Role of the intestinal microbiota in the pathogenesis of multiple sclerosis. Part 2. Gut microbiota as a predisposition factor for the multiple sclerosis development
- Authors: Abdurasulova I.N.1
-
Affiliations:
- Institute of Experimental Medicine
- Issue: Vol 23, No 1 (2023)
- Pages: 5-40
- Section: Analytical reviews
- URL: https://journals.rcsi.science/MAJ/article/view/134194
- DOI: https://doi.org/10.17816/MAJ115019
- ID: 134194
Cite item
Abstract
This part of the review focuses on the proposed involvement of the gut microbiota in the realization of the genetic risk of multiple sclerosis, the formation of the intestinal microbiome in early life, and provides data supporting the hypothesis that aberrant formation of the intestinal microbiota in early life may be a predisposing factor to multiple sclerosis.
Full Text
##article.viewOnOriginalSite##About the authors
Irina N. Abdurasulova
Institute of Experimental Medicine
Author for correspondence.
Email: i_abdurasulova@mail.ru
ORCID iD: 0000-0003-1010-6768
SPIN-code: 5019-3940
Scopus Author ID: 22233604700
Cand. Sci. (Biol.), Head of the Pavlov Department of Physiology
Russian Federation, Sаint PetersburgReferences
- Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491(7422):119–124. doi: 10.1038/nature11582
- Knights D, Silverberg MS, Weersma RK, et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med. 2014;6(12):107. doi: 10.1186/s13073-014-0107-1
- Brestoff JR, Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol. 2013;14(7):676–684. doi: 10.1038/ni.2640
- Grise EA, Serge JA. The human microbiome: our second genome. Annu Rev Genomics Hum Genet. 2012;13:151–170. doi: 10.1146/annurev-genom-090711-163814
- Benson AK, Kelly SA, Legge R, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci USA. 2010;107(44):18933–18938. doi: 10.1073/pnas.1007028107
- Rothschild D, Weissbrod O, Barkan E, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555(7695):210–215. doi: 10.1038/nature25973
- Goodrich JK, Waters JL, Poole AC, et al. Human genetics shape the gut microbiome. Cell. 2014;159(4):789–799. doi: 10.1016/j.cell.2014.09.053
- Davenport ER, Cusanovich DA, Michelini K, et al. Genome-wide association studies of the human gut microbiota. PLoS One. 2015;10(11):e0140301. doi: 10.1371/journal.pone.0140301
- Goodrich JK, Davenport ER, Waters JL, et al. Cross-species comparisons of host genetic associations with the microbiome. Science. 2016;352(6285):532–535. doi: 10.1126/science.aad9379
- Goodrich JK, Davenport ER, Beaumont M, et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe. 2016;19(5):731–743. doi: 10.1016/j.chom.2016.04.017
- Goodrich JK, Davenport ER, Clark AG, Ley RE. The relationship between the human genome and microbiome comes into view. Annu Rev Genet. 2017;51:413–433. doi: 10.1146/annurev-genet-110711-155532
- Turpin W, Espin-Garcia O, Xu W, et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet. 2016;48(11):1413–1417. doi: 10.1038/ng.3693
- Lim MY, You HJ, Yoon HS, et al. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut. 2017;66(6):1031–1038. doi: 10.1136/gutjnl-2015-311326
- Wells PM, Williams FMK, Matey-Hernandez ML, et al. RA and the Microbiome: Do host genetic factors provide the link? J Autoimmun. 2019;99:104–115. doi: 10.1016/j.jaut.2019.02.004
- He Z, Shao T, Li H, et al. Alterations of the gut microbiome in Chinese patients with systemic lupus erythematosus. Gut Pathog. 2016;8:64. doi: 10.1186/s13099-016-0146-9
- Kwon Y-C, Chun S, Kim K, Mak A. Update on the genetics of systemic lupus erythematosus: genome-wide association studies and beyond. Cells. 2019;8(10):1180. doi: 10.3390/cells8101180
- Blekhman R, Goodrich JK, Huang K, et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015;16(1):191. doi: 10.1186/s13059-015-0759-1
- Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 2006;127(2):423–433. doi: 10.1016/j.cell.2006.08.043
- Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM, et al. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis. 2001;13(3):129–134. doi: 10.1080/089106001750462669
- Stewart JA, Chadwick VS, Murray A. Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children. J Med Microbiol. 2005;54(Pt 12):1239–1242. doi: 10.1099/jmm.0.46189-0
- Xie H, Guo R, Zhong H, et al. Shotgun Metagenomics of 250 Adult Twins Reveals Genetic and Environmental Impacts on the Gut Microbiome. Cell Syst. 2016;3(6):572–584. doi: 10.1016/j.cels.2016.10.004
- Dicksved J, Halfvarson J, Rosenquist M, et al. Molecular analysis of the gut microbiota of identical twins with Crohn’s disease. ISME J. 2008;2(7):716–727. doi: 10.1038/ismej.2008.37
- Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6–14. doi: 10.1126/scitranslmed.3000322
- Sandoval-Motta S, Aldana M, Martínez-Romero E, Frank A. The human microbiome and the missing heritability problem. Front Genet. 2017;8:80. doi: 10.3389/fgene.2017.00080
- Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229–241. doi: 10.1016/j.cell.2004.07.002
- Petnicki-Ocwieja T, Hrncir T, Liu YJ, et al. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci USA. 2009;106(37):15813–15818. doi: 10.1073/pnas.0907722106
- Carvalho FA, Koren O, Goodrich JK, et al. Transient inability to manage Proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe. 2012;12(2):139–152. doi: 10.1016/j.chom.2012.07.004
- Fulde M, Sommer F, Chassaing B, et al. Neonatal selection by Toll-like receptor 5 influences long-term gut microbiota composition. Nature. 2018;560(7719):489–493. doi: 10.1038/s41586-018-0395-5
- Rehman A, Sina C, Gavrilova O, et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut. 2011;60(10):1354–1362. doi: 10.1136/gut.2010.216259
- Mondot S, Barreau F, Al Nabhani Z, et al. Altered gut microbiota composition in immune-impaired Nod2(-/-) mice. Gut. 2012;61(4):634–635. doi: 10.1136/gutjnl-2011- 300478
- Gulati AS, Kruek L, Sartor RB. Influence of NOD 2 on the protective intestinal commensal bacterium Faecalibacterium prausnitzii. Gastroenterology. 2010;138(5):S–14. doi: 10.1016/s0016-5085(10)60064-9
- Wen L, Ley RE, Volchkov PY, et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature. 2008;455(7216):1109–1113. doi: 10.1038/nature07336
- Salzman NH, Hung K, Haribhai D, et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol. 2010;11(1):76–83. doi: 10.1038/ni.1825
- McFall-Ngai M. Adaptive immunity: care for the community. Nature. 2007;445(7124):153. doi: 10.1038/445153a
- De Palma G, Capilla A, Nadal I, et al. Interplay between Human Leukocyte Antigen genes and the microbial colonization process of the newborn intestine. Curr Issues Mol Biol. 2010;12(1):1–10. doi: 10.2174/1871528113666140330201056
- Vijay-Kumar M, Aitken JD, Carvalho FA, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010;328(5975):228–231. doi: 10.1126/science.1179721
- Shulzhenko N, Morgun A, Hsiao W, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med. 2011;17(12):1585–1593. doi: 10.1038/nm.2505
