W poszukiwaniu źródeł – rola flory jelitowej w zdrowiu i chorobie. Część II – mikrobiom jelitowy a stwardnienie rozsiane Artykuł przeglądowy
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Opublikowane:
gru 31, 2015
Słowa kluczowe:
mikrobiom jelitowy, stwardnienie rozsiane, autoimmunizacja, transfer flory jelitowej, kolonizacja jelita
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Abstrakt
Dzięki zdobyczom technologicznym i pogłębiającej się wiedzy badania nad światem mikroorganizmów i cząsteczek wchodzących w skład ludzkiego ustroju nabrały tempa. Zaczynamy coraz lepiej rozumieć mikrokosmos współżyjących z nami symbiontów i komensali. Największym ich siedliskiem w organizmie człowieka są jelita, zawierające nawet do 2 kg flory jelitowej. Oddziaływania przestrzenne i molekularne mikroorganizmów jelitowych widoczne są nie tylko w ich wzajemnej komunikacji i rywalizacji o przetrwanie, ale dotyczą również antygenów, związków immunologicznie czynnych, hormonów czy neurotransmiterów wchodzących w ścisłe zależności z gospodarzem. Mikrobiom jelitowy odgrywa kluczową rolę w rozwoju układu odpornościowego, a w świetle obecnych badań – także układu nerwowego. Na styku obu układów powstają choroby autoimmunizacyjne ośrodkowego układu nerwowego, w tym stwardnienie rozsiane. Mimo licznych opracowań na temat patogenezy tej choroby w dalszym ciągu jej podłoże i bezpośrednia przyczyna rozwoju nie są do końca znane. Najnowsze badania z zastosowaniem zaawansowanych metod genetycznych i molekularnych wskazują, że wpływ na powstawanie choroby może mieć mikrobiom jelitowy, zarówno ze względu na jego niezmienioną w toku ewolucji strukturę i skład, jak i wzajemną komunikację z gospodarzem. W niniejszym opracowaniu omówiono rolę mikrobiomu jelitowego w utrzymaniu homeostazy immunologicznej ustroju, interakcje mikrobiomu z układem odpornościowym, nerwowym i dokrewnym, a także wskazano na potencjalne źródła autoimmunizacji oraz ich udział w patogenezie stwardnienia rozsianego, co może znaleźć przełożenie na działania terapeutyczne.
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Bibliografia
1. Basak G.W.: W poszukiwaniu źródeł – rola flory jelitowej w zdrowiu i chorobie. Część I. MS Report 2015; 3(14): 15-18.
2. Backhed F., Ley R.E., Sonnenburg J.L. et al.: Host-bacterial mutualism in the human intestine. Science 2005; 307: 1915-1920.
3. Wang Y., Kasper L.H.: The role of microbiome in central nervous system disorders. Brain Behav. Immun. 2014; 38: 1-12.
4. Joscelyn J., Kasper L.H.: Digesting the emerging role for the gut microbiome in central nervous system demyelination. Mult. Scler. 2014; 20(12): 1553-1559.
5. Strachan D.P.: Family size, infection and atopy: the first decade of the ‘hygiene hypothesis’. Thorax 2000; 55: S2-10.
6. Bhargava P., Mowry E.M.: Gut microbiome and multiple sclerosis. Curr. Neurol. Neurosci. Rep. 2014; 14: 492.
7. Mielcarz D.W., Kasper L.H.: The gut microbiome in multiple sclerosis. Curr. Treat. Options Neurol. 2015; 17(4): 344.
8. Compston A., Coles A.: Multiple sclerosis. Lancet 2008; 372: 1502-1517.
9. Ochoa-Repáraz J., Kasper L.H.: Gut microbiome and the risk factors in central nervous system autoimmunity. FEBS Lett. 2014; 588(22): 4214-4222.
10. Fazekas F., Enzinger C., Wallner-Blazek M. et al.: Gender differences in MRI studies on multiple sclerosis. J. Neurol. Sci. 2009; 286: 28-30.
11. Trojano M., Lucchese G., Graziano G. et al.: Geographical variations in sex ratio trends over time in multiple sclerosis. PLoS One 2012; 7: e48078.
12. Maranduba C.M., De Castro S.B., de Souza G.T. et al.: Intestinal Microbiota as Modulators of the Immune System and Neuroimmune System: Impact on the Host Health and Homeostasis. J. Immunol. Res. 2015; 2015: 931574.
13. Maynard C.L., Elson C.O., Hatton R.D. et al.: Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489(7415): 231-224.
