The role of the gut microbiota and microbial metabolites in neuroinflammation.


Journal

European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201

Informations de publication

Date de publication:
12 2020
Historique:
received: 09 02 2020
revised: 30 09 2020
accepted: 10 11 2020
pubmed: 15 11 2020
medline: 30 1 2021
entrez: 14 11 2020
Statut: ppublish

Résumé

Recent literature indicates a potential importance of the gut microbiota for immune-mediated diseases. For instance, decreased diversity of commensals or an outgrowth of some bacterial strains, referred to as gut dysbiosis, was recently linked to hypertension, colitis, lupus, rheumatoid arthritis, and multiple sclerosis (MS). Studies in experimental autoimmune encephalomyelitis (EAE) as pivotal animal model of MS revealed a potential importance of microbial metabolites, including short-chain fatty acids or tryptophan metabolites. Both metabolites may influence the disease by modulation of the immune system, mainly by inducing Treg. These studies prompted researchers to investigate the contribution of the gut microbiota and microbial metabolites in the pathogenesis of MS. This review summarizes recent findings on the gut microbiota in MS patients and discusses the potential mechanisms how microbial metabolites may affect neuroinflammation. Many of these studies have been performed in the EAE model and were later reversely translated to humans. We also give a short summary on dietary high-salt effects on microbiota components and discuss the potential relevance of high-salt as a risk factor in MS.

Identifiants

pubmed: 33188704
doi: 10.1002/eji.201847807
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1863-1870

Informations de copyright

© 2020 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.

