3,323
Views
21
CrossRef citations to date
0
Altmetric
Research paper

How oral probiotics affect the severity of an experimental model of progressive multiple sclerosis? Bringing commensal bacteria into the neurodegenerative process

, ORCID Icon, ORCID Icon, , , , , , , ORCID Icon & show all
Article: 1813532 | Received 24 Feb 2020, Accepted 12 Aug 2020, Published online: 08 Sep 2020

References

  • Ebers GC. Environmental factors and multiple sclerosis. Lancet Neurol. 2008;7:268–15. doi:10.1016/S1474-4422(08)70042-5.
  • Olsson T, Barcellos LF, Alfredsson L. Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis. Nat Rev Neurol. 2017;13:25–36. doi:10.1038/nrneurol.2016.187.
  • Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011;479:538–541. doi:10.1038/nature10554.
  • Chen J, Chia N, Kalari KR, Yao JZ, Novotna M, Paz Soldan MM, Luckey DH, Marietta EV, Jeraldo PR, Chen X, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep. 2016;6:28484. doi:10.1038/srep28484.
  • Jangi S, Gandhi R, Cox LM, Li N, von Glehn F, Yan R, Patel B, Mazzola MA, Liu S, Glanz BL et al. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun. 2016;7:12015. doi:10.1038/ncomms12015.
  • Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Foureau DM, Haque-Begum S, Kasper LH. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol. 2009;183:6041–6050. doi:10.4049/jimmunol.0900747.
  • Yokote H, Miyake S, Croxford JL, Oki S, Mizusawa H, Yamamura T. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am J Pathol. 2008;173:1714–1723. doi:10.2353/ajpath.2008.080622.
  • Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4615–4622. doi:10.1073/pnas.1000082107.
  • Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Begum-Haque S, Dasgupta S, Kasper DL, Kasper LH. Central nervous system demyelinating disease protection by the human commensal bacteroides fragilis depends on polysaccharide A expression. J Immunol. 2010;185:4101–4108. doi:10.4049/jimmunol.1001443.
  • Wang Y, Begum-Haque S, Telesford KM, Ochoa-Reparaz J, Christy M, Kasper EJ, Kasper DL, Robson SC, Kasper LH. A commensal bacterial product elicits and modulates migratory capacity of CD39+CD4 T regulatory subsets in the suppression of neuroinflammation. Gut Microbes. 2014;5:552–561. doi:10.4161/gmic.29797.
  • Shahi SK, Freedman SN, Murra AC, Zarei K, Sompallae R, Gibson-Corley KN, Karandikar NJ, Murray JA, Mangalam AK. Prevotella histicola, a human gut commensal, is as potent as COPAXONE(R) in an animal model of multiple sclerosis. Front Immunol. 2019;10:462. doi:10.3389/fimmu.2019.00462.
  • Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, Molin G, Thorlacius H, Alenfall J, Jeppsson B, Weström B, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009. doi:10.1371/journal.pone.0009009.
  • He B, Hoang TK, Tian X, Taylor CM, Blanchard E, Luo M, Bhattacharjee MB, Freeborn J, Park S, Couturier J, et al. Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Front Immunol. 2019;10:385. doi:10.3389/fimmu.2019.00385.
  • Yamashita M, Ukibe K, Matsubara Y, Hosoya T, Sakai F, Kon S, Arima Y, Murakami M, Nakagawa H, Miyazaki T, et al. Lactobacillus helveticus SBT2171 attenuates experimental autoimmune encephalomyelitis in Mice. Front Microbiol. 2017;8:2596. doi:10.3389/fmicb.2017.02596.
  • Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, Kim J-E, Nam JH, Im S-H. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol. 2013;146:217–227. doi:10.1016/j.clim.2013.01.001.
  • Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, Tajabadi-Ebrahimi M, Jafari P, Asemi Z. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin Nutr. 2017;36(5):1245–1249. doi:10.1016/j.clnu.2016.08.015.
  • Tankou SK, Regev K, Healy BC, Tjon E, Laghi L, Cox LM, Kivisäkk P, Pierre IV, Hrishikesh L, Gandhi R, et al. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann Neurol. 2018;83(6):1147–1161. doi:10.1002/ana.25244.
  • Miyake S, Kim S, Suda W, Oshima K, Nakamura M, Matsuoka T, Chihara N, Tomita A, Sato W, Kim S-W, 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(9):e0137429. doi:10.1371/journal.pone.0137429.
  • Mielcarz DW, Kasper LH. The gut microbiome in multiple sclerosis. Curr Treat Options Neurol. 2015;17:344. doi:10.1007/s11940-015-0344-7.
  • Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3:4–14. doi:10.4161/gmic.19320.
  • Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535:75–84. doi:10.1038/nature18848.
  • Colpitts SL, Kasper LH. Influence of the gut microbiome on autoimmunity in the central nervous system. J Immunol. 2017;198:596–604. doi:10.4049/jimmunol.1601438.
  • Cheng FS, Pan D, Chang B, Jiang M, Sang LX. Probiotic mixture VSL#3: an overview of basic and clinical studies in chronic diseases. World J Clin Cases. 2020;8:1361–1384. doi:10.12998/wjcc.v8.i8.1361.
  • Camara-Lemarroy CR, Metz LM, Yong VW. Focus on the gut-brain axis: multiple sclerosis, the intestinal barrier and the microbiome. World J Gastroenterol. 2018;24:4217–4223. doi:10.3748/wjg.v24.i37.4217.
  • Schepici G, Silvestro S, Bramanti P, Mazzon E. The gut microbiota in multiple sclerosis: an overview of clinical trials. Cell Transplant. 2019;28:1507–1527. doi:10.1177/0963689719873890.
  • Telesford KM, Yan W, Ochoa-Reparaz J, Pant A, Kircher C, Christy MA, Begum-Haque S, Kasper DL, Kasper LH. A commensal symbiotic factor derived from Bacteroides fragilis promotes human CD39 + Foxp3 + T cells and T reg function. Gut Microbes. 2015;6:234–242. doi:10.1080/19490976.2015.1056973.
  • Mestre L, Carrillo-Salinas FJ, Mecha M, Feliu A, Espejo C, Alvarez-Cermeno JC, Villar LM, Guaza C. Manipulation of gut microbiota influences immune responses, axon preservation, and motor disability in a model of progressive multiple sclerosis. Front Immunol. 2019;10:1374. doi:10.3389/fimmu.2019.01374.
  • Fletcher JM, Lonergan R, Costelloe L, Kinsella K, Moran B, O’Farrelly C, Tubridy N, Mills KHG. CD39 + Foxp3 + regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol. 2009;183:7602–7610. doi:10.4049/jimmunol.0901881.
  • Li J, Ridgway W, Fathman CG, Tse HY, Shaw MK. High cell surface expression of CD4 allows distinction of CD4(+)CD25(+) antigen-specific effector T cells from CD4(+)CD25(+) regulatory T cells in murine experimental autoimmune encephalomyelitis. J Neuroimmunol. 2007;192:57–67. doi:10.1016/j.jneuroim.2007.09.004.
  • Kim M, Kim CH. Regulation of humoral immunity by gut microbial products. Gut Microbes. 2017;8:392–399. doi:10.1080/19490976.2017.1299311.
  • Rosser EC, Oleinika K, Tonon S, Doyle R, Bosma A, Carter NA, Harris KA, Jones SA, Klein N, Mauri C, et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1beta and interleukin-6 production. Nat Med. 2014;20:1334–1339. doi:10.1038/nm.3680.
  • Ochoa-Reparaz J, Kasper LH. The influence of gut-derived CD39 regulatory T cells in CNS demyelinating disease. Transl Res. 2017;179:126–138. doi:10.1016/j.trsl.2016.07.016.
  • Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci. 2017;20:145–155. doi:10.1038/nn.4476.
  • De Biase LM, Schuebel KE, Fusfeld ZH, Jair K, Hawes IA, Cimbro R, Zhang H-Y, Liu Q-R, Shen H, Xi Z-X, et al. Local cues establish and maintain region-specific phenotypes of basal ganglia microglia. Neuron. 2017;95(2):341–56 e6. doi:10.1016/j.neuron.2017.06.020.