- Wang J, Thingholm LB., Skiecevièienë J. et al. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat Genet. 2016;48(11):1396–1406. doi: 10.1038/ng.3695
- Kolde R, Franzosa EA, Rahnavard G, et al. Host genetic variation and its microbiome interactions within the Human Microbiome Project. Genome Med. 2018;10(1):6. doi: 10.1186/s13073-018-0515-8
- Wacklin P, Mäkivuokko H, Alakulppi N, et al. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS One. 2011;6(5):e20113. doi: 10.1371/journal.pone.0020113
- Su D, Nie Y, Zhu A, et al. Vitamin D signaling through induction of paneth cell defensins maintains gut microbiota and improves metabolic disorders and hepatic steatosis in animal models. Front Physiol. 2016;7:498. doi: 10.3389/fphys.2016.00498
- Awany D, Allali I, Dalvie S, et al. Host and microbiome genome-wide association studies: current state and challenges. Front Genet. 2019;9:637. doi: 10.3389/fgene.2018.00637
- Maglione A, Zuccalà M, Tosi M, et al. Host genetics and gut microbiome: perspectives for multiple sclerosis. Genes (Basel). 2021;12(8):1181. doi: 10.3390/genes12081181
- Abdurasulova IN. Role of the intestinal microbiota in the pathogenesis of multiple sclerosis. Part 1. Clinical and experimental evidence for the involvement of the gut microbiota in the development of multiple sclerosis. Medical Academic Journal. 2022;22(2):9–36. (In Russ.) doi: 10.17816/MAJ108241
- Hall AB, Tolonen AC, Xavier RJ. Human genetic variation and the gut microbiome in disease. Nat Rev Genet. 2017;18(11):690–699. doi: 10.1038/nrg.2017.63
- Imhann F, Vich Vila A, Bonder MJ, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018;67(1):108–119. doi: 10.1136/gutjnl-2016-312135
- Miller PG, Bonn MB, Franklin CL, et al. TNFR2 deficiency acts in concert with gut microbiota to precipitate spontaneous sex-biased central nervous system demyelinating autoimmune disease. J Immunol. 2015;195(10):4668–4684. doi: 10.4049/jimmunol.1501664
- Abdollahzadeh R, Fard MS, Rahmani F, et al. Predisposing role of vitamin D receptor (VDR) polymorphisms in the development of multiple sclerosis: A case-control study. J Neurol Sci. 2016;367:148–151. doi: 10.1016/j.jns.2016.05.053
- Imani D, Razi B, Motallebnezhad M, Rezaei R. Association between vitamin D receptor (VDR) polymorphisms and the risk of multiple sclerosis (MS): an updated meta-analysis. BMC Neurol. 2019;19(1):339. doi: 10.1186/s12883-019-1577-y
- Bakke D, Sun J. Ancient Nuclear Receptor VDR with new functions: microbiome and inflammation. Inflamm Bowel Dis. 2018;24(6):1149–1154. doi: 10.1093/ibd/izy092
- Haussler MR, Haussler CA, Bartik L, et al. Vitamin D receptor: molecular signaling and actions of nutritional ligands in disease prevention. Nutr Rev. 2008;66(Suppl. 2):S98–S112. doi: 10.1111/j.1753-4887.2008.00093.x
- Makishima M, Lu TT, Xie W, et al. Vitamin D receptor as an intestinal bile acid sensor. Science. 2002;296(5571):1313–1316. doi: 10.1126/science.1070477
- Han S, Li T, Ellis E, et al. A novel bile acid-activated vitamin D receptor signaling in human hepatocytes. Mol Endocrinol. 2010;24(6):1151–1164. doi: 10.1210/me.2009-0482
- Wang K, Liao M, Zhou N, et al. Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids. Cell Reports. 2019;25:222–235. doi: 10.1016/j.celrep.2018.12.028
- Tremlett H, Fadrosh DW, Faruqi AA, et al. Gut microbiota in early pediatric multiple sclerosis: a case-control study. Eur J Neurol. 2016;23(8):1308–1321. doi: 10.1111/ene.13026
- Reynders T, Devolder L, Valles-Colomer M, et al. Gut microbiome variation is associated to Multiple Sclerosis phenotypic subtypes. Ann Clin Transl Neurol. 2020;7(4):406–419. doi: 10.1002/acn3.51004
- Pellizoni FP, Leite AZ, de Campos Rodrigues N, et al. Detection of dysbiosis and increased intestinal permeability in Brazilian patients with relapsing-remitting multiple sclerosis. Int J Environ Res Public Health. 2021;18(9):4621. doi: 10.3390/ijerph18094621
- Oezguen N, Yalcinkaya N, Kücükali CI, et al. Microbiota stratification identifies disease-specific alterations in neuro-Behçet’s disease and multiple sclerosis. Clin Exp Rheumatol. 2019;37 Suppl 121(6):58–66.
- Bhargava P, Smith MD, Mische L, et al. Bile acid metabolism is altered in multiple sclerosis and supplementation ameliorates neuroinflammation. J Clin Invest. 2020;130(7):3467–3482. doi: 10.1172/JCI129401
- Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141. doi: 10.1016/j.cell.2014.03.011
- Schirmer M, Smeekens SP, Vlamakis H, et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell. 2016;167(4):1125–1136. doi: 10.1016/j.cell.2016.10.020
- Bevins CL, Salzman NH. The potter’s wheel: the host’s role in sculpting its microbiota. Cell Mol Life Sci. 2011;68(22):3675–3685. doi: 10.1007/s00018-011-0830-3
- Kozhieva M, Naumova N, Alikina T, et al. Primary progressive multiple sclerosis in a Russian cohort: relationship with gut bacterial diversity. BMC Microbiol. 2019;19(1):309. doi: 10.1186/s12866-019-1685-2
- Fujiwara M, Anstadt EJ, Flynn B, et al. Enhanced TLR2 responses in multiple sclerosis. Clin Exp Immunol. 2018;193(3):313–326. doi: 10.1111/cei.13150
- Farez MF, Quintana FJ, Gandi R, et al. Toll-like receptor 2 and poly(ADP-ribose) polymerase 1 promote central nervous system neuroinflammation in progressive EAE. Nat Immunol. 2009;10(9):958–964. doi: 10.1038/ni.1775
- Miranda-Hernandez S, Gerlach N, Fletcher JM, et al. Role for MyD88, TLR2 and TLR9 but not TLR1, TLR4 or TLR6 in experimental autoimmune encephalomyelitis. J Immunol. 2011;187(2):791–804. doi: 10.4049/jimmunol.1001992
- Prinz M, Garbe F, Schmidt H, et al. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest. 2006;116(2):456–464. doi: 10.1172/JCI26078
- Horton MK, McCauley K, Fadrosh D, et al. Gut microbiome is associated with multiple sclerosis activity in children. Ann Clin Transl Neurol. 2021;8(9):1867–1883. doi: 10.1002/acn3.51441
- Rezende RM, Oliveira RP, Medeiros SR, et al. Hsp65-producing Lactococcus lactis prevents experimental autoimmune encephalomyelitis in mice by inducing CD4+LAP+ regulatory T cells. J Autoimmun. 2013;40:45–57. doi: 10.1016/j.jaut.2012.07.012
- Cox LM, Maghzi AH, Liu S, et al. The gut microbiome in progressive multiple sclerosis. Ann Neurol. 2021;89(6):1195–1211. doi: 10.1002/ana.26084
- Abdurasulova IN, Tarasova EA, Ermolenko EI, et al. Multiple sclerosis is associated with altered quantitative and qualitative composition of intestinal microbiota. Medical Academic Journal. 2015;15(3):55–67. (In Russ.) doi: 10.17816/MAJ15355-67
- Cekanaviciute E, Yoo BB, Runia TF, 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(40):10713–10718. doi: 10.1073/pnas.1711235114
- Chiurchiù V, Leuti A, Cencioni M, et al. Modulation of monocytes by bioactive lipid anandamide in multiple sclerosis involves distinct Toll-like receptors. Pharmacol Res. 2016;113(Pt A):313–319. doi: 10.1016/j.phrs.2016.09.003
- Hughes L, Smith P, Bonell S, et al. Cross-reactivity between related sequences found in Acinetobacter sp., Pseudomonas aeruginosa, myelin basic protein and myelin oligodendrocyte glycoprotein in multiple sclerosis. J Neuroimmunol. 2003;144(1–2):105–115. doi: 10.1016/s0165-5728(03)00274-1
- Ebringer A, Hughes L, Rashid T, Wilson C. Acinetobacter immune responses in multiple sclerosis etiopathogenetic role and its possible use as a diagnostic marker. Arch Neurol. 2005;62(1):33–36. doi: 10.1001/archneur.62.1.33
- Ebringer A, Rashid T, Wilson C. The role of Acinetobacter in the pathogenesis of multiple sclerosis examined by using Popper sequences. Med Hypotheses. 2012;78(6):763–769. doi: 10.1016/j.mehy.2012.02.026
- Cuesta CM, Pascual M, Pérez-Moraga R, et al. TLR4 deficiency affects the microbiome and reduces intestinal dysfunctions and inflammation in chronic alcohol-fed mice. Int J Mol Sci. 2021;22(23):12830. doi: 10.3390/ijms222312830
- Forbes JD, Chen C-Y, Knox NC, et al. A comparative study of the gut microbiota in immune-mediated inflammatory diseases – does a common dysbiosis exist? Microbiome. 2018;6(1):221. doi: 10.1186/s40168-018-0603-4
- Cantoni С, Lin Q, Dorsett Y, et al. Alterations of host-gut microbiome interactions in multiple sclerosis. EBioMedicine. 2022;76:103798. doi: 10.1016/j.ebiom.2021.103798
- Miyake S, Kim S, Suda W, et al. Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belondind to Clostridia XIVa and IV clusters. PLoS One. 2015;10(9):e0137429. doi: 10.1371/journal.pone.0137429
- Cantarel BL, Waubant E, Chehoud C, et al. Gut microbiota in multiple sclerosis: possible influence of immunomodulators. J Investig Med. 2015;63(5):729–734. doi: 10.1097/JIM.0000000000000192
- Storm-Larsen C, Myhr K-M, Farbu E, et al. Gut microbiota composition during a 12-week intervention with delayed-release dimethyl fumarate in multiple sclerosis – a pilot trial. Mult Scler J Exp Transl Clin. 2019;5(4):2055217319888767. doi: 10.1177/2055217319888767
- Ling Z, Cheng Y, Yan X, et al. Alterations of the fecal microbiota in Chinese patients with multiple sclerosis. Front Immunol. 2020;11:590783. doi: 10.3389/fimmu.2020.590783
- Takewaki D, Suda W, Sato W, et al. Alterations of the gut ecological and functional microenvironment in different stages of multiple sclerosis. PNAS. 2020;117(36):22402–22412. doi: 10.1073/pnas.2011703117
- Castillo-Álvarez F, Pérez-Matute P, Oteo JA, Marzo-Sola ME. The influence of interferon β-1b on gut microbiota composition in patients with multiple sclerosis. Neurologia (Engl Ed). 2021;36(7):495–503. doi: 10.1016/j.nrleng.2020.05.006
- Marta M, Andersson A, Isaksson M, et al. Unexpected regulatory roles of TLR4 and TLR9 in experimental autoimmune encephalomyelitis. Eur J Immunol. 2008;38(2):565–575. doi: 10.1002/eji.200737187
- Zhang Y, Han J, Wu M, et al. Toll-like receptor 4 promotes Th17 lymphocyte infiltration via CCL25/CCR9 in pathogenesis of experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol. 2019;14(3):493–502. doi: 10.1007/s11481-019-09854-1
- Carrillo-Salinas FJ, Mestre L, Mecha M, et al. Gut dysbiosis and neuroimmune responses to brain infection with Theiler’s murine encephalomyelitis virus. Sci Rep. 2017. Vol. 7. P. 44377. doi: 10.1038/srep44377
- Abdurasulova IN, Tarasova EA, Matsulevich AV, et al. Influence of Bifidobacteria in the composition of the intestinal microbiota on the multiple sclerosis course. Problems Med Mycol. 2022;24(2):38. (In Russ.)
- Tan TG, Sefik E, Geva-Zatorsky N, et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc Natl Acad Sci USA. 2016;113(50):E8141–E8150. doi: 10.1073/pnas.1617460113
- Bouskra D, Brézillon C, Bérard M, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nat Lett. 2008;456(7221):507–510. doi: 10.1038/nature07450
- Chen GY, Núñez G. Gut Immunity: a NOD to the commensals. Curr Biol. 2009;19(4):R171–174. doi: 10.1016/j.cub.2008.12.027
- Galluzzo P, Capri FC, Vecchioni L, et al. Comparison of the intestinal microbiome of Italian patients with multiple sclerosis and their household relatives. Life (Basel). 2021;11(7):620. doi: 10.3390/life11070620
- Ventura RE, Iizumi1 T, Battaglia T, et al. Gut microbiome of treatment-naïve MS patients of different ethnicities early in disease course. Sci Rep. 2019;9(1):16396. doi: 10.1038/s41598-019-52894-z
- Cekanaviciute E., Pröbstel A.-K., Thomann A. et al. Multiple sclerosis-associated changes in the composition and immune functions of spore-forming bacteria. mSystems. 2018;3(6):e00083–18. doi: 10.1128/mSystems.00083-18
- Shaw PJ, Barr MJ, Lukens JR, et al. Signaling via the RIP2 adaptor protein in central nervous system-infiltrating dendritic cells promotes inflammation and autoimmunity. Immunity. 2011;34(1):75–84. doi: 10.1016/j.immuni.2010.12.015
- Rumah KR, Linden J, Fischetti VA, Vartanian T. Isolation of clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease. PLoS One. 2013;8(10):e76359. doi: 10.1371/journal.pone.0076359
- Ochoa-Repáraz J, Mielcarz DW, Wang Y, et al. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 2010;3(5):487–495. doi: 10.1038/mi.2010.29
- Gulati AS, Kreuk L, Sartor RB. 69 Influence of NOD2 on the protective intestinal commensal bacterium faecalibacterium prausnitzii. Gastroenterology. 2010;138(5):S–14. doi: 10.1016/S0016-5085(10)60064-9
- Chen J, Chia N, Kalari KR, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep. 2016;6:28484. doi: 10.1038/srep28484
- Taras D, Simmering R, Collins MD, et al. Reclassification of Eubacterium formicigenerans Holdeman and Moore 1974 as Dorea formicigenerans gen. nov., comb. nov., and description of Dorea longicatena sp. nov., isolated from human faeces. Int J Syst Evol Microbiol. 2002;52(Pt 2):423–428. doi: 10.1099/00207713-52-2-423
- Schirmer M, Smeekens SP, Vlamakis H, et al. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell. 2016;167(4):1897. doi: 10.1016/j.cell.2016.10.020
- Al KF, Craven LJ, Gibbons S, et al. Fecal microbiota transplantation is safe and tolerable in patients with multiple sclerosis: A pilot randomized controlled trial. Mult Scler J Exp Transl Clin. 2022;8(2):20552173221086662. doi: 10.1177/20552173221086662
- Chen L, Wilson JE, Koenigsknecht MJ, et al. NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth. Nat Immunol. 2017;18(5):541–551. doi: 10.1038/ni.3690
- Swidsinski A, Dörffel Y, Loening-Baucke V, et al. Reduced mass and diversity of the colonic microbiome in patients with multiple sclerosis and their improvement with ketogenic diet. Front Microbiol. 2017;8:1141. doi: 10.3389/fmicb.2017.01141
- Vilariño-Güell C, Zimprich A, Martinelli-Boneschi F, et al. Exome sequencing in multiple sclerosis families identifies 12 candidate genes and nominates biological pathways for the genesis of disease. PLoS Genet. 2019;15(6):e1008180. doi: 10.1371/journal.pgen.1008180
- Gharagozloo M, Mahvelati TM, Imbeault E, et al. The nod-like receptor, Nlrp12, plays an anti-inflammatory role in experimental autoimmune encephalomyelitis. J Neuroinflammation. 2015;12:198. doi: 10.1186/s12974-015-0414-5
- Gharagozloo M, Mahmoud S, Simard C, et al. The dual immunoregulatory function of Nlrp12 in T cell-mediated immune response: lessons from experimental autoimmune encephalomyelitis. Cells. 2018;7(9):119. doi: 10.3390/cells7090119
- Lukens JR, Gurung P, Shaw PJ, et al. The NLRP12 sensor negatively regulates autoinflammatory disease by modulating interleukin-4 production in T cells. Immunity. 2015;42(4):654–664. doi: 10.1016/j.immuni.2015.03.006
- Vacca M, Celano G, Calabrese FM, et al. The controversial role of human gut Lachnospiraceae. Microorganisms. 2020;8(4):573. doi: 10.3390/microorganisms8040573
- Tye H, Yu C-H, Simms LA, et al. NLRP1 restricts butyrate producing commensals to exacerbate inflammatory bowel disease. Nat Commun. 2018;9(1):3728. doi: 10.1038/s41467-018-06125-0
- Popplewell LF, Encarnacion M, Bernales CQ, et al. Genetic analysis of nucleotide-binding leucine-rich repeat (NLR) receptors in multiple sclerosis. Immunogenetics. 2020;72(6–7):381–385. doi: 10.1007/s00251-020-01170-w
- Maver A, Lavtar P, Ristić S, et al. Identification of rare genetic variation of NLRP1 gene in familial multiple sclerosis. Sci Rep. 2017;7(1):3715. doi: 10.1038/s41598-017-03536-9
- Bernales CQ, Encarnacion M, Criscuoli MG, et al. Analysis of NOD-like receptor NLRP1 in multiple sclerosis families. Immunogenetics. 2017;70(3):205–207. doi: 10.1007/s00251-017-1034-2
- Venkatesh M, Mukherjee S, Wang H, et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity. 2014;41(2):296–310. doi: 10.1016/j.immuni.2014.06.014
- Vascellari S, Palmas V, Melis M, et al. Gut microbiota and metabolome alterations associated with Parkinson’s disease. mSystems. 2020;15(5):e00561–20. doi: 10.1128/mSystems.00561-20
- Bell A, Brunt J, Crost E, et al. Elucidation of a sialic macid metabolism pathway in mucus-foraging Ruminococcus gnavus unravels mechanisms of bacterial adaptation to the gut. Nat Microbiol. 2019;4(12):2393–2404. doi: 10.1038/s41564-019-0590-7
- Zhang Y, Huang R, Cheng M, et al. Gut microbiota from NLRP3-deficient mice ameliorates depressive-like behaviors by regulating astrocyte dysfunction via circHIPK2. Microbiome. 2019;7(1):116. doi: 10.1186/s40168-019-0733-3
- Jha S, Srivastava SY, Brickey WJ, et al. The inflammasome sensor, NLRP3, regulates CNS inflammation and demyelination via caspase-1 and interleukin-18. J Neurosci. 2010;30(47):15811–15820. doi: 10.1523/JNEUROSCI.4088-10.2010
- Inoue M, Williams KL, Gunn MD, Shinohara ML. NLRP3 inflammasome induces chemotactic immune cell migration to the CNS in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA. 2012;109(26):10480–10485. doi: 10.1073/pnas.1201836109
- Malhotra S, Rio J, Urcelay E, et al. NLRP3 inflammasome is associated with the response to IFN-β in patients with multiple sclerosis. Brain. 2015;138(3):644–652. doi: 10.1093/brain/awu388
- Gris D, Ye Z, Iocca HA, et al. NLRP3 plays a critical role in the development of experimental autoimmune encephalomyelitis by mediating Th1 and Th17 responses. J Immunol. 2010;185(2):974–981. doi: 10.4049/jimmunol.0904145
- Farrokhi V, Nemati R, Nichols FC. Bacterial lipodipeptide, Lipid 654, is a microbiome-associated biomarker for multiple sclerosis. Clin Transl Immunol. 2013;2(11):e8. doi: 10.1038/cti.2013.11
- Haghikia A, Jörg S, Duscha A, et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 2015;43(4):817–829. doi: 10.1016/j.immuni.2015.09.007
- Nomura K, Ishikawa D, Okahara K, et al. Bacteroidetes species are correlated with disease activity in ulcerative colitis. J Clin Med. 2021;10(8):1749. doi: 10.3390/jcm10081749
- Elgendy SG, Abd-Elhameed R, Daef E, et al. Gut microbiota in forty cases of egyptian relapsing remitting multiple sclerosis. Iran J Microbiol. 2021;13(5):632–641. doi: 10.18502/ijm.v13i5.7428
- Shahi SK, Jensen SN, Murra AC, et al. Human commensal Prevotella histicola ameliorates disease as effectively as interferon-beta in the experimental autoimmune encephalomyelitis. Front Immunol. 2020;11:578648. doi: 10.3389/fimmu.2020.578648
- Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202. doi: 10.7554/eLife.01202
- Ghaly S, Kaakoush NO, Lloyd F, et al. Ultraviolet irradiation of skin alters the faecal microbiome independently of vitamin D in mice. Nutrients. 2018;10(8):1069. doi: 10.3390/nu10081069
- Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011;145(5):745–757. doi: 10.1016/j.cell.2011.04.022
- Ratsimandresy RA, Dorfleutner A, Stehlik C. An update on PYRIN domain-containing pattern recognition receptors: from immunity to pathology. Front Immunol. 2013;4(440):153–171. doi: 10.3389/fimmu.2013.00440
- Bernard NJ. Rheumatoid arthritis: Prevotella copri associated with new-onset untreated RA. Nat Rev Rheumatol. 2014;10(1):2. doi: 10.1038/nrrheum.2013.187
- Illescas O, Rodriguez-Sosa M, Gariboldi M. Mediterranean diet to prevent the development of colon diseases: a meta-analysis of gut microbiota studies. Nutrients. 2021;13(7):2234. doi: 10.3390/nu13072234
- Lavasani S, Dzhambazov B, Nouri M, 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
- Yamashita M., Ukibe K., Matsubara Y. et al. Lactobacillus helveticus SBT2171 attenuates experimental autoimmune encephalomyelitis in mice. Front Microbiol. 2018;8:2596. doi: 10.3389/fmicb.2017.02596
- Larsson E, Tremaroli V, Lee YS, et al. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut. 2012;61(8):1124–1131. doi: 10.1136/gutjnl-2011-301104
- Gandy K, Zhang J, Nagarkatti P, Nagarkatti M. The role of gut microbiota in shaping the relapse-remitting and chronic-progressive forms of multiple sclerosis in mouse models. Sci Rep. 2019;9(1):6923. doi: 10.1038/s41598-019-43356-7
- Lin X, Singh A, Shan X, et al. Akkermansia muciniphila-mediated degradation of host mucin expands the tryptophan utilizer alistipes and exacerbates autoimmunity by promoting Th17 immune responses. Cell Press. 2022. doi: 10.2139/ssrn.4065073
- Olsen I, Lambris JD, Hajishengallis G. Porphyromonas gingivalis disturbs host–commensal homeostasis by changing complement function. J Oral Microbiol. 2017;9(1):1340085. doi: 10.1080/20002297.2017.1340085
- Amano A. Disruption of epithelial barrier and impairment of cellular function by Porphyromonas gingivalis. Front Biosci. 2007;12:3965–3974. doi: 10.2741/2363
- Lee Y-K, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4615–4622. doi: 10.1073/pnas.1000082107
- Toivanen P, Vaahtovuo J, Eerola E. Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect Immun. 2001;69(4):2372–2377. doi: 10.1128/IAI.69.4.2372-2377.2001
- Kubinak JL, Zac Stephens W, Soto R, et al. MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection. Nat Commun. 2015;6:8642. doi: 10.1038/ncomms9642
- Gavalas E, Kountouras J, Boziki M, et al. Relationship between Helicobacter pylori infection and multiple sclerosis. Ann Gastroenterol. 2015;28(3):353–356.
- Lincoln MR, Montpetit A, Cader MZ, et al. A predominant role for the HLA class II region in the association of the MHC region with multiple sclerosis. Nat Genet. 2005;37(10):1108–1112. doi: 10.1038/ng1647
- Goris A, Pauwels I, Dubois B. Progress in multiple sclerosis genetics. Curr Genom. 2012;13(8):646–663. DOI: 10.2174/ 138920212803759695
- Alcina A, Abad-Grau Mdel M, Fedetz M, et al. Multiple sclerosis risk variant HLA-DRB1*1501 associates with high expression of DRB1 gene in different human populations. PLoS One. 2012;7(1):e29819. doi: 10.1371/journal.pone.0029819
- Shahi SK, Soham A, Jaime CM, et al. HLA class II polymorphisms modulate gut microbiota and EAE phenotype. Immunohorizons. 2022;5(8):627–646. doi: 10.4049/immunohorizons.2100024
- Li W, Minohara M, Su JJ, et al. Helicobacter pylori infection is a potential protective factor against conventional multiple sclerosis in the Japanese population. J Neuroimmunol. 2007;184(1–2):227–231. doi: 10.1016/j.jneuroim.2006.12.010
- Pedrini MJ, Seewann A, Bennett K.A. et al. Helicobacter pylori infection as a protective factor against multiple sclerosis risk in females. J Neurol Neurosurg Psychiatry. 2015;86(6):603–607. doi: 10.1136/jnnp-2014-309495
- Cook KW, Crooks J, Hussain K, et al. Helicobacter pylori infection reduces disease severity in an experimental model of multiple sclerosis. Front Microbiol. 2015;6:52. doi: 10.3389/fmicb.2015.00052
- Bonder MJ, Kurilshikov A, Tigchelaar EF, et al. The effect of host genetics on the gut microbiome. Nat Genet. 2016;48(11):1407–1412. doi: 10.1038/ng.3663
- Kurilshikov A, Medina-Gomez C, Bacigalupe R, et al. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat Genet. 2021;53(2):156–165. doi: 10.1038/s41588-020-00763-1
- Abdurasulova IN, Tarasova EA, Kudryavtsev IV, et al. Intestinal microbiota composition and peripheral blood Th cell subsets in patients with multiple sclerosis. Infect. Immun. 2019;9(3-4):504–522. (In Russ.) doi: 10.15789/2220-7619-2019-3-4-504-522
- Zhang Z, Wang M, Yuan S, et al. Genetically predicted milk intake and risk of neurodegenerative diseases. Nutrients. 2021;13(8):2893. doi: 10.3390/nu13082893
- Hall AB, Tolonen AC, Xavier RJ. Human genetic variation and the gut microbiome in disease. Nat Rev Genet. 2017;18(11):690–699. doi: 10.1038/nrg.2017.63
- Gampa A, Engen PA, Shobar R, Mutli EA. Relationships between gastrointestinal microbiota and blood group antigens. Physiol Genomics. 2017;49(9):473–483. doi: 10.1152/physiolgenomics.00043.2017
- Cosorich I, Dalla-Costa G, Sorini C. et al. High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci Adv. 2017;3(7):e1700492. doi: 10.1126/sciadv.1700492
- Berer K, Gerdes LA, Cekanaviciute E, et al. Gut Microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalitis in mice. Proc Natl Acad Sci USA. 2017;114(40):10719–10724. doi: 10.1073/pnas.1711233114
- Wu R, An J, Ding T et al. The level of peripheral regulatory T cells is associated with the changes of intestinal microbiota in patients with rheumatoid arthritis. Ann Rheumatic Dis. 2021;80(Suppl 1):427. POS0396. doi: 10.1136/annrheumdis-2021-eular.2783
- Shahi SK, Freedman SN, Mangalam AK. Gut microbiome in multiple sclerosis: The players involved and the roles they play. Gut Microbes. 2017;8(6):607–615. doi: 10.1080/19490976.2017.1349041
- Saresella M, Marventano I, Barone M, et al. Alterations in circulating fatty acid are associated with gut microbiota dysbiosis and inflammation in multiple sclerosis. Front Immunol. 2020;11:1390. doi: 10.3389/fimmu.2020.01390
- Zhang Y-J, Zhang L, Chen S-Y, et al. Association between VDR polymorphisms and multiple sclerosis: systematic review and updated meta-analysis of case-control studies. Neurol Sci. 2018;39(2):225–234. doi: 10.1007/s10072-017-3175-3
- Eftekharian MM, Azimi T, Ghafouri-Fard S, et al. Phospholipase D1 expression analysis in relapsing-remitting multiple sclerosis patients. Neurol Sci. 2017;38(5):865–872. doi: 10.1007/s10072-017-2857-1
- Göbel K, Schuhmann MK, Pankratz S, et al. Phospholipase D1 mediates lymphocyte adhesion and migration in experimental autoimmune encephalomyelitis. Eur J Immunol. 2014;44(8):2295–2305. doi: 10.1002/eji.201344107
- Ahn M, Min DS, Kang J, et al. Increased expression of phospholipase D1 in the spinal cords of rats with experimental autoimmune encephalomyelitis. Neurosci Lett. 2001;316(2):95–98. doi: 10.1016/s0304-3940(01)02383-7
- Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54:1469–1476. doi: 10.1099/ijs.0.02873-0
- Levi I, Gurevich M, Perlman G, et al. Potential role of indolelactate and butirate in multiple sclerosis revealed by integrated microbiome-metabolome analysis. Cell Rep Med. 2021;2(4):100246. doi: 10.1016/j.xcrm.2021.100246
- Bell ME, Bernard KA, Harrington SM, et al. Lawsonella clevelandensis gen. nov., sp. nov., a new member of the suborder Corynebacterineae isolated from human abscesses. Int J Evol Microbiol. 2016;66(8):2929–2935. doi: 10.1099/ijsem.0.001122
- Alonso R, Pisa D, Carrasco K. Searching for bacteria in neural tissue from amyotrophic lateral sclerosis. Front Neurosci. 2019;13:171. doi: 10.3389/fnins.2019.00171
- Abdurasulova IN, Dmitriev AV. Group B vitamins: From homeostasis to pathogenesis and treatment of multiple sclerosis Adv Physiol Sci. 2023;54(1). (In Russ.) doi: 10.31857/S0301179823010034
- Montgomery TL, Künstner A, Kennedy JJ et al. Interactions between host genetics and gut microbiota determine susceptibility to CNS autoimmunity. Proc Natl Acad Sci USA. 2020;117(44):27516–27527. doi: 10.1073/pnas.2002817117
- Rodríguez JM, Murphy K, Stranton CS, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26(1):26050. doi: 10.3402/mehd.v26.26050
- Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703. doi: 10.1016/j.chom.2015.04.004
- Köenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiom. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4578–4585. doi: 10.1073/pnas.1000081107
- La Rosa PS, Warner BB, Zhou Y, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci USA. 2014;111(34):12522–12527. doi: 10.1073/pnas.1409497111
- Falk PG, Hooper LV, Midtverd T, Gordon JI. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev. 1998;62(4):1157–1170. doi: 10.1128/MMBR.62.4.1157-1170.1998
- Perez-Muñoz ME, Arrieta M-C, Ramer-Tait AE, Walter J. A critical assessment of the sterile womb and in utero colonization hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017;5(1):48. doi: 10.1186/s40168-017-0268-4
- Cooperstock MSZ, Zedd AJ. Intestinal flora of infants. In: Human intestinal microflora in health and disease. Ed. by D.J. Hentges. 1983. Chapter 4. P. 79–99. doi: 10.1016/B978-0-12-341280-5.50010-0
- Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra65. doi: 10.1126/scitranslmed.3008599
- Collado MC, Rautava S, Aakko J, et al. Human gut colonization may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;6:23129. doi: 10.1038/srep23129
- Satokari R, Gronroos T, Laitinen K, et al. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol. 2009;48(1):8–12. doi: 10.1111/j.1472-765X.2008.02475.x
- Parnell LA, Briggs CM, Cao B, et al. Microbial communities in placentas from term normal pregnancy exhibit spatially variable profiles. Sci Rep. 2017;7(1):11200. doi: 10.1038/s41598-017-11514-4
- Mueller NT, Bakacs E, Combellick J, et al. The infant microbiome development: Mom matters. Trends Mol Med. 2015;21(2):109–117. doi: 10.1016/j.molmed.2014.12.002
- Jimenez E, Fernandez L, Marin ML, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005;51(4):270–274. doi: 10.1007/s00284-005-0020-3
- Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid microorganism infection and microflora in the mouth. BJOG. 2002;109(5):527–533. doi: 10.1111/j.1471-0528.2002.01349.x
- DiGiulio DB. Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med. 2012;17(1):2–11. doi: 10.1016/j.siny.2011.10.001
- Rautava S, Collado MC, Salminen S, Isolauri E. Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology. 2012;102(3):178–184. doi: 10.1159/000339182
- Steel JH, Malatos S, Kennea N, et al. Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor. Pediatr Res. 2005;57(3):404–411. doi: 10.1203/01.PDR.0000153869.96337.90
- Vazquez-Torres A, Jones-Carson J, Baumler AJ et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature. 1999;401(6755):804–808. doi: 10.1038/44593
- Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001;204(5):572–581. doi: 10.1078/0171-2985-00094
- Perez PF, Dore J, Leclerc M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007;119(3):e724–e732. doi: 10.1542/peds.2006-1649
- Gosalbes MJ, Abellan JJ, Durbán A, et al. Metagenomics of human microbiome: beyond 16s rDNA. Clin Microbiol Infect. 2012;18 Suppl(4):47–49. doi: 10.1111/j.1469-0691.2012.03865.x
- Mold JE, Michaëlsson J, Burt TD, et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science. 2008;322(5907):1562–1565. doi: 10.1126/science.1164511
- Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470–480. doi: 10.1016/j.cell.2012.07.008
- Donnet-Hughes A, Perez PF, Doré J, et al. Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc. 2010;69(3):407–415. doi: 10.1017/S0029665110001898
- Collado MC, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res. 2012;72(1):77–85. doi: 10.1038/pr.2012.42
- Matamoros S, Gras-Leguen C, Le Vacon F, et al. Development of intestinal microbiota in infants and its impact on health.Trends Microbiol. 2013;21(4):167–173. doi: 10.1016/j.tim.2012. 12.001
- Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107(26):11971–11975. doi: 10.1073/pnas.1002601107
- Fernandez L, Langa S, Martin V, et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res. 2013;69:1–10. doi: 10.1016/j.phrs.2012.09.001
- Sanz Y. Gut microbiota and probiotics in maternal and infant health. Am J Clin Nutr. 2011;94(Suppl 6):2000S–2005S. doi: 10.3945/ajcn.110.001172
- Hunt KM, Foster JA, Forney LJ, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One. 2011;6(6):e21313. doi: 10.1371/journal.pone.0021313
- Cabrera-Rubio R, Collado MC, Laitinen K, et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96(3):544–551. doi: 10.3945/ajcn.112.037382
- Hyman RW, Fukushima M, Diamond L, et al. Microbes on the human vaginal epithelium. Proc Natl Acad Sci USA. 2005;102(22):7952–7957. doi: 10.1073/pnas.0503236102
- Zhou X, Brown CJ, Abdo Z, et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 2007;1(2):121–133. doi: 10.1038/ismej.2007.12
- Palmer C, Bik EM, Di Giulio DB, et al. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5(7):e177. doi: 10.1371/journal.pbio.0050177
- Vael C, Desager K. The importance of the development of the intestinal microbiota in infancy. Curr Opin Pediatr. 2009;21(6):794–800. doi: 10.1097/MOP.0b013e328332351b
- Quigley EMM. Gut bacteria in health and disease. Gastroenterol Hepatol (NY). 2013;9(9):560–569.
- Mackie RI., Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999;69(5):1035S–1045S. doi: 10.1093/ajcn/69.5.1035s
- O’Toole PW, Claesson MJ. Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J. 2010;20(4):281–291. doi: 10.1016/j.idairyj.2009.11.010
- Balmer SE, Hanvey LS, Wharton BA. Diet and faecal flora in the newborn: nucleotides. Arch Dis Child Fetal Neonatal Ed. 1994;70(2):F137–F140. doi: 10.1136/fn.70.2.f137
- Bennet R, Nord CE. Development of the faecal anaerobic microflora after caesarean section and treatment with antibiotics in newborn infants. Infection. 1987;15(5):332–336. doi: 10.1007/bf01647733
- Ruiz VE, Battaglia T, Kurtz ZD, et al. A single early-in-life macrolide course has lasting effects on murine microbial network topology and immunity. Nat Commun. 2017;8:518. doi: 10.1038/s41467-017-00531-6
- Lynn MA, Tumes DJ, Choo JM et al. Early-life antibiotic-driven dysbiosis leads to dysregulated vaccine immune responses in mice. Cell Host Microbe. 2018;23:653–660.e5. doi: 10.1016/j.chom.2018.04.009
- Dinan TG, Cryan JF. Gut instincts: Microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol. 2017;595(2):489–503. doi: 10.1113/JP273106
- Korpela K, Salonen A, Virta LJ, et al. Intestinal microbiome is related to lifetime antibiotic use in finnish pre-school children. Nat Commun. 2016;7:10410. doi: 10.1038/ncomms10410
- Maghzi AH, Ghazavi H, Ahsan M, et al. Increasing female preponderance of multiple sclerosis in Isfahan, Iran: a population-based study. Mult Scler. 2010;16(3):359–361. doi: 10.1177/1352458509358092
- Di Giulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3(8):e3056. doi: 10.1371/journal.pone.0003056
- Wahlberg J, Fredriksson J, Nikolic E, et al. Environmental factors related to the induction of beta cell autoantibodies in 1-yr-old healthy children. Pediatr Diabetes. 2005;6(4):199–205. doi: 10.1111/j.1399-543X.2005.00129.x
- Beijers R, Jansen J, Riksen-Walraven M, de Weerth C. Maternal prenatal anxiety and stress predict infant illnesses and health complaints. Pediatrics. 2010;12(2):e401–e409. doi: 10.1542/peds.2009-3226
- Aoyama K, Seaward PG, Lapinsky SE. Fetal outcome in the critically ill pregnant woman. Crit Care. 2014;18(3):307. doi: 10.1186/cc13895
- Mor G, Cardenas I. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol. 2010;63(6):425–433. doi: 10.1111/j.1600-0897.2010.00836.x
- Gomes de Agüero M, Ganal-Vonarburg SC, Fuhrer T, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;361(6279):1296–1302. doi: 10.1126/science.aad2571
- Kabat AM, Srinivasan N, Maloy KJ. Modulation of immune development and function by intestinal microbiota. Trends Immunol. 2014;35(11):507–517. doi: 10.1016/j.it.2014.07.010
- Cortessis VK, Thomas DC, Levine AJ, et al. Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. Hum Genet. 2012;131(10):1565–1589. doi: 10.1007/s00439-012-1189-8
- Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rew Gen. 2007;8(4):253–262. doi: 10.1038/nrg2045
- Perera F, Herbstman J. Prenatal environmental exposures, epigenetics, and disease. Reprod Toxicol. 2011;31(3):363–373. doi: 10.1016/j.reprotox.2010.12.055
- Luo A, Leach ST, Barres R, et al. The microbiota and epigenetic regulation of T helper 17 / regulatory T cells: in search of a balanced immune system. Front Immunol. 2017;8:417. doi: 10.3389/fimmu.2017.00417
- Zager A, Peron JP, Mennecier G, et al. Maternal immune activation in late gestation increases neuroinflammation and aggravates experimental autoimmune encephalomyelitis in the offspring. Brain Behav Immun. 2015;43:159–171. doi: 10.1016/j.bbi.2014.07.021
- Mandal M, Donnelly R, Elkabes S, et al. Maternal immune stimulation during pregnancy shapes the immunological phenotype of offspring. Brain Behav Immun. 2013;33:33–45. doi: 10.1016/j.bbi.2013.04.012
- Solati J, Asiaei M, Hoseini MH. Using experimental autoimmune encephalomyelitis as a model to study the effect of prenatal stress on fetal programming. Neurol Res. 2012;34(5):478–483. doi: 10.1179/1743132812Y.0000000032
- Stanisavljević S, Čepić A, Bojić S, et al. Oral neonatal antibiotic treatment perturbs gut microbiota and aggravates central nervous system autoimmunity in Dark Agouti rats. Sci Rep. 2019;9(1):918. doi: 10.1038/s41598-018-37505-7
- Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, et al. Role of gut commensal microfora in the development of experimental autoimmune encephalomyelitis. J Immunol. 2009;183(10):6041–6050. doi: 10.4049/jimmunol.0900747
- Ochoa-Reparaz J, Mielcarz DW, Haque-Begum S, Kasper LH. Induction of a regulatory B cell population in experimental allergic encephalomyelitis by alteration of the gut commensal microbiora. Gut Microbes. 2010;1(2):103–108. doi: 10.4161/gmic.1.2.11515
- Yokote H, Miyake S, Croxford JL, et al. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut microflora. Am J Pathol. 2008;173(6):1714–1723. doi: 10.2353/ajpath.2008.080622
- Graves JS, Chitnis T, Weinstock-Guttman B, et al. Maternal and perinatal exposures are associated with risk for pediatric-onset multiple sclerosis. Pediatrics. 2017;139(4):e20162838. doi: 10.1542/peds.2016-2838
- Corsini E, Sokooti M, Galli CL, et al. Pesticide induced immunotoxicity in humans: a comprehensive review of the existing evidence. Toxicology. 2013;307:123–135. doi: 10.1016/j.tox.2012.10.009
- Mokarizadeh A, Faryabi MR, Rezvanfar MA, Abdollahi M. A comprehensive review of pesticides and the immune dysregulation: mechanisms, evidence and consequences. Toxicol Mech Methods. 2015;25(4):258–278. doi: 10.3109/15376516.2015.1020182
- Barrett E, Guinane CM, Ryan CA, et al. Microbiota diversity and stability of the preterm neonatal ileum and colon of two infants. Microbiologyopen. 2013;2(2):215–225. doi: 10.1002/mbo3.64
- Barrett E, Deshpandey AK, Ryan CA, et al. The neonatal gut harbours distinct bifidobacterial strains. Arch Dis Child Fetal Neonatal Ed. 2015;100(5):F405–F410. doi: 10.1136/archdischild-2014-306110
- Goldacre A, Pakpoor J, Goldacre M. Maternal and perinatal characteristics of infants who, later in life, developed multiple sclerosis: Record-linkage study. Mult Scler Relat Disord. 2017;13:98–102. doi: 10.1016/j.msard.2017.02.004
- Ramagopalan SV, Valdar W, Dyment DA, et al. Canadian collaborative study group. no effect of preterm birth on the risk of multiple sclerosis: a population based study. BMC Neurol. 2008;8:30. doi: 10.1186/1471-2377-8-30
- Maghzi A-H, Etemadifar M, Heshmat-Ghahdarijani K, et al. Cesarean delivery may increase the risk of multiple sclerosis. Mult Scler J. 2012;18(4):468–471. doi: 10.1177/1352458511424904
- Conradi S, Malzahn U, Paul F, et al. Breastfeeding is associated with lower risk for multiple sclerosis. Mult Scler. 2013;19(5):553–558. doi: 10.1177/1352458512459683
- Norgaard M, Nielsen RB, Jacobsen JB, et al. Use of penicillin and other antibiotics and risk of multiple sclerosis: a population-based case-control study. Am J Epidemiol. 2011;174(8):945–948. doi: 10.1093/aje/kwr201
- Zeissig S, Blumberg RS. Life at the beginning: perturbation of the microbiota by antibiotics in early life and its role in health and disease. Nat Immunol. 2014;15(4):307–310. doi: 10.1038/ni.2847
- Neu J, Rushing J. Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis. Clin Perinatol. 2011;38(2):321–331. doi: 10.1016/j.clp.2011.03.008
- Bokulich NA, Chung J, Battaglia T, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82. doi: 10.1126/scitranslmed.aad7121
- Yassour M, Vatanen T, Siljander H, et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016;8(343):343ra81. doi: 10.1126/scitranslmed.aad0917
- Salminen S, Gibson G, McCartney A, Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut. 2004;53(9):1388–1389. doi: 10.1136/gut.2004.041640
- Goedert JJ, Hua X, Yu G, Shi J. Diversity and composition of the adult fecal microbiome associated with history of cesarean birth or appendectomy: Analysis of the American Gut Project. EBioMedicine. 2014;1(2-3):167–172. doi: 10.1016/j.ebiom.2014.11.004
- Blaser MJ, Dominguez-Bello MG. The human microbiome before birth. Cell Host Microbe. 2016;20(5):558–560. doi: 10.1016/j.chom.2016.10.014
- Dalla Costa G, Romeo M, Esposito F, et al. Caesarean section and infant formula feeding are associated with an earlier age of onset of multiple sclerosis. Mult Scler Relat Disord. 2019;33:75–77. doi: 10.1016/j.msard.2019.05.010
- Nielsen NM, Bager P, Stenager E, et al. Cesarean section and offspring’s risk of multiple sclerosis: a Danish nationwide cohort study. Mult Scler. 2013;19(11):1473–1477. doi: 10.1177/1352458513480010
- Boehm G, Moro G. Structural and functional aspects of prebiotics used in infant nutrition. J Nutr. 2008;138(9):1818S–1828S. doi: 10.1093/jn/138.9.1818S
- Walker A. Breast milk as the gold standard for protective nutrients. J Pediatr. 2010;156(2 Suppl):S3–S7. doi: 10.1016/j.jpeds.2009.11.021
- Fernandez L, Langa S, Martin V, et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res. 2013;69(1):1–10. doi: 10.1016/j.phrs.2012.09.001
- Andersson B, Porras O, Hanson LA, et al. Inhibition of attachment of Streptococcus pneumoniae and Haemophilus influenzae by human milk and receptor oligosaccharides. J Infect Dis. 1986;153(2):232–237. doi: 10.1093/infdis/153.2.232
- Cravioto A, Tello A, Villafan H, et al. Inhibition of localized adhesion of enteropathogenic Escherichia coli to HEp-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. J Infect Dis. 1991;163(6):1247–1255. doi: 10.1093/infdis/163.6.1247
- Gueimonde M, Laitinen K, Salminen S, Isolauri E. Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology. 2007;92(1):64–66. doi: 10.1159/000100088
- Martín R, Heilig G, Zoetendal E, et al. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J Appl Microbiol. 2007;103(6):2638–2644. doi: 10.1111/j.1365-2672.2007.03497.x
- Penders J, Vink C, Driessen C, et al. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett. 2005;243(1):141–147. doi: 10.1016/j.femsle.2004.11.052
- Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe. 2011;17(6):478–482. doi: 10.1016/j.anaerobe.2011. 03.009
- Ezendam J, de Klerk A, Gremmer ER, van Loveren H. Effects of Bifidobacterium animalis administered during lactation on allergic and autoimmune responses in rodents. Clin Exp Immunol. 2008;154(3):424–431. doi: 10.1111/j.1365-2249.2008.03788.x