Références

Han, M., Wang, C., Liu, P., Li, D., Li, Y. and Ma, X., Dietary fiber gap and host gut microbiota. Protein Pept. Lett. 2017. 24: 388-396.
Sender, R., Fuchs, S. and Milo, R., Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016. 14.
Mowat, A. M. and Agace, W. W., Regional specialization within the intestinal immune system. Nat. Rev. Immunol. 2014. 14: 667-685.
Ley, R. E., Turnbaugh, P. J., Klein, S. and Gordon, J. I., Microbial ecology: human gut microbes associated with obesity. Nature 2006. 444: 1022-1023.
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C. J., Fagerberg, B., Nielsen, J. et al., Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 2013. 498: 99-103.
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N. and Pace, N. R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007. 104: 13780-13785.
Li, J., Zhao, F., Wang, Y., Chen, J., Tao, J., Tian, G., Wu, S. et al., Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 2017. 5: 14.
Yang, T., Santisteban, M. M., Rodriguez, V., Li, E., Ahmari, N., Carvajal, J. M., Zadeh, M. et al., Gut dysbiosis is linked to hypertension. Hypertension 2015. 65: 1331-1340.
Jangi, S., Gandhi, R., Cox, L. M., Li, N., von Glehn, F., Yan, R., Patel, B. et al., Alterations of the human gut microbiome in multiple sclerosis. Nat. Commun. 2016. 7: 12015.
Miyake, S., Kim, S., Suda, W., Oshima, K., Nakamura, M., Matsuoka, T., Chihara, N. et al., Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to clostridia XIVa and IV clusters. PLoS One 2015. 10: e0137429.
World Health Organization(Who). Guideline. Sodium Intake for Adults and Children. World Health Organization. 2012.
Wilck, N., Balogh, A., Markó, L., Bartolomaeus, H. and Müller, D. N., The role of sodium in modulating immune cell function. Nat. Rev. Nephrol. 2019. 15: 546-558.
Müller, S., Quast, T., Schröder, A., Hucke, S., Klotz, L., Jantsch, J., Gerzer, R. et al., Salt-dependent chemotaxis of macrophages. PLoS One 2013. 8: e73439.
Zhang, W.-C., Zheng, X.-J., Du, L.-J., Sun, J.-Y., Shen, Z.-X., Shi, C., Sun, S. et al., High salt primes a specific activation state of macrophages, M(Na). Cell Res. 2015. 25: 893-910.
Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R. A., Muller, D. N. et al., Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 2013. 496: 518-522.
Wu, C., Yosef, N., Thalhamer, T., Zhu, C., Xiao, S., Kishi, Y., Regev, A. et al., Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 2013. 496: 513-517.
Binger, K. J., Gebhardt, M., Heinig, M., Rintisch, C., Schroeder, A., Neuhofer, W., Hilgers, K. et al., High salt reduces the activation of IL-4- and IL-13-stimulated macrophages. J. Clin. Invest. 2015. 125: 4223-4238.
Hernandez, A. L., Kitz, A., Wu, C., Lowther, D. E., Rodriguez, D. M., Vudattu, N., Deng, S. et al., Sodium chloride inhibits the suppressive function of FOXP3+ regulatory T cells. J. Clin. Invest. 2015. 125: 4212-4222.
Müller, D. N., Wilck, N., Haase, S., Kleinewietfeld, M. and Linker, R. A., Sodium in the microenvironment regulates immune responses and tissue homeostasis. Nat. Rev. Immunol. 2019; 19: 243-254.
Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T. et al., A human gut microbial gene catalog established by metagenomic sequencing. Nature 2010. 464: 59-65.
Cuesta-Zuluaga, J., Kelley, S. T., Chen, Y., Escobar, J. S., Mueller, N. T., Ley, R. E., McDonald, D. et al., Age and sex-dependent patterns of gut microbial diversity in human adults. mSystems 2019. 4. https://doi.org/10.1128/mSystems.00261-19.
Langdon, A., Crook, N. and Dantas, G., The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med. 2016. 8: 39.
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V. et al., Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014. 505: 559-563.
Gensollen, T., Iyer, S. S., Kasper, D. L. and Blumberg, R. S., How colonization by microbiota in early life shapes the immune system. Science 2016. 352: 539-544.
Dendrou, C. A., Fugger, L. and Friese, M. A., Immunopathology of multiple sclerosis. Nat. Rev. Immunol. 2015. 15: 545-558.
Gold, R., Linington, C. and Lassmann, H., Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006. 129: 1953-1971.
Yokote, H., Miyake, S., Croxford, J. L., Oki, S., Mizusawa, H. and Yamamura, T., NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am. J. Pathol. 2008. 173: 1714-1723.
Ochoa-Repáraz, J., Mielcarz, D. W., Ditrio, L. E., Burroughs, A. R., Foureau, D. M., Haque-Begum, S. and Kasper, L. H., Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009. 183: 6041-6050.
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., Wekerle, H. et al., Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011. 479: 538-541.
Lee, Y. K., Menezes, J. S., Umesaki, Y. and Mazmanian, S. K., Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 2011. 108: 4615-4622.
Ochoa-Repáraz, J., Mielcarz, D. W., Wang, Y., Begum-Haque, S., Dasgupta, S., Kasper, D. L. and Kasper, L. H., A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal. Immunol. 2010. 3: 487-495.
Ventura, R. E., Iizumi, T., Battaglia, T., Liu, M., Perez-Perez, G. I., Herbert, J. and Blaser, M. J., Gut microbiome of treatment-naïve MS patients of different ethnicities early in disease course. Sci. Rep. 2019. 9: 16396.
Chen, J., Chia, N., Kalari, K. R., Yao, J. Z., Novotna, M., Paz Soldan, M. M., Luckey, D. H. et al., Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci. Rep. 2016. 6. https://doi.org/10.1038/srep28484.