  • Haghikia A, Jorg S, Duscha A, Berg J, Manzel A, Waschbisch A, Hammer A, Lee D-H, May C, Wilck N, et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 2015;43:817–829. doi:10.1016/j.immuni.2015.09.007.
  • Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18:965–977. doi:10.1038/nn.4030.
  • Mizuno M, Noto D, Kaga N, Chiba A, Miyake S, Ashour HM. The dual role of short fatty acid chains in the pathogenesis of autoimmune disease models. PLoS One. 2017;12:e0173032. doi:10.1371/journal.pone.0173032.
  • Chitrala KN, Guan H, Singh NP, Busbee B, Gandy A, Mehrpouya-Bahrami P, Ganewatta MS, Tang C, Chatterjee S, Nagarkatti P, et al. CD44 deletion leading to attenuation of experimental autoimmune encephalomyelitis results from alterations in gut microbiome in mice. Eur J Immunol. 2017;47(7):1188–1199. doi:10.1002/eji.201646792.
  • Luu M, Pautz S, Kohl V, Singh R, Romero R, Lucas S, Hofmann J, Raifer H, Vachharajani N, Carrascosa LC, et al. The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat Commun. 2019;10:760. doi:10.1038/s41467-019-08711-2.
  • Sanchez HN, Moroney JB, Gan H, Shen T, Im JL, Li T, Taylor JR, Zan H, Casali P. B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids. Nat Commun. 2020;11:60. doi:10.1038/s41467-019-13603-6.
  • Rosser EC, Piper CJM, Matei DE, Blair PA, Rendeiro AF, Orford M, Alber DG, Krausgruber T, Catalan D, Klein N, et al. Microbiota-derived metabolites suppress arthritis by amplifying aryl-hydrocarbon receptor activation in regulatory B cells. Cell Metab. 2020;31(4):837–51 e10. doi:10.1016/j.cmet.2020.03.003.
  • Rothhammer V, Mascanfroni ID, Bunse L, Takenaka MC, Kenison JE, Mayo L, Chao -C-C, Patel B, Yan R, Blain M, 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. doi:10.1038/nm.4106.
  • Rothhammer V, Borucki DM, Tjon EC, Takenaka MC, Chao CC, Ardura-Fabregat A, de Lima KA, Gutiérrez-Vázquez C, Hewson P, Staszewski O, et al. Microglial control of astrocytes in response to microbial metabolites. Nature. 2018;557:724–728. doi:10.1038/s41586-018-0119-x.
  • Mangalam A, Shahi SK, Luckey D, Karau M, Marietta E, Luo N, Choung RS, Ju J, Sompallae R, Gibson-Corley K, et al. Human gut-derived commensal bacteria suppress CNS inflammatory and demyelinating disease. Cell Rep. 2017;20:1269–1277. doi:10.1016/j.celrep.2017.07.031.
  • Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62:67–72. doi:10.1079/PNS2002207.
  • Vital M, Howe AC, Tiedje JM, Moran MA. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. mBio. 2014;5(2):e00889. doi:10.1128/mBio.00889-14.
  • van Baarlen P, Wells JM, Kleerebezem M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol. 2013;34:208–215. doi:10.1016/j.it.2013.01.005.
  • Mestre L, Correa F, Arevalo-Martin A, Molina-Holgado E, Valenti M, Ortar G, Marzo V, Guaza C. Pharmacological modulation of the endocannabinoid system in a viral model of multiple sclerosis. J Neurochem. 2005;92:1327–1339. doi:10.1111/j.1471-4159.2004.02979.x.
  • Carrillo-Salinas FJ, Mestre L, Mecha M, Feliu A, Del Campo R, Villarrubia N, Espejo C, Montalbán X, Álvarez-Cermeño JC, Villar LM. Gut dysbiosis and neuroimmune responses to brain infection with Theiler’s murine encephalomyelitis virus. Sci Rep. 2017;7:44377. doi:10.1038/srep44377.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–336. doi:10.1038/nmeth.f.303.