Gut microbiota and probiotics: novel immune system modulators in myasthenia gravis?

Annals of the New York Academy of Sciences

Volumn 1413, Issue 1, 2018, Pages 49-58

  Rinaldi, Elena ^a   Consonni, Alessandra ^a   Guidesi, Elena ^b   Elli, Marina ^b   Mantegazza, Renato ^a   Baggi, Fulvio ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

^b AAT Advanced Analytical Technologies Srl   (Italy)

Author keywords

autoimmune diseases; experimental autoimmune myasthenia gravis; immunomodulation; microbiota; probiotics

Indexed keywords

IMMUNOMODULATING AGENT; PROBIOTIC AGENT; IMMUNOLOGIC FACTOR;

ADJUVANT THERAPY; AUTOIMMUNE DISEASE; CLINICAL EFFECTIVENESS; CLINICAL TRIAL (TOPIC); COMMENSAL; DRUG EFFICACY; HUMAN; IMMUNE SYSTEM; IMMUNOMODULATION; INTESTINE; INTESTINE FLORA; MICROFLORA; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; NONHUMAN; REVIEW; RHEUMATOID ARTHRITIS; ANIMAL; DISEASE MODEL; DYSBIOSIS; IMMUNOLOGY; SYMBIOSIS;

ANIMALS; ARTHRITIS, RHEUMATOID; DISEASE MODELS, ANIMAL; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNOLOGIC FACTORS; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; PROBIOTICS; SYMBIOSIS;

EID: 85040741607     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.13567     Document Type: Review

References (57)

1. Cerf-Bensussan, N. & V. Gaboriau-Routhiau. 2010. The immune system and the gut microbiota: friends or foes? Nat. Rev. Immunol. 10: 735–744.
2. Peterson, L.W. & D. Artis. 2014. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14: 141–153.
3. Donaldson, G.P., S.M. Lee & S.K. Mazmanian. 2015. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14: 20–32.
4. Bevins, C.L. & N.H. Salzman. 2011. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat. Rev. Microbiol. 9: 356–368.
5. Mabbott, N.A., D.S. Donaldson, H. Ohno, et al. 2013. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 6: 666–677.
6. Mantis, N.J., N. Rol & B. Corthésy. 2011. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4: 603–611.
7. Blander, J.M. & L.E. Sander. 2012. Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 12: 215–225.
8. Lee, J., J.-H. Mo, K. Katakura, et al. 2006. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell Biol. 8: 1327–1336.
9. + , antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206: 3101–3114.
10. + dendritic cells. Immunity 40: 248–261.
11. + regulatory T cells via a TGF-β– and retinoic acid–dependent mechanism. J. Exp. Med. 204: 1757–1764.
12. Mann, E.R. & X. Li. 2014. Intestinal antigen-presenting cells in mucosal immune homeostasis: crosstalk between dendritic cells, macrophages and B-cells. World J. Gastroenterol. 20: 9653–9664.
13. Rimoldi, M., M. Chieppa, V. Salucci, et al. 2005. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6: 507–514.
14. Honda, K. & D.R. Littman. 2016. The microbiota in adaptive immune homeostasis and disease. Nature 535: 75–84.
15. Lécuyer, E., S. Rakotobe, H. Lengliné-Garnier, et al. 2014. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 40: 608–620.
16. Ivanov, I.I., K. Atarashi, N. Manel, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485–498.
17. Wu, H.-J.J., I.I. Ivanov, J. Darce, et al. 2010. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32: 815–827.
18. Hill, C., F. Guarner, G. Reid, et al. 2014. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11: 506–514.
19. Gallo, A., G. Passaro, A. Gasbarrini, et al. 2016. Modulation of microbiota as treatment for intestinal inflammatory disorders: an uptodate. World J. Gastroenterol. 22: 7186–7202.
20. Konieczna, P., C.A. Akdis, E.M.M. Quigley, et al. 2012. Portrait of an immunoregulatory Bifidobacterium. Gut Microbes 3: 1–6.
21. López, P., I. González-Rodríguez, B. Sánchez, et al. 2012. Interaction of Bifidobacterium bifidum LMG13195 with HT29 cells influences regulatory-T-cell-associated chemokine receptor expression. Appl. Environ. Microbiol. 78: 2850–2857.
22. Tobita, K., H. Yanaka, H. Otani, et al. 2010. Lactobacillus crispatus KT-11 enhances intestinal immune functions in C3H/HeN mice. J. Nutr. Sci. Vitaminol. 56: 441–445.
23. Vargas Garcìa, C.E., M. Petrova, I.J.J. Claes, et al. 2015. Piliation of Lactobacillus rhamnosus GG promotes adhesion, phagocytosis, and cytokine modulation in macrophages. Appl. Environ. Microbiol. 81: 2050–2062.
24. Schlee, M., J. Harder, B. Köten, et al. 2008. Probiotic lactobacilli and VSL#3 induce enterocyte β-defensin 2. Clin. Exp. Immunol. 151: 528–535.
25. Abhari, K., S.S. Shekarforoush, S. Hosseinzadeh, et al. 2016. The effects of orally administered Bacillus coagulans and inulin on prevention and progression of rheumatoid arthritis in rats. Food Nutr. Res. 60: 30876.
26. Kwon, H.-K., G.-C. Kim, Y. Kim, et al. 2013. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin. Immunol. 146: 217–227.
27. de Oliveira, G.L.V., A.Z. Leite, B.S. Higuchi, et al. 2017. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology 152: 1–12.
28. Catrina, A.I., C.I. Svensson, V. Malmström, et al. 2016. Mechanisms leading from systemic autoimmunity to joint-specific disease in rheumatoid arthritis. Nat. Rev. Rheumatol. 13: 79–86.
29. Liu, X., B. Zeng, J. Zhang, et al. 2016. Role of the gut microbiome in modulating arthritis progression in mice. Sci. Rep. 6: 30594.
30. Simelyte, E., M. Rimpiläinen, X. Zhang, et al. 2003. Role of peptidoglycan subtypes in the pathogenesis of bacterial cell wall arthritis. Ann. Rheum. Dis. 62: 976–982.
31. Vaahtovuo, J., E. Munukka, M. Korkeamaki, et al. 2008. Fecal microbiota in early rheumatoid arthritis. J. Rheumatol. 35: 1500–1505.
32. Chen, J., K. Wright, J.M. Davis, et al. 2016. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med. 8: 43.
33. Pianta, A., S.L. Arvikar, K. Strle, et al. 2017. Two rheumatoid arthritis-specific autoantigens correlate microbial immunity with autoimmune responses in joints. J. Clin. Invest. 127: 2946–2956.
34. Vaghef-Mehrabany, E., B. Alipour, A. Homayouni-Rad, et al. 2014. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis. Nutrition 30: 430–435.
35. Vaghef-Mehrabany, E., L. Vaghef-Mehrabany, M. Asghari-Jafarabadi, et al. 2017. Effects of probiotic supplementation on lipid profile of women with rheumatoid arthritis: a randomized placebo-controlled clinical trial. Health Promot. Perspect. 7: 95–101.
36. Tan, T.G., E. Sefik, N. Geva-Zatorsky, et al. 2016. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc. Natl. Acad. Sci. USA 113: E8141–E8150.
37. Mandel, D.R., K. Eichas & J. Holmes. 2010. Bacillus coagulans: a viable adjunct therapy for relieving symptoms of rheumatoid arthritis according to a randomized, controlled trial. BMC Complement. Altern. Med. 10: 1.
38. Pan, H., R. Li, T. Li, et al. 2017. Whether probiotic supplementation benefits rheumatoid arthritis patients: a systematic review and meta-analysis. Engineering 3: 115–121.
39. Berer, K., M. Mues, M. Koutrolos, et al. 2011. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479: 538–541.
40. Stanisavljević, S., J. Lukić, S. Soković, et al. 2016. Correlation of gut microbiota composition with resistance to experimental autoimmune encephalomyelitis in rats. Front. Microbiol. 7: 2005.
41. Cosorich, I., G. Dalla-Costa, C. Sorini, et al. 2017. High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci. Adv. 3: 1–9.
42. Jangi, S., R. Gandhi, L.M. Cox, et al. 2016. Alterations of the human gut microbiome in multiple sclerosis. Nat. Commun. 7: 12015.
43. Berer, K., L.A. Gerdes, E. Cekanaviciute, et al. 2017. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc. Natl. Acad. Sci. USA 114: 10719–10724.
44. Cekanaviciute, E., B.B. Yoo, T.F. Runia, et al. 2017. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci. USA 114: 10713–10718.
45. Lavasani, S., B. Dzhambazov, M. Nouri, et al. 2010. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One 5: e9009.
46. + T cell subset balance. Biomed. Pharmacother. 95: 1535–1548.
47. Secher, T., S. Kassem, M. Benamar, et al. 2017. Oral administration of the probiotic strain Escherichia coli Nissle 1917 reduces susceptibility to neuroinflammation and repairs experimental autoimmune encephalomyelitis-induced intestinal barrier dysfunction. Front. Immunol. 8: 1096.
48. Kouchaki, E., O.R. Tamtaji, M. Salami, et al. 2017. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin. Nutr. 36: 1245–1249.
49. Berrih-Aknin, S. 2014. Myasthenia gravis: paradox versus paradigm in autoimmunity. J. Autoimmun. 52: 1–28.
50. low/− T cells in patients with myasthenia gravis. Clin. Immunol. 145: 209–223.
51. Gradolatto, A., D. Nazzal, F. Truffault, et al. 2014. Both Treg cells and Tconv cells are defective in the myasthenia gravis thymus: roles of IL-17 and TNF-α. J. Autoimmun. 52: 53–63.
52. + T regulatory cell subsets in myasthenia gravis patients. Clin. Immunol. 179: 40–46.
53. Dalakas, M.C. 2013. Novel future therapeutic options in myasthenia gravis. Autoimmun. Rev. 12: 936–941.
54. + T cells in the thymus of patients with autoimmune myasthenia gravis. Blood 105: 735–741.
55. Chae, C.-S., H.-K. Kwon, J.-S. Hwang, et al. 2012. Prophylactic effect of probiotics on the development of experimental autoimmune myasthenia gravis. PLoS One 7: e52119.
56. Cordiglieri, C., R. Marolda, M. Elli, et al. 2014. Probiotics as immune-regulators in the rat experimental autoimmune encephalomyelitis and myasthenia gravis models. In 15th International Congress of Immunology. 1–8. Bologna: Medimond.
57. + T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. USA 107: 2159–2164.