Cekanaviciute, E., Yoo, B. B., Runia, T. F., Debelius, J. W., Singh, S., Nelson, C. A., Kanner, R. et al., Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci. USA 2017. 114: 10713-10718.
Kozhieva, M., Naumova, N., Alikina, T., Boyko, A., Vlassov, V. and Kabilov, M. R., Primary progressive multiple sclerosis in a Russian cohort: relationship with gut bacterial diversity. BMC Microbiol. 2019. 19. https://doi.org/10.1186/s12866-019-1685-2.
Takewaki, D., Suda, W., Sato, W., Takayasu, L., Kumar, N., Kimura, K., Kaga, N. et al., Alterations of the gut ecological and functional microenvironment in different stages of multiple sclerosis. Proc. Natl. Acad. Sci. USA 2020. 117: 22402-22412.
Miyake, S., Kim, S., Suda, W., Oshima, K., Nakamura, M., Matsuoka, T., Chihara, N. et al., Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to clostridia XIVa and IV clusters. PLoS One 2015. 10. https://doi.org/10.1371/journal.pone.0137429.
Berer, K., Gerdes, L. A., Cekanaviciute, E., Jia, X., Xiao, L., Xia, Z., Liu, C. et al., Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc. Natl. Acad. Sci. USA 2017. 114: 10719-10724. https://doi.org/10.1073/pnas.1711233114.
Mangalam, A., Shahi, S. K., Luckey, D., Karau, M., Marietta, E., Luo, N., Choung, R. S. et al., Human gut-derived commensal bacteria suppress CNS inflammatory and demyelinating disease. Cell Rep. 2017. 20: 1269-1277.
Shahi, S. K., Freedman, S. N., Murra, A. C., Zarei, K., Sompallae, R., Gibson-Corley, K. N., Karandikar, N. J. et al., Prevotella histicola, A human gut commensal, is as potent as COPAXONE® in an animal model of multiple sclerosis. Front. Immunol. 2019. 10. https://doi.org/10.3389/fimmu.2019.00462.
Haghikia, A., Jörg, S., Duscha, A., Berg, J., Manzel, A., Waschbisch, A., Hammer, A. et al., Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity 2015. 43: 817-829.
Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H. et al., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013. 504: 451-455.
Duscha, A., Gisevius, B., Hirschberg, S., Yissachar, N., Stangl, G. I., Eilers, E., Bader, V. et al., Propionic acid shapes the multiple sclerosis disease course by an immunomodulatory mechanism. Cell 2020. https://doi.org/10.1016/j.cell.2020.02.035.
Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A. et al., The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 2014. 6: 263ra158.
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H. et al., Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 2015. 18: 965-977. https://doi.org/10.1038/nn.4030.
Round, J. L. and Mazmanian, S. K., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2010. 107: 12204-12209..
Haase, S., Haghikia, A., Wilck, N., Müller, D. N. and Linker, R. A., Impacts of microbiome metabolites on immune regulation and autoimmunity. Immunology 2018. 154: 230-238.
Zelante, T., Iannitti, R. G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R. et al., Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013. 39: 372-385.
He, B., Hoang, T. K., Tian, X., Taylor, C. M., Blanchard, E., Luo, M., Bhattacharjee, M. B. et al., Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Front. Immunol. 2019. 10: 385.
Wilck, N., Matus, M. G., Kearney, S. M., Olesen, S. W., Forslund, K., Bartolomaeus, H., Haase, S. et al., Salt-responsive gut commensal modulates TH17 axis and disease. Nature 2017. https://doi.org/10.1038/nature24628.
Calvo-Barreiro, L., Eixarch, H., Ponce-Alonso, M., Castillo, M., Lebrón-Galán, R., Mestre, L., Guaza, C. et al., A commercial probiotic induces tolerogenic and reduces pathogenic responses in experimental autoimmune encephalomyelitis. Cells 2020. 9. https://doi.org/10.3390/cells9040906.
Cui, Y., Miao, K., Niyaphorn, S. and Qu, X., Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int. J. Mol. Sci. 2020. 21: 995.
Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., Ma, L., Nagler, C. R. et al., Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015. 161: 264-276.
Dinan, T. G., Stilling, R. M., Stanton, C. and Cryan, J. F., Collective unconscious: how gut microbes shape human behavior. J. Psychiatr. Res. 2015. 63: 1-9.
Cao, G., Edden, R. A. E., Gao, F., Li, H., Gong, T., Chen, W., Liu, X. et al., Reduced GABA levels correlate with cognitive impairment in patients with relapsing-remitting multiple sclerosis. Eur. Radiol. 2018. 28: 1140-1148.
Takata, K., Kinoshita, M., Okuno, T., Moriya, M., Kohda, T., Honorat, J. A., Sugimoto, T. et al., The lactic acid bacterium pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells. PLoS One 2011. 6: e27644.
Lee, K., Hwang, S., Paik, D. J., Kim, W. K., Kim, J. M. and Youn, J., Bacillus-derived poly-γ-glutamic acid reciprocally regulates the differentiation of T helper 17 and regulatory T cells and attenuates experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 2012. 170: 66-76.
Visser, L., Heer, H.J., Boven, L. A., Riel, D., Meurs, M., Melief, M.-J., Zähringer, U. et al., Proinflammatory bacterial peptidoglycan as a cofactor for the development of central nervous system autoimmune disease. J. Immunol. 2005. 174: 808-816.
Schrijver, I. A., van Meurs, M., Melief, M.-J., Wim Ang, C., Buljevac, D., Ravid, R., Hazenberg, M. P. et al., Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis. Brain 2001. 124: 1544-1554.
Jose, P. A., Yang, Z., Zeng, C. and Felder, R. A., The importance of the gastrorenal axis in the control of body sodium homeostasis. Exp. Physiol. 2016. 101: 465-470.
