:10.1007/s00394-017-1445-8 · Cited by 2,878 · see citing works
A subcellular map of the human proteome
Thul, P. J., Åkesson, L., Wiking, M., Mahdessian, D., Geladaki, A., Ait Blal, H., Alm, T., Asplund, A., Björk, L., Breckels, L. M., et al. (2017) · Science · doi:10.1126/science.aal3321 · Cited by 2,813 · see citing works
Animals in a bacterial world, a new imperative for the life sciences
McFall‐Ngai, M., Hadfield, M. G. ., Bosch, T. C. G., Carey, H. V., Domazet‐Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218525110 · Cited by 2,741 · see citing works
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
The gut microbiota influences blood-brain barrier permeability in mice
Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A., Bakocevic, N., Ng, L. G., Kundu, P., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009759 · Cited by 2,530 · see citing works
Neurotrophin regulation of neural circuit development and function
Park, H., & Poo, M.-M. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3379 · Cited by 2,060 · see citing works
Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans
Sender, R., Fuchs, S., & Milo, R. (2016) · Cell · doi:10.1016/j.cell.2016.01.013 · Cited by 2,050 · see citing works
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
The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism
Frost, G., Sleeth, M. L., Sahuri-Arisoylu, M., Lizarbe, B., Cerdan, S., Brody, L., Anastasovska, J., Ghourab, S., Hankir, M., Zhang, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4611 · Cited by 1,771 · see citing works
Unusual brain growth patterns in early life in patients with autistic disorder: An MRI study
Courchesne, E., Karns, C. M., Davis, H. R., Ziccardi, R., Carper, R. A., Tigue, Z. D., Chisum, H. J., Moses, P., Pierce, K., Lord, C., et al. (2001) · Neurology · doi:10.1212/wnl.57.2.245 · Cited by 1,487 · see citing works
Inferences, questions and possibilities in Toll-like receptor signalling
Beutler, B. (2004) · Nature · doi:10.1038/nature02761 · Cited by 1,458 · see citing works
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
Maternal immune activation: Implications for neuropsychiatric disorders
Estes, M. L., & McAllister, A. K. (2016) · Science · doi:10.1126/science.aag3194 · Cited by 1,206 · see citing works
Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring
Buffington, S. A., Di Prisco, G. V., Auchtung, T. A., Ajami, N. J., Petrosino, J. F., & Costa-Mattioli, M. (2016) · Cell · doi:10.1016/j.cell.2016.06.001 · Cited by 1,163 · see citing works
Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity
Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., & Weiser, J. N. (2010) · Nature Medicine · doi:10.1038/nm.2087 · Cited by 1,154 · see citing works
Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis
Bouskra, D., Brézillon, C., Bérard, M., Werts, C., Varona, R., Boneca, I. G., & Eberl, G. (2008) · Nature · doi:10.1038/nature07450 · Cited by 1,107 · 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
Adams, J. B., Johansen, L. J., Powell, L. D., Quig, D., & Rubin, R. A. (2011) · BMC Gastroenterology · doi:10.1186/1471-230x-11-22 · Cited by 1,076 · 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
A gut-brain neural circuit for nutrient sensory transduction
Kaelberer, M. M., Buchanan, K. L., Klein, M. E., Barth, B. B., Montoya, M. M., Shen, X., & Bohórquez, D. V. (2018) · Science · doi:10.1126/science.aat5236 · Cited by 932 · see citing works
Maternal Infection Requiring Hospitalization During Pregnancy and Autism Spectrum Disorders
Atladóttir, H. Ó., Thorsen, P., Østergaard, L., Schendel, D. E., Lemcke, S., Abdallah, M., & Parner, E. T. (2010) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1006-y · Cited by 916 · see citing works
Sgritta, M., Dooling, S. W., Buffington, S. A., Momin, E. N., Francis, M. B., Britton, R. A., & Costa-Mattioli, M. (2019) · Neuron · doi:10.1016/j.neuron.2018.11.018 · Cited by 865 · see citing works
Role of the microbiome in human development
Domínguez-Bello, M. G., Godoy‐Vitorino, F., Knight, R. D., & Blaser, M. J. (2019) · Gut · doi:10.1136/gutjnl-2018-317503 · Cited by 786 · see citing works
Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner
Thion, M. S., Low, D., Silvin, A., Chen, J., Grisel, P., Schulte-Schrepping, J., Blecher, R., Ulas, T., Squarzoni, P., Hoeffel, G., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.042 · Cited by 779 · see citing works
A Neural Circuit for Gut-Induced Reward
Han, W., Téllez, L. A., Perkins, M. H., Pérez-Martínez, I. O., Qu, T., Ferreira, J. G. P., Ferreira, T. L., Quinn, D., Liu, Z.-W., Gao, X., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.049 · Cited by 739 · see citing works
Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring
Kim, S., Kim, H., Yim, Y. S., Ha, S., Atarashi, K., Tan, T. G., Longman, R. S., Honda, K., Littman, D. R., Choi, G. B., et al. (2017) · Nature · doi:10.1038/nature23910 · Cited by 678 · see citing works
NOD proteins: regulators of inflammation in health and disease
Philpott, D. J., Sorbara, M. T., Robertson, S. J., Croitoru, K., & Girardin, S. E. (2014) · Nature Reviews Immunology · doi:10.1038/nri3565 · Cited by 668 · see citing works
Hazlett, H. C., Poe, M., Gerig, G., Smith, R. G., Provenzale, J., Ross, A., Gilmore, J., & Piven, J. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.12.1366 · Cited by 665 · see citing works
Regulation of prefrontal cortex myelination by the microbiota
Hoban, A. E., Stilling, R. M., Ryan, F. J., Shanahan, F., Dinan, T. G., Claesson, M. J., Clarke, G., & Cryan, J. F. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.42 · Cited by 635 · see citing works
Innate immune recognition of the microbiota promotes host-microbial symbiosis
Chu, H., & Mazmanian, S. K. (2013) · Nature Immunology · doi:10.1038/ni.2635 · Cited by 630 · see citing works
Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder
Vuong, H. E., & Hsiao, E. Y. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.024 · Cited by 595 · see citing works
Gut Microbe to Brain Signaling: What Happens in Vagus…
Fülling, C., Dinan, T. G., & Cryan, J. F. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.008 · Cited by 590 · see citing works
Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity
Just, M. A., Keller, T. A., Malave, V. L., Kana, R. K., & Varma, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.02.007 · Cited by 578 · see citing works
Gastrointestinal Problems in Children with Autism, Developmental Delays or Typical Development
Chaidez, V., Hansen, R. L., & Hertz-Picciotto, I. (2014) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-013-1973-x · Cited by 528 · see citing works
Maternal infection and immune involvement in autism
Patterson, P. H. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.03.001 · Cited by 520 · see citing works
Toll-like receptor signaling in neural plasticity and disease
Okun, E., Griffioen, K. J. S., & Mattson, M. P. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.005 · Cited by 513 · see citing works
Moresco, E. M. Y., LaVine, D., & Beutler, B. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.039 · Cited by 500 · see citing works
Prefrontal Cortex and Social Cognition in Mouse and Man
Bicks, L. K., Koike, H., Akbarian, S., & Morishita, H. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01805 · Cited by 491 · see citing works
Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice
Kimura, I., Miyamoto, J., Ohue‐Kitano, R., Watanabe, K., Yamada, T., Onuki, M., Aoki, R., Isobe, Y., Kashihara, D., Inoue, D., et al. (2020) · Science · doi:10.1126/science.aaw8429 · Cited by 488 · see citing works
Microbiota and the social brain
Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G., & Cryan, J. F. (2019) · Science · doi:10.1126/science.aar2016 · Cited by 462 · see citing works
The idiosyncratic brain: distortion of spontaneous connectivity patterns in autism spectrum disorder
Hahamy, A., Behrmann, M., & Malach, R. (2015) · Nature Neuroscience · doi:10.1038/nn.3919 · Cited by 416 · see citing works
Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences
Royet, J., & Dziarski, R. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1620 · Cited by 411 · 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
Peptidoglycan recognition proteins: modulators of the microbiome and inflammation
Royet, J., Gupta, D., & Dziarski, R. (2011) · Nature reviews. Immunology · doi:10.1038/nri3089 · Cited by 388 · see citing works
The Landscape of Genetic Content in the Gut and Oral Human Microbiome
Tierney, B. T., Yang, Z., Luber, J. M., Beaudin, M., Wibowo, M. C., Baek, C., Mehlenbacher, E., Patel, C. J., & Kostic, A. D. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.07.008 · Cited by 346 · see citing works
Microbiomes as sources of emergent host phenotypes
Lynch, J. B., & Hsiao, E. Y. (2019) · Science · doi:10.1126/science.aay0240 · Cited by 339 · see citing works
Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders
Lee, B. K., Magnusson, C., Gardner, R. M., Blomström, Å., Newschaffer, C. J., Burstyn, I., Karlsson, H., & Dalman, C. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.09.001 · Cited by 337 · see citing works
Immune signalling in neural development, synaptic plasticity and disease
Boulanger, L. M., & Shatz, C. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1428 · Cited by 334 · see citing works
The ASD Living Biology: from cell proliferation to clinical phenotype
Courchesne, E., Pramparo, T., Gazestani, V. H., Lombardo, M. V., Pierce, K., & Lewis, N. E. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0056-y · Cited by 333 · see citing works
Gacias, M., Gaspari, S., Santos, P.-M. G., Tamburini, S., Andrade, M., Zhang, F., Shen, N., Tolstikov, V., Kiebish, M. A., Dupree, J. L., et al. (2016) · eLife · doi:10.7554/elife.13442 · Cited by 308 · see citing works
Imprinting of the immune system by the microbiota early in life
Al Nabhani, Z., & Eberl, G. (2020) · Mucosal Immunology · doi:10.1038/s41385-020-0257-y · Cited by 301 · see citing works
Maternal Immune Activation and Neuropsychiatric Illness: A Translational Research Perspective
Brown, A. S., & Meyer, U. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2018.17121311 · Cited by 285 · see citing works
Ma, Y., Li, J., Chiu, I., Wang, Y., Sloane, J., Lu, J.-N., Kosaras, B., Sidman, R., Volpe, J., & Vartanian, T. (2006) · Journal of Cell Biology · doi:10.1083/jcb.200606016 · Cited by 284 · see citing works
The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior
Arentsen, T., Qian, Y., Gkotzis, S., Femenia, T., Wang, T., Udekwu, K., Forssberg, H., & Diaz Heijtz, R. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.182 · Cited by 280 · see citing works
IL-17a promotes sociability in mouse models of neurodevelopmental disorders
Reed, M. D., Yim, Y. S., Wimmer, R. D., Kim, H., Ryu, C., Welch, G. M., Andina, M., King, H. O., Waisman, A., Halassa, M. M., et al. (2020) · Nature · doi:10.1038/s41586-019-1843-6 · Cited by 274 · see citing works
Temporal development of the infant gut microbiome
Moore, R. E., & Townsend, S. D. (2019) · Open Biology · doi:10.1098/rsob.190128 · Cited by 266 · see citing works
The fetal origins of mental illness
al-Haddad, B. J. S., Oler, E., Armistead, B., Elsayed, N. A., Weinberger, D. R., Bernier, R., Burd, I. D., Kapur, R. P., Jacobsson, B., Wang, C., et al. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2019.06.013 · Cited by 265 · see citing works
Wang, L. W., Tancredi, D. J., & Thomas, D. W. (2011) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e31821bd06a · Cited by 258 · see citing works
The Microbiome in Psychology and Cognitive Neuroscience
Sarkar, A., Harty, S., Lehto, S. M., Moeller, A. H., Dinan, T. G., Dunbar, R., Cryan, J. F., & Burnet, P. W. J. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.04.006 · Cited by 231 · see citing works
Synapse elimination and learning rules co-regulated by MHC class I H2-Db
Lee, H., Brott, B. K., Kirkby, L. A., Adelson, J. D., Cheng, S., Feller, M. B., Datwani, A., & Shatz, C. J. (2014) · Nature · doi:10.1038/nature13154 · Cited by 228 · see citing works
Inter-Regional Brain Communication and Its Disturbance in Autism
Schipul, S. E., Keller, T. A., & Just, M. A. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00010 · Cited by 223 · see citing works
Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis
Okun, E., Griffioen, K. J. S., Barak, B., Roberts, N. J., Castro, K., Pita, M. A., Cheng, A., Mughal, M. R., Wan, R., Ashery, U., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005807107 · Cited by 207 · see citing works
Toll-Like Receptor 3 Is a Negative Regulator of Embryonic Neural Progenitor Cell Proliferation
Lathia, J. D., Okun, E., Tang, S., Griffioen, K. J. S., Cheng, A., Mughal, M. R., Laryea, G. N., Selvaraj, P., ffrench‐Constant, C., Magnus, T., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2140-08.2008 · Cited by 206 · see citing works
NOD1 and NOD2 in inflammation, immunity and disease
Mukherjee, T., Hovingh, E. S., Foerster, E. G., Abdel‐Nour, M., Philpott, D. J., & Girardin, S. E. (2018) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2018.12.022 · Cited by 202 · see citing works
Peptidoglycan Muropeptides: Release, Perception, and Functions as Signaling Molecules
Irazoki, O., Hernández, S. B., & Cava, F. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00500 · Cited by 200 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Programming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
Codagnone, M. G., Spichak, S., O’Mahony, S. M., O’Leary, O. F., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.014 · Cited by 198 · see citing works
Heijtz, R. D. (2016) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2016.04.012 · Cited by 193 · see citing works
The composition of sleep-promoting factor isolated from human urine.
Krueger, J. M., Pappenheimer, J. R., & Karnovsky, M. L. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68088-9 · Cited by 192 · see citing works
The development of intestinal lymphoid tissues at the interface of self and microbiota
Eberl, G., & Lochner, M. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.114 · Cited by 149 · see citing works
Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis
Schrijver, I. A. (2001) · Brain · doi:10.1093/brain/124.8.1544 · Cited by 143 · see citing works
Small talk: microbial metabolites involved in the signaling from microbiota to brain
Caspani, G., & Swann, J. R. (2019) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2019.08.001 · Cited by 138 · see citing works
Evidence for a Developmental Role for TLR4 in Learning and Memory
Okun, E., Barak, B., Madar, R., Rothman, S. M., Griffioen, K. J. S., Roberts, N. J., Castro, K., Mughal, M. R., Pita, M. A., Stranahan, A. M., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047522 · Cited by 131 · see citing works
Prenatal and postnatal contributions of the maternal microbiome on offspring programming
Jašarević, E., & Bale, T. L. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100797 · Cited by 127 · see citing works
Emerging roles for the intestinal microbiome in epilepsy
Lum, G. R., Olson, C. A., & Hsiao, E. Y. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104576 · Cited by 123 · see citing works
Krueger, J. M., & Opp, M. R. (2016) · International Review of Neurobiology · doi:10.1016/bs.irn.2016.07.003 · Cited by 120 · see citing works
Martin, S. A., Karnovsky, M. L., Krueger, J. M., Pappenheimer, J. R., & BIEMANN, K. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90795-7 · Cited by 114 · see citing works
TLR2 activation inhibits embryonic neural progenitor cell proliferation
Okun, E., Griffioen, K. J. S., Son, T. G., Lee, J., Roberts, N. J., Mughal, M. R., Hutchison, E. R., Cheng, A., Arumugam, T. V., Lathia, J. D., et al. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06778.x · Cited by 110 · see citing works
Huang, Z., Wang, J., Xu, X., Wang, H., Qiao, Y., Chu, W. C., Xu, S., Chai, L., Cottier, F., Pavelka, N., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0381-1 · Cited by 107 · see citing works
McFall‐Ngai, M., Nyholm, S. V., & Castillo, M. G. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.11.003 · Cited by 103 · see citing works
Neuroinflammation in preterm babies and autism spectrum disorders
Bokobza, C., Steenwinckel, J. V., Mani, S., Mezger, V., Fleiss, B., & Gressèns, P. (2018) · Pediatric Research · doi:10.1038/s41390-018-0208-4 · Cited by 103 · see citing works
Humann, J., Mann, B., Gao, G., Moresco, P., Ramahi, J., Loh, L. N., Farr, A., Hu, Y., Durick-Eder, K., Fillon, S. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.02.009 · Cited by 100 · see citing works
Bacterial Peptidoglycan as a Driver of Chronic Brain Inflammation
Laman, J. D., Hart, B. A. ‘., Power, C., & Dziarski, R. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.11.006 · Cited by 89 · see citing works
Sterka, D. G., Rati, D. M., & Marriott, I. (2005) · Glia · doi:10.1002/glia.20286 · Cited by 83 · see citing works
PirB regulates a structural substrate for cortical plasticity.
Djurisic, M., Vidal, G. S., Mann, M., Aharon, A., Kim, T., Ferrao Santos, A., Zuo, Y., Hübener, M., & Shatz, C. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321092110 · Cited by 79 · see citing works
Toll-like receptor 4 restricts retinal progenitor cell proliferation
Shechter, R., Ronen, A., Rolls, A., London, A., Bakalash, S., Young, M. J., & Schwartz, M. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200804010 · Cited by 77 · see citing works
The biology of bacterial peptidoglycans and their impact on host immunity and physiology
Wheeler, R., Chevalier, G., Eberl, G., & Boneca, I. G. (2014) · Cellular Microbiology · doi:10.1111/cmi.12304 · Cited by 69 · see citing works
Nod-like receptors are critical for gut-brain axis signalling in mice
Pusceddu, M. M., Barboza, M., Keogh, C. E., Schneider, M., Stokes, P., Sladek, J. A., Kim, H. J. D., Torres‐Fuentes, C., Goldfild, L. R., Gillis, S. E., et al. (2019) · The Journal of Physiology · doi:10.1113/jp278640 · Cited by 69 · see citing works
Radulescu, C. I., Garcia‐Miralles, M., Sidik, H., Bardile, C. F., Yusof, N. A. B. M., Lee, H. U., Ho, E. X. P., Chu, C. W., Layton, E., Low, D., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.02.011 · Cited by 68 · see citing works
Sterka, D. G., & Marriott, I. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.06.009 · Cited by 67 · see citing works
Needham, B. D., Tang, W., & Wu, W. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22581 · Cited by 59 · see citing works
Rehman, A., Taishi, P., Fang, J., Majde, J. A., & Krueger, J. M. (2001) · Cytokine · doi:10.1006/cyto.2000.0800 · Cited by 55 · see citing works
The Innate Immune Receptor PGRP-LC Controls Presynaptic Homeostatic Plasticity
Harris, N., Braiser, D. J., Dickman, D. K., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.049 · Cited by 54 · see citing works
Peptidoglycan recognition protein genes and risk of Parkinson's disease
Goldman, S. M., Kamel, F., Ross, G. W., Jewell, S. A., Marras, C., Hoppin, J. A., Umbach, D. M., Bhudhikanok, G. S., Meng, C., Korell, M., et al. (2014) · Movement Disorders · doi:10.1002/mds.25895 · Cited by 52 · see citing works
Developmental Signatures of Microbiota-Derived Metabolites in the Mouse Brain
Swann, J. R., Spitzer, S. O., & Heijtz, R. D. (2020) · Metabolites · doi:10.3390/metabo10050172 · Cited by 52 · see citing works
Bacterial peptidoglycans as novel signaling molecules from microbiota to brain
Tosoni, G., Conti, M., & Heijtz, R. D. (2019) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2019.08.003 · Cited by 50 · see citing works
Molinaro, R., Mukherjee, T., Flick, R., Philpott, D. J., & Girardin, S. E. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007997 · Cited by 49 · see citing works
Arentsen, T., Khalid, R., Qian, Y., & Diaz Heijtz, R. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.09.014 · Cited by 42 · see citing works
Self-citationThe Pleiotropic MET Receptor Network: Circuit Development and the Neural-Medical Interface of Autism
Eagleson, K., Xie, Z., & Levitt, P. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.035 · Cited by 31 · see citing works
Kuniomi Ishimori and the first discovery of sleep-inducing substances in the brain
Kubota, K. (1989) · Neuroscience Research · doi:10.1016/0168-0102(89)90041-2 · Cited by 29 · see citing works
Somnogenic activity of O-acetylated and dimeric muramyl peptides
Johannsen, L., Rosenthal, R. S., Martin, S. A., Cady, A. B., Obál, F., Guinand, M., & Krueger, J. M. (1989) · Infection and Immunity · doi:10.1128/iai.57.9.2726-2732.1989 · Cited by 28 · see citing works
Somnogenic activity of muramyl peptide-derived immune adjuvants
Johannsen, L., Orál, F., Kapás, L., Kovalzon, V. M., & Krueger, J. M. (1994) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(94)90066-3 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
From gut microbiota to host appetite: gut microbiota-derived metabolites as key regulators
Han, H., Yi, B., Zhong, R., Wang, M., Zhang, S., Ma, J., Yin, Y., Yin, J., Chen, L., & Zhang, H. (2021) · Microbiome · doi:10.1186/s40168-021-01093-y · Cited by 292 · see citing works
Inflammatory pathways in Alzheimer’s disease mediated by gut microbiota
Qian, X.-H., Song, X.-X., Liu, X.-L., Chen, S.-D., & Tang, H.-D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101317 · Cited by 153 · see citing works
Immunological classification of tumor types and advances in precision combination immunotherapy
Ren, X., Guo, S., Guan, X., Kang, Y., Liu, J., & Yang, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.790113 · Cited by 62 · see citing works
The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders
Młynarska, E., Barszcz, E., Budny, E., Gajewska, A., Kopeć, K., Wasiak, J., Rysz, J., & Franczyk, B. (2025) · Nutrients · doi:10.3390/nu17071135 · Cited by 44 · see citing works
RISING STARS: Bumps and bacteria: influence of the maternal microbiota on pregnancy outcomes
Willmott, T., & Cottrell, E. C. (2024) · Journal of Endocrinology · doi:10.1530/joe-23-0360
- Authors
- Gonzalez-Santana, A., & Diaz Heijtz, R.
- Venue
- Trends in Molecular Medicine
- Publisher
- Elsevier BV
- Published
- 2020-08
- Volume
- 26
- Issue
- 8
- Pages
- 729-743
- ISSN
- 1471-4914 (ISSN-L)
- OpenAlex
- W3033081102
- Cited by
- 118
- References
- 109
- Citations by year
- 2026: 17 · 2025: 25 · 2024: 23 · 2023: 25 · 2022: 15 · 2021: 11 · 2020: 2
- FWCI
- 1.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Trends in Molecular Medicine (acceptedVersion, other-oa)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc)
- Funders
- Stiftelsen Olle Engkvist Byggmästare
- Vetenskapsrådet
- Hjärnfonden
- Stiftelsen Frimurare Barnhuset i Stockholm
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- bacterial peptidoglycan, gut microbiota, microbiota-brain axis, brain development, behavior, pattern recognition receptors, innate immunity, neurodevelopmental disorders, autism spectrum disorder
- MeSH terms
- Gastrointestinal Microbiome, Animals, Bacteria, Brain, Humans, Peptidoglycan, Signal Transduction, Receptors, Pattern Recognition, 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