14. Goto Y., Ivanov I.I.: Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol. Cell Biol. 2013; 91(3): 204-214.
15. Collins S.M., Surette M., Bercik P.: The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012; 10(11): 735-742.
16. Hooper L.V., Littman D.R., Macpherson A.J.: Interactions between the microbiota and the immune system. Science 2012; 336: 1268-1273.
17. Kamada N., Seo S., Chen G. et al.: Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 2013; 13(5): 321-335.
18. Macpherson A.J., Harris N.L.: Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 2004; 4: 478-485.
19. Round J.L., Mazmanian S.K.: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. of Sci. USA. 2010; 107: 12204-12209.
20. Furusawa Y., Obata Y., Fukuda S. et al.: Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504(7480): 446-450.
21. Cryan J.F., Dinan T.G.: Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012; 13(10): 701-712.
22. Romijn J.A., Corssmit E.P., Havekes L.M. et al.: Gut-brain axis. Curr. Opin. Clin. Nutr. Metab. Care 2008; 11: 518-521.
23. Barrett E., Ross R.P., O’Toole P.W. et al.: γ-Aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 2012; 113: 411-417.
24. Rhee S.H., Pothoulakis C., Mayer E.A.: Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009; 6: 306-314.
25. Brun P., Giron M.C., Qesari M. et al.: Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 2013; 145(6): 1323-1333.
26. Barajon I., Serrao G., Arnaboldi F. et al.: Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 2009; 57: 1013-1023.
27. Keast J.R., Furness J.B., Costa M.: Somatostatin in human enteric nerves. Distribution and characterization. Cell Tissue Res. 1984; 237(2): 299-308.
28. Ekblad E., Winther C., Ekman R. et al.: Projections of peptide-containing neurons in rat small intestine. Neuroscience 1987; 20(1): 169-188.
29. Kunze W.A., Mao Y.K., Wang B. et al.: Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J. Cell Mol. Med. 2009; 13(8 B): 2261-2270.
30. Rousseaux C., Thuru X., Gelot A. et al.: Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 2007; 13(1): 35-37.
31. Sudo N., Chida Y., Aiba Y. et al.: Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 2004; 558(1): 263-275.
32. Sudo N.: Role of microbiome in regulating the HPA axis and its relevance to allergy. Chem. Immunol. Allergy. 2012; 98: 163-175.
33. Velickovic K., Markelic M., Golic I. et al.: Long-term dietary L-arginine supplementation increases endothelial nitric oxide synthase and vasoactive intestinal peptide immunoexpression in rat small intestine. Eur. J. Nutr. 2014; 53(3): 813-821.
34. Gonzalez-Rey E., Fernandez-Martin A., Chorny A. et al.: Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am. J. Pathol. 2006; 168: 1179-1188.
35. Gonzalez D.A., Diaz B.B., Rodriguez Perez Mdel C. et al.: Sex hormones and autoimmunity. Immunol. Lett. 2010; 133(1): 6-13.
36. Klein S.L., Jedlicka A., Pekosz A.: The Xs and Y of immune responses to viral vaccines. Lancet Infect. Dis. 2010; 10: 338-349.
37. Chervonsky A.V.: Influence of microbial environment on autoimmunity. Nat. Immunol. 2010; 11: 28-35.
38. Gomez A., Luckey D., Taneja V.: The gut microbiome in autoimmunity: Sex matters. Clin. Immunol. 2015; 159(2): 154-162.
39. Ridlon J.M., Ikegawa S., Alves J.M. et al.: Clostridium scindens: a human gut microbe with a high potential to convert glucocorticoids into androgens. J. Lipid Res. 2013; 54: 2437-2449.
40. Yurkovetskiy L., Burrows M., Khan A.A. et al.: Gender bias in autoimmunity is influenced by microbiota. Immunity 2013; 39: 400-412.
41. Markle J.G., Frank D.N., Mortin-Toth S. et al.: Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013; 339: 1084-1088.
42. Mangalam A.K., Taneja V., David C.S.: HLA class II molecules influence susceptibility versus protection in inflammatory diseases by determining the cytokine profile. J. Immunol. 2013; 190(2): 513-518.
43. Ochoa-Repáraz J., Riccardi C., Rynda A. et al.: Regulatory T cell vaccination without autoantigen protects against experimental autoimmune encephalomyelitis. J. Immunol. 2007; 178: 1791-1799.
44. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E. et al.: Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009; 183: 6041-6050.
45. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E. et al.: Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J. Immunol. 2010; 185: 4101-4108.
46. Ochoa-Repáraz J., Mielcarz D.W., Wang