Wang, C., Huang, Z., Yu, K., Ding, R., Ye, K., Dai, C., Xu, X. et al., High-salt diet has a certain impact on protein digestion and gut microbiota: a sequencing and proteome combined study. Front. Microbiol. 2017. 8. https://doi.org/10.3389/fmicb.2017.01838.
Ferguson, J. F., Aden, L. A., Barbaro, N. R., Van Beusecum, J. P., Xiao, L., Simmons, A. J., Warden, C. et al., High dietary salt-induced dendritic cell activation underlies microbial dysbiosis-associated hypertension. JCI Insight 2019. 5. https://doi.org/10.1172/jci.insight.126241.
Scher, J. U., Sczesnak, A., Longman, R. S., Segata, N., Ubeda, C., Bielski, C., Rostron, T. et al., Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013. 2: e01202.
Miranda, P. M., De Palma, G., Serkis, V., Lu, J., Louis-Auguste, M. P., McCarville, J. L., Verdu, E. F. et al., High salt diet exacerbates colitis in mice by decreasing Lactobacillus levels and butyrate production. Microbiome 2018. 6: 57.
Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R. A., Muller, D. N. et al., Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 2013. 496: 518-522.
Rothhammer, V., Mascanfroni, I. D., Bunse, L., Takenaka, M. C., Kenison, J. E., Mayo, L., Chao, C.-C. et al., Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 2016. 22: 586-597.
Bier, A., Braun, T., Khasbab, R., Di Segni, A., Grossman, E., Haberman, Y. and Leibowitz, A., A high salt diet modulates the gut microbiota and short chain fatty acids production in a salt-sensitive hypertension rat model. Nutrients 2018. 10.
Mizuno, M., Noto, D., Kaga, N., Chiba, A. and Miyake, S., The dual role of short fatty acid chains in the pathogenesis of autoimmune disease models. PLoS One 2017. 12: e0173032.
Jörg, S., Kissel, J., Manzel, A., Kleinewietfeld, M., Haghikia, A., Gold, R., Müller, D. N. et al., High salt drives Th17 responses in experimental autoimmune encephalomyelitis without impacting myeloid dendritic cells. Exp. Neurol. 2016. 279: 212-222.
Hammer, A., Schliep, A., Jörg, S., Haghikia, A., Gold, R., Kleinewietfeld, M., Müller, D. N. et al., Impact of combined sodium chloride and saturated long-chain fatty acid challenge on the differentiation of T helper cells in neuroinflammation. J Neuroinflammation 2017. 14: 184.
Hucke, S., Eschborn, M., Liebmann, M., Herold, M., Freise, N., Engbers, A., Ehling, P. et al., Sodium chloride promotes pro-inflammatory macrophage polarization thereby aggravating CNS autoimmunity. J. Autoimmun. 2016. 67: 90-101.
Krementsov, D. N., Case, L. K., Hickey, W. F. and Teuscher, C., Exacerbation of autoimmune neuroinflammation by dietary sodium is genetically controlled and sex specific. FASEB J. 2015. 29: 3446-3457.
Farez, M. F., Fiol, M. P., Gaitán, M. I., Quintana, F. J. and Correale, J., Sodium intake is associated with increased disease activity in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2015. 86: 26-31.
Fitzgerald, K. C., Munger, K. L., Hartung, H.-P., Freedman, M. S., Montalbán, X., Edan, G., Wicklein, E.-M. et al., Sodium intake and multiple sclerosis activity and progression in BENEFIT. Ann. Neurol. 2017. 82: 20-29.
McDonald, J., Graves, J., Waldman, A., Lotze, T., Schreiner, T., Belman, A., Greenberg, B. et al., A case-control study of dietary salt intake in pediatric-onset multiple sclerosis. Mult. Scler. Relat. Disord. 2016. 6: 87-92.
Nourbakhsh, B., Graves, J., Casper, T. C., Lulu, S., Waldman, A., Belman, A., Greenberg, B. et al., Dietary salt intake and time to relapse in paediatric multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2016. 87: 1350-1353.
Tankou, S. K., Regev, K., Healy, B. C., Cox, L. M., Tjon, E., Kivisakk, P., Vanande, I. P. et al., Investigation of probiotics in multiple sclerosis. Mult. Scler. 2018. 24: 58-63.
Tankou, S. K., Regev, K., Healy, B. C., Tjon, E., Laghi, L., Cox, L. M., Kivisäkk, P. et al., A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann. Neurol. 2018. 83: 1147-1161.
Saresella, M., Marventano, I., Barone, M., La Rosa, F., Piancone, F., Mendozzi, L., d'Arma, A. et al., Alterations in circulating fatty acid are associated with gut microbiota dysbiosis and inflammation in multiple sclerosis. Front. Immunol. 2020. 11: 1390.

Auteurs

Stefanie Haase (S)

Department of Neurology, University Hospital Regensburg, Regensburg, Germany.

Nicola Wilck (N)

Medizinische Klinik mit Schwerpunkt Nephrologie und Internistische Intensivmedizin, Charité-Universitätsmedizin Berlin, Berlin, Germany.
Experimental and Clinical Research Center, Charité-Universitätsmedizin Berlin and Max Delbrück Center for Molecular Medicine, Berlin, Germany.
Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.
DZHK (German Centre for Cardiovascular Research), Berlin, Germany.
Berlin Institute of Health (BIH), Berlin, Germany.

Aiden Haghikia (A)

Department of Neurology, University Medicine Magdeburg, Magdeburg, Germany.

Ralf Gold (R)

Department of Neurology, Ruhr University Bochum, Bochum, Germany.

Dominik N Mueller (DN)

Experimental and Clinical Research Center, Charité-Universitätsmedizin Berlin and Max Delbrück Center for Molecular Medicine, Berlin, Germany.
Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.
DZHK (German Centre for Cardiovascular Research), Berlin, Germany.
Berlin Institute of Health (BIH), Berlin, Germany.

Ralf A Linker (RA)

Department of Neurology, University Hospital Regensburg, Regensburg, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH