The microbiota regulates murine inflammatory responses to toxin-induced CNS demyelination but has minimal impact on remyelination
Open accessAbstract
Significance: People with multiple sclerosis have a microbiota distinct from healthy controls, and there is growing interest in how these differences might contribute to the onset and progression of CNS autoimmunity. However, the impact that the microbiota may also have on the endogenous regeneration of myelin—remyelination—has not yet been explored. Here we show that inflammatory responses during remyelination depend upon the microbiota, being modulated by antibiotics or probiotics or in germ-free mice. In contrast, these interventions had minimal impact on the activity of oligodendrocyte progenitor cells, with only supratherapeutic doses of antibiotics having an inhibitory effect. Our results suggest that endogenous CNS remyelination is largely resilient to interventions that modify the microbiota.
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?
OPC differentiation and extent of remyelination are unaltered in cuprizone-treated GF mice compared with their SPF counterparts.
“However, the OPC differentiation and extent of remyelination were unaltered in cuprizone-treated GF mice when compared to their SPF counterparts.269”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [269]
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
1 retracted
Kouchaki, E., Tamtaji, O. R., Salami, M., Bahmani, F., Daneshvar Kakhaki, R., Akbari, E., Tajabadi-Ebrahimi, M., Jafari, P., & Asemi, Z. (2017) · Clinical Nutrition · doi:10.1016/j.clnu.2016.08.015 · Cited by 317 · see citing works
RetractedA Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.018 · Cited by 5,493 · see citing works
CellProfiler: image analysis software for identifying and quantifying cell phenotypes
Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-10-r100 · Cited by 5,077 · see citing works
Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease
Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., Challis, C., Schretter, C. E., Rocha, S., Gradinaru, V., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.018 · Cited by 3,622 · see citing works
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
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979 · see citing works
Identification of a unique TGF-β–dependent molecular and functional signature in microglia
Butovsky, O., Jedrychowski, M. P., Moore, C. S., Cialic, R., Lanser, A. J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P. M., Doykan, C. E., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3599 · Cited by 2,543 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
New tools for studying microglia in the mouse and human CNS
Bennett, M. L., Bennett, F. C., Liddelow, S. A., Ajami, B., Zamanian, J. L., Fernhoff, N. B., Mulinyawe, S. B., Bohlen, C. J., Adil, A., Tucker, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525528113 · Cited by 1,804 · see citing works
M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination
Miron, V. E., Boyd, A., Zhao, J.-W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3469 · Cited by 1,788 · see citing works
Self-citationProinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis
Lee, Y. K., Menezes, J. S., Umesaki, Y., & Mazmanian, S. K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000082107 · Cited by 1,323 · see citing works
Alterations of the human gut microbiome in multiple sclerosis
Jangi, S., Gandhi, R., Cox, L. M., Li, N., von Glehn, F., Yan, R., Patel, B., Mazzola, M. A., Liu, S., Glanz, B. L., et al. (2016) · Nature Communications · doi:10.1038/ncomms12015 · Cited by 1,307 · see citing works
Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., Wekerle, H., & Krishnamoorthy, G. (2011) · Nature · doi:10.1038/nature10554 · Cited by 1,251 · see citing works
Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls
Chen, J., Chia, N., Kalari, K. R., Yao, J. Z., Novotna, M., Paz Soldan, M. M., Luckey, D. H., Marietta, E. V., Jeraldo, P. R., Chen, X., et al. (2016) · Scientific Reports · doi:10.1038/srep28484 · Cited by 933 · see citing works
Berer, K., Gerdes, L. A., Cekanaviciute, E., Jia, X., Xiao, L., Xia, Z., Liu, C., Klotz, L., Stauffer, U., Baranzini, S. E., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711233114 · Cited by 933 · see citing works
Myelin Impairs CNS Remyelination by Inhibiting Oligodendrocyte Precursor Cell Differentiation
Kotter, M. R., Li, W.-W., Zhao, C., & Franklin, R. J. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2615-05.2006 · Cited by 768 · see citing works
Self-citationNG2-Positive Oligodendrocyte Progenitor Cells in Adult Human Brain and Multiple Sclerosis Lesions
Chang, A., Nishiyama, A., Peterson, J. W., Prineas, J. W., & Trapp, B. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06404.2000 · Cited by 711 · see citing works
Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion
Yadav, H., Lee, J.-H., Lloyd, J., Walter, P., & Rane, S. G. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.452516 · Cited by 709 · see citing works
Zawadzka, M., Rivers, L. E., Fancy, S. P. J., Zhao, C., Tripathi, R., Jamen, F., Young, K., Goncharevich, A., Pohl, H., Rizzi, M., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.04.002 · Cited by 650 · see citing works
Self-citationRejuvenation of Regeneration in the Aging Central Nervous System
Ruckh, J. M., Zhao, J.-W., Shadrach, J. L., van Wijngaarden, P., Rao, T. N., Wagers, A. J., & Franklin, R. J. M. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2011.11.019 · Cited by 649 · see citing works
Self-citationRegenerating CNS myelin — from mechanisms to experimental medicines
Franklin, R. J. M., & ffrench-Constant, C. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.136 · Cited by 647 · cited 2× · see citing works
“These derive from endogenous OPCs, which migrate to lesions, proliferate, and subsequently differentiate into oligodendrocytes (5, 27).”
Self-citationRegulation 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
Perry, V. H., & Teeling, J. L. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0382-8 · Cited by 599 · see citing works
Role of Gut Commensal Microflora in the Development of Experimental Autoimmune Encephalomyelitis
Ochoa-Repáraz, J., Mielcarz, D. W., Ditrio, L. E., Burroughs, A. R., Foureau, D. M., Haque-Begum, S., & Kasper, L. H. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900747 · Cited by 590 · see citing works
Retinoid X receptor gamma signaling accelerates CNS remyelination
Huang, J. K., Jarjour, A. A., Nait Oumesmar, B., Kerninon, C., Williams, A., Krezel, W., Kagechika, H., Bauer, J., Zhao, C., Evercooren, A. B.-V., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2702 · Cited by 547 · see citing works
Self-citationWolswijk, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-02-00601.1998 · Cited by 498 · see citing works
Möhle, L., Mattei, D., Heimesaat, M. M., Bereswill, S., Fischer, A., Alutis, M., French, T., Hambardzumyan, D., Matzinger, P., Dunay, I. R., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.074 · Cited by 470 · see citing works
Self-citationPraet, J., Guglielmetti, C., Berneman, Z., Van der Linden, A., & Ponsaerts, P. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.004 · Cited by 435 · see citing works
Remyelination protects axons from demyelination-associated axon degeneration
Irvine, K. A., & Blakemore, W. F. (2008) · Brain · doi:10.1093/brain/awn080 · Cited by 420 · see citing works
Kotter, M. R., Setzu, A., Sim, F. J., Van Rooijen, N., & Franklin, R. J. M. (2001) · Glia · doi:10.1002/glia.1085 · Cited by 385 · see citing works
Self-citationHeimesaat, M. M., Bereswill, S., Fischer, A., Fuchs, D., Struck, D., Niebergall, J., Jahn, H.-K., Dunay, I. R., Moter, A., Gescher, D. M., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.12.8785 · Cited by 345 · see citing works
Self-citationDavis, B. M., Salinas‐Navarro, M., Cordeiro, M. F., Moons, L., & Groef, L. D. (2017) · Scientific Reports · doi:10.1038/s41598-017-01747-8 · Cited by 343 · see citing works
Gut dysbiosis impairs recovery after spinal cord injury
Kigerl, K. A., Hall, J. C. E., Wang, L., Mo, X. M., Yu, Z., & Popovich, P. G. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20151345 · Cited by 338 · see citing works
Woodruff, R. H., Fruttiger, M., Richardson, W. D., & Franklin, R. J. M. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2003.10.014 · Cited by 335 · see citing works
Self-citationCentral remyelination restores secure conduction
Smith, K. J., Blakemore, W. F., & MCDONALD, W. I. (1979) · Nature · doi:10.1038/280395a0 · Cited by 332 · see citing works
Central nervous system regeneration is driven by microglia necroptosis and repopulation
Lloyd, A. F., Davies, C. L., Holloway, R. K., Labrak, Y., Ireland, G., Carradori, D., Dillenburg, A., Borger, E., Soong, D., Richardson, J. C., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0418-z · Cited by 316 · cited 1× · see citing works
“This could be explained by the role of the immune system in mediating demyelination as well as remyelination in the lysolecithin and cuprizone models (47, 48, 56, 57).”
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
Immune Modulation of Stem Cells and Regeneration
Aurora, A., & Olson, E. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.06.009 · Cited by 293 · see citing works
Raising the flag on marine alien fouling species
Peters, K., Sink, K. J., & Robinson, T. B. (2017) · Management of Biological Invasions · doi:10.3391/mbi.2017.8.1.01 · Cited by 232 · see citing works
Extensive remyelination of the CNS leads to functional recovery
Duncan, I. D., Brower, A., Kondo, Y., Curlee, J. F., & Schultz, R. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812500106 · Cited by 227 · see citing works
Natrajan, M. S., de la Fuente, A. G., Crawford, A. H., Linehan, E., Núñez, V., Johnson, K. R., Wu, T., Fitzgerald, D. C., Ricote, M., Bielekova, B., et al. (2015) · Brain · doi:10.1093/brain/awv289 · Cited by 217 · see citing works
Self-citationLiu, L., Belkadi, A., Darnall, L., Hu, T., Drescher, C., Cotleur, A. C., Padovani-Claudio, D., He, T., Choi, K., Lane, T. E., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2491 · Cited by 214 · see citing works
Distrutti, E., O’Reilly, J.-A., McDonald, C., Cipriani, S., Renga, B., Lynch, M. A., & Fiorucci, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106503 · Cited by 207 · see citing works
Steelman, A. J., Thompson, J. P., & Li, J. (2012) · Neuroscience Research · doi:10.1016/j.neures.2011.10.002 · Cited by 183 · see citing works
Skin Wound Healing Is Accelerated and Scarless in the Absence of Commensal Microbiota
Canesso, M. C. C., Vieira, A. T., Castro, T. B. R., Schirmer, B. G. D. A., Cisalpino, D., Martins, F. S., Rachid, M. A., Nicoli, J. R., Teixeira, M. M., & Barcelos, L. S. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400625 · Cited by 182 · see citing works
Cornell, R. P., Liljequist, B. L., & Bartizal, K. F. (1990) · Hepatology · doi:10.1002/hep.1840110603 · Cited by 178 · see citing works
Nikodémová, M., Watters, J. J., Jackson, S. J., Yang, S. K., & Duncan, I. D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611907200 · Cited by 159 · see citing works
CXCL10 Triggers Early Microglial Activation in the Cuprizone Model
Clarner, T., Janssen, K., Nellessen, L., Stangel, M., Skripuletz, T., Krauspe, B., Hess, F.-M., Denecke, B., Beutner, C., Linnartz-Gerlach, B., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1401459 · Cited by 150 · see citing works
Zhao, C., Li, W.-W., & Franklin, R. J. M. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.06.008 · Cited by 142 · cited 2× · see citing works
“To create an environment that permits remyelination, endogenous microglia and infiltrating macrophages must clear myelin debris remaining from the disintegrated sheath (12), and also secrete proregenerative factors (10, 11, 13).”
Self-citationPericytes Stimulate Oligodendrocyte Progenitor Cell Differentiation during CNS Remyelination
de la Fuente, A. G., Lange, S., Silva, M. E., González, G. A., Tempfer, H., van Wijngaarden, P., Zhao, C., Canio, L. D., Trost, A., Bieler, L., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.007 · Cited by 129 · see citing works
Self-citationContact with Central Nervous System Myelin Inhibits Oligodendrocyte Progenitor Maturation
Robinson, S., & Miller, R. H. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9466 · Cited by 115 · see citing works
Naito, T., Mulet, C., Castro, C. D., Molinaro, A., Saffarian, A., Nigro, G., Berard, M., Clerc, M., Pedersen, A. B., Sansonetti, P. J., et al. (2017) · mBio · doi:10.1128/mbio.01680-17 · Cited by 112 · see citing works
Arnold, C. P., Merryman, M. S., Harris‐Arnold, A., McKinney, S., Seidel, C. W., Loethen, S., Proctor, K. N., Guo, L., & Alvarado, A. S. (2016) · eLife · doi:10.7554/elife.16793 · Cited by 105 · see citing works
Yuen, T. J., Johnson, K. R., Miron, V. E., Zhao, C., Quandt, J., Harrisingh, M. C., Swire, M., Williams, A., McFarland, H. F., Franklin, R. J. M., et al. (2013) · Brain · doi:10.1093/brain/awt024 · Cited by 80 · see citing works
Self-citationKeough, M. B., Jensen, S. K., & Yong, V. W. (2015) · Journal of Visualized Experiments · doi:10.3791/52679 · Cited by 74 · see citing works
Matsuo, A., Lee, G. C., Terai, K., Takami, K., Hickey, W. F., McGeer, E. G., & McGeer, P. L. (1997) · Europe PMC (PubMed Central) · Cited by 71 · see citing works
Fredua‐Agyeman, M., & Gaisford, S. (2014) · Beneficial Microbes · doi:10.3920/bm2014.0051 · Cited by 71 · see citing works
Ghasemlou, N., Jeong, S. Y., Lacroix, S., & David, S. (2006) · Glia · doi:10.1002/glia.20449 · Cited by 68 · see citing works
Tanaka, T., Murakami, K., Bandô, Y., & Yoshida, S. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12289 · Cited by 63 · see citing works
Baror, R., Neumann, B., Segel, M., Chalut, K. J., Fancy, S. P. J., Schafer, D. P., & Franklin, R. J. M. (2019) · Glia · doi:10.1002/glia.23612 · Cited by 54 · see citing works
Self-citationDefaux, A., Zurich, M.-G., Honegger, P., & Monnet-Tschudi, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.04.053 · Cited by 40 · see citing works
Synthesis and release of L-serine by rat astroglia-rich primary cultures
Verleysdonk, S., & Hamprecht, B. (2000) · Glia · doi:10.1002/(sici)1098-1136(200003)30:1 · Cited by 37 · see citing works
Keough, M. B., Jensen, S. K., & Yong, V. W. (2015) · Journal of Visualized Experiments · doi:10.3791/52679-v · Cited by 17 · see citing works
Treatment of EAE and MS Subjects with Probiotic VSL#3 (P5.320)
Tankou, S. K., Bailey, K., Regev, K., Kivisäkk, P., Ghandi, R., Kirlis, A., Cook, S., Stuart, F., Glanz, B. I., Stankiewicz, J. M., et al. (2016) · Neurology · doi:10.1212/wnl.86.16_supplement.p5.320 · Cited by 5 · see citing works
P0002 : Liver regeneration is not impacted in the absence of intestinal microbiota
Malinka, T., Keogh, A., Kudira, R., Moghadamrad, S., McCoy, C., Stroka, D., Candinas, D., & Beldi, G. (2015) · Journal of Hepatology · doi:10.1016/s0168-8278(15)30210-5 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
The impact of the gut microbiome on extra-intestinal autoimmune diseases
Miyauchi, E., Shimokawa, C., Steimle, A., Desai, M. S., & Ohno, H. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00727-y · Cited by 375 · see citing works
Current understanding of the Alzheimer’s disease-associated microbiome and therapeutic strategies
Seo, D.-O., & Holtzman, D. M. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01146-2 · Cited by 249 · see citing works
Microglia regulation of central nervous system myelin health and regeneration
Kent, S. A., & Miron, V. E. (2024) · Nature Reviews Immunology · doi:10.1038/s41577-023-00907-4 · Cited by 183 · see citing works
Bonomo, R. R., Cook, T. M., Gavini, C. K., White, C. R., Jones, J. R., Bovo, E., Zima, A. V., Brown, I. A., Dugas, L. R., Zakharian, E., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006065117 · Cited by 113 · see citing works
Targeting the gut to treat multiple sclerosis
Ghezzi, L., Cantoni, C., Pinget, G. V., Zhou, Y., & Piccio, L. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143774 · Cited by 114 · see citing works
Oligodendrocytes and Microglia: Key Players in Myelin Development, Damage and Repair
Kalafatakis, I., & Karagogeos, D. (2021) · Biomolecules · doi:10.3390/biom11071058 · Cited by 111 · see citing works
The microbiota–microglia axis in central nervous system disorders
Mossad, O., & Erny, D. (2020) · Brain Pathology · doi:10.1111/bpa.12908 · Cited by 98 · see citing works
How microbiota shape microglial phenotypes and epigenetics
Erny, D., & Prinz, M. (2020) · Glia · doi:10.1002/glia.23822 · Cited by 77 · see citing works
Next-Generation Liquid Biopsies: Embracing Data Science in Oncology
Im, Y. R., Tsui, D. W. Y., Diaz, L. A., & Wan, J. C. M. (2020) · Trends in cancer · doi:10.1016/j.trecan.2020.11.001 · Cited by 67 · see citing works
Blais, L. L., Montgomery, T. L., Amiel, E., Deming, P. B., & Krementsov, D. N. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1943289 · Cited by 45 · see citing works
Targeting gut microbiota: new therapeutic opportunities in multiple sclerosis
Kujawa, D., Łaczmański, Ł., Budrewicz, S. P., Pokryszko‐Dragan, A., & Podbielska, M. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2274126 · Cited by 44 · see citing works
Ji, X., Tian, L., Niu, S., Yao, S., & Qu, C. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.963876 · Cited by 38 · see citing works
A role for microglia in mediating the microbiota–gut–brain axis
Keane, L., Clarke, G. A., & Cryan, J. F. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01188-9 · Cited by 37 · see citing works
Gödel, C., Kunkel, B., Kashani, A., Lassmann, H., Arumugam, M., & Krishnamoorthy, G. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01766-9 · Cited by 28 · see citing works
Melamed, E., Palmer, J. L., & Fonken, C. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1019877 · Cited by 27 · see citing works
How the gut microbiota impacts neurodegenerative diseases by modulating CNS immune cells
Schaible, P., Henschel, J., & Erny, D. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03371-0 · Cited by 31 · see citing works
Lynch, C. M. K., Nagpal, J. K., Clarke, G. A., & Cryan, J. F. (2021) · Current Opinion in Physiology · doi:10.1016/j.cophys.2021.100468 · Cited by 23 · see citing works
Hasaniani, N., Ghasemi‐Kasman, M., Halaji, M., & Rostami-Mansoor, S. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03593-4 · Cited by 23 · see citing works
Ullah, H., Товчига, О. В., Daglia, M., & Khan, H. Z. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210217084827 · Cited by 25 · see citing works
He, Y., Zhang, Y., Li, F., & Shi, Y. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.849372 · Cited by 21 · see citing works
Gut microbiota in multiple sclerosis and animal models
Schumacher, S. M., Doyle, W. J., Hill, K., & Ochoa‐Repáraz, J. (2025) · The FEBS Journal · doi:10.1111/febs.17161 · Cited by 21 · see citing works
Hoffman, K. R., Brownell, Z., Doyle, W. J., & Ochoa‐Repáraz, J. (2022) · Journal of Autoimmunity · doi:10.1016/j.jaut.2022.102957 · Cited by 20 · see citing works
Gut-brain communication in demyelinating disorders
Sauma, S., & Casaccia, P. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.01.005 · Cited by 18 · see citing works
Tang, W., Wang, Q., Sun, M., Liu, C., Huang, Y., Zhou, M., Zhang, X., Meng, Z., & Zhang, J. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122952 · Cited by 14 · see citing works
Remyelination and the gut−brain axis
Duncan, I. D., & Watters, J. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918897116 · Cited by 11 · see citing works
The Impact of IgA and the Microbiota on CNS Disease
Pu, A., Lee, D. S. W., Isho, B., Naouar, I., & Gommerman, J. L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.742173 · Cited by 9 · see citing works
Cen, Q., Cui, Y., Jin, J., Feng, J., Xin, Y., Zhang, Z., Li, J., Wang, J., & Zhang, A. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2576657 · Cited by 8 · see citing works
Li, J., Xue, H., Qingqing, M., He, X., Ma, L., Shi, B., Sun, S., & Yao, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.576445 · Cited by 7 · see citing works
Murayama, R., Liu, G., Zhao, M., Xu, D., Zhu, T., Cai, Y., Yue, Y., Nakamura, H., & Hashimoto, K. (2024) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2024.173946 · Cited by 5 · see citing works
The influence of aging and the microbiome in multiple sclerosis and other neurologic diseases
Fettig, N. M., Pu, A., Osborne, L. C., & Gommerman, J. L. (2024) · Immunological Reviews · doi:10.1111/imr.13361 · Cited by 6 · see citing works
Animal model of multiple sclerosis: Experimental autoimmune encephalomyelitis
Muñoz-Jurado, A., Escribano, B. M., & Túnez, I. (2024) · Methods in cell biology · doi:10.1016/bs.mcb.2024.03.013 · Cited by 4 · see citing works
The mechanism of disease progression by aging and age-related gut dysbiosis in multiple sclerosis
Yadav, S. K., Chen, C., Dhib-Jalbut, S. S., & Ito, K. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.106956 · Cited by 4 · see citing works
The Nerves to Conduct a Multiple Sclerosis Crime Investigation
Chopra, S., Myers, Z., Sekhon, H., & Dufour, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052498 · Cited by 2 · see citing works
McMurran, C. E. (2021) · Multiple Sclerosis Journal · doi:10.1177/13524585211016722 · Cited by 3 · see citing works
Self-citationFerreira, C., Carvalho, F. S., Vieira, P., Alves, A. D. C., Palavra, F., Almeida, J., Alves, V., Coscueta, E. R., Dias‐Pereira, P., Pintado, M., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1682183 · Cited by 2 · see citing works
Hohlfeld, R. (2021) · Multiple Sclerosis Journal · doi:10.1177/13524585211018990 · Cited by 1 · see citing works
Cabeza‐Fernández, S., Niñerola, S., Armengol-Gomis, A., Paraíso‐Luna, J., Casillas-Bajo, Á., Gomez-Sanchez, J. A., Cabedo, H., Barco, Á., & de la Fuente, A. G. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.11.724385 · Cited by 1 · see citing works
Microbiota influence brain systems—Work in animal models
Foster, J. A., & Clarke, G. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-814800-6.00010-8
- Authors
- McMurran, C. E., Guzman de la Fuente, A., Penalva, R., Ben Menachem-Zidon, O., Dombrowski, Y., Falconer, J., Gonzalez, G. A., Zhao, C., Krause, F. N., Young, A. M. H., Griffin, J. L., Jones, C. A., Hollins, C., Heimesaat, M. M., Fitzgerald, D. C., & Franklin, R. J. M.
- Affiliations
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- Wellcome–MRC Stem Cell Institute, University of Cambridge, CB2 0AW Cambridge, United Kingdom;
- Wellcome–Wolfson Institute for Experimental Medicine, Queen’s University Belfast, BT9 7BL Belfast, United Kingdom;
- Queen's University Belfast (GB)
- University of Cambridge (GB)
- Respiratory, Inflammation and Autoimmunity Research, MedImmune Ltd., CB21 6GH Cambridge, United Kingdom;
- Charité – Universitätsmedizin Berlin (DE)
- Corresponding author
- Fitzgerald, Denise C.
- Franklin, Robin J. M.
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2019-11-18
- Volume
- 116
- Issue
- 50
- Pages
- 25311-25321
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC6911206
- OpenAlex
- W2991319492
- Cited by
- 39
- References
- 65
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 3 · 2022: 5 · 2021: 9 · 2020: 7 · 2019: 1
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Portal (Queen's University Belfast) (submittedVersion, cc-by)
- Spiral (Imperial College London) (submittedVersion, other-oa)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
- European Committee for Treatment and Research in Multiple Sclerosis
- Wellcome Trust (110138/Z/15/Z)
- Leverhulme Trust
- Multiple Sclerosis Society
- Rosetrees Trust
- Jean Shanks Foundation
- BIRAX
- Directorate for Biological Sciences
- Medical Research Council (MR/P01836X/1, MC_PC_12009, MC_PC_13030, MR/P011705/1)
- Biotechnology and Biological Sciences Research Council (BB/J01026X/1, BB/N003721/1)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- gut microbiota, central nervous system demyelination, remyelination, multiple sclerosis, antibiotic therapy, probiotics, germ-free mice, oligodendrocyte precursor cells, neuroinflammation, oral microbiota
- MeSH terms
- Gastrointestinal Microbiome, Remyelination, Animals, Anti-Bacterial Agents, Cell Differentiation, Central Nervous System, Female, Humans, Male, Mice, Inbred C57BL, Multiple Sclerosis, Oligodendroglia, Stem Cells, Probiotics, Mice
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