- Ezendam J, van Loveren H. Lactobacillus casei Shirota administered during lactation increases the duration of autoimmunity in rats and enhances lung inflammation in mice. Br J Nutr. 2008;99(1):83–90. doi: 10.1017/S0007114507803412
- Conradi S, Malzahn U, Paul F, et al. Breastfeeding is associated with lower risk for multiple sclerosis. Mult Scler. 2013;19(5):553–558. doi: 10.1177/1352458512459683
- Brenton JN, Engel CE, Sohn MW, Goldman MD. Breastfeeding during infancy is associated with a lower future risk of pediatric multiple sclerosis. Pediart Neurol. 2017;77:67–72. doi: 10.1016/j.pediatrneurol.2017.09.007
- Pisacane A, Impagliazzo N, Russo M, et al. Breast feeding and multiple sclerosis. BMJ. 1994;308(6941):1411–1412. doi: 10.1136/bmj.308.6941.1411
- Ragnedda G, Leoni S, Parpinel M, et al. Reduced duration of breastfeeding is associated with a higher risk of multiple sclerosis in both Italian and Norwegian adult males: the EnvI MS study. J Neurol. 2015;262(5):1271–1277. doi: 10.1007/s00415-015-7704-9
- Simon AK, Hollander GA, McMichael A. Evolution of the immune system in humans from infancy to old age. Proc Biol Sci. 2015;282(1821):20143085. doi: 10.1098/rspb.2014.3085
- Martin R, Nauta AJ, Ben Amor K, et al. Early life: Gut microbiota and immune development in infancy. Benef Microbes. 2010;1(4):367–382. doi: 10.3920/BM2010.0027
- Kamada N, Seo S-U, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321–335. doi: 10.1038/nri3430
- Kamada N, Núñez G. Regulation of the immune system by the resident intestinal bacteria. Gastroenterology. 2014;146(6):1477–1488. doi: 10.1053/j.gastro.2014.01.060
- Vatanen T, Kostic AD, d’Hennezel E, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165(4):842–853. doi: 10.1016/j.cell.2016.04.007
- Wang Z-W, Wang P, Lin F-H. Early-life exposure to lipopolysaccharide reduces the severity of experimental autoimmune encephalomyelitis in adulthood and correlated with increased urine corticosterone and apoptotic CD4+ T cells. Neuroscienci. 2011;193:283–290. doi: 10.1016/j.neuroscience.2011.07.047
- Ellestad KK, Tsutsui S, Noorbakhsh F, et al. Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J Immunol. 2009;183(1):298–309. doi: 10.4049/jimmunol.0803576
- Abdurasulova IN, Zubareva OE, Zhitnukhin Yu.L, et al. The course of experimental allergic encephalomyelitis in adult rats after administration of interleukin-1β at different periods in early life. J Neurosci Behav Physiol. 2015;46(7):794–802. doi: 10.1007/s11055-016-0313-y
- Bakker JM, Kavelaars A, Kamphuis PJGH, et al. Neonatal dexamethasone treatment increases susceptibility to experimental autoimmune disease in adult rats. J Immunol. 2000;165(10):5932–5937. doi: 10.4049/jimmunol.165.10.5932
- Stephan M, Straub RH, Breivik T, et al. Postnatal maternal deprivation aggravates experimental autoimmune encephalomyelitis in adult Lewis rats: reversal by chronic imipramine treatment. Int J Devl Neurosi. 2002;20(2):125–132. doi: 10.1016/s0736-5748(02)00007-2
- Teunis MAT, Heijnen CJ, Sluyter F, et al. Maternal deprivation of rat pups increases clinical symptoms of experimental autoimmune encephalomyelitis at adult age. J Neuroimmunol. 2002;133(1-2):30–38. doi: 10.1016/s0165-5728(02)00351-x
- Laban O, Dimitrijevic M, von Hoersten S, et al. Experimental allergic encephalomyelitis in adult DA rats subjected to neonatal handling or gentling. Brain Res. 1995;676(1):133–140. doi: 10.1016/0006-8993(95)00106-z
- Dimitrijevic M, Laban O, von Hoersten S, et al. Neonatal sound stress and development of experimental allergic encephalomyelitis in Lewis and DA rats. Int J Neurosci. 1994;78(1-2):135–143. doi: 10.3109/00207459408986052
- Columba-Cabezas S, Iaffaldano G, Chiarotti F, et al. Early handling increases susceptibility to experimental autoimmune encephalomyelitis (EAE) in C57BL/6 male mice. J Neuroimmunol. 2009;212(1-2):10–16. doi: 10.1016/j.jneuroim.2009.05.007
- Golubeva AV, Crampton S, Desbonnet L, et al. Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood. Psychoneuroendocrinol. 2015;60:58–74. doi: 10.1016/j.psyneuen.2015.06.002
- Zijlmans MAC, Korpela K, Riksen-Walravena JM, et al. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinol. 2015;53:233–245. doi: 10.1016/j.psyneuen.2015.01.006
- Bailey MT, Lubach GR, Coe CL. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr. 2004;38(4):414–421. doi: 10.1097/00005176-200404000-00009
- Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol. 1999;35(2):146–155.
- Bokulich NA, Chung J, Battaglia T, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82. doi: 10.1126/scitranslmed.aad7121
- Miller JE, Wu C, Pedersen LH, et al. Maternal antibiotic exposure during pregnancy and hospitalization with infection in offspring: a population-based cohort study. Int J Epidemiol. 2018;47(2):561–571. doi: 10.1093/ije/dyx272
- Keogh CE, Kim DHJ, Pusceddu MM, et al. Myelin as a regulator of development of the microbiota – gut – brain axis. Brain Behav Immun. 2021;91:437–450. doi: 10.1016/j.bbi.2020.11.001
- Mirzaei F, Michels KB, Munger K, et al. Gestational vitamin D and the risk of multiple sclerosis in offspring. Ann Neurol. 2011;70(1):30–40. doi: 10.1002/ana.22456
- Fernandes de Abreu DA, Ibrahim EC, Boucraut J, et al. Severity of experimental autoimmune encephalomyelitis is unexpectedly reduced in mice born to vitamin D-deficient mothers. J Steroid Biochem Mol Biol. 2010;121(1-2):250–253. doi: 10.1016/j.jsbmb.2010.03.006
- Fernandes de Abreu DA, Landel V, Barnett AG. Prenatal vitamin D deficiency induces an early and more severe experimental autoimmune encephalomyelitis in the second generation. Int J Mol Sci. 2012;13(9):10911–10919. doi: 10.3390/ijms130910911
- Fernandes de Abreu DA, Landel V, Feron F. Seasonal, gestational and postnatal influences on multiple sclerosis: the beneficial role of a vitamin D supplementation during early life. J Neurol Sci. 2011;311(1-2):64–68. doi: 10.1016/j.jns.2011.08.044
- Adzemovic MZ, Zeitelhofer M, Hochmeister S, et al. Efficacy of vitamin D in treating multiple sclerosis-like neuroinflammation depends on developmental stage. Exp Neurol. 2013;249:39–48. doi: 10.1016/j.expneurol.2013.08.002
- Biesalski HK. Nutrition meets the microbiome: Micronutrients and the microbiota. Ann NY Acad Sci. 2016;1372(1):53–64. doi: 10.1111/nyas.13145
- Smith AD, Kim YI, Refsum H. Is folic acid good for everyone? Am J Clin Nutr. 2008;87(3):517–533. doi: 10.1093/ajcn/87.3.517
- Nagy-Szakal D, Ross MC, Dowd SE, et al. Maternal micronutrients can modify colonic mucosal microbiota matuartation in murien offspring. Gut Microbes. 2012;3(5):426–433. doi: 10.4161/gmic.20697
- Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, et al. Periconceptional maternal folic acid use of 400 g per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One. 2009;4(11):e7845. doi: 10.1371/journal.pone.0007845
- Collado MC, Cernada M, Baüerl C, et al. Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes. 2012;3(4):352–365. doi: 10.4161/gmic.21215
Supplementary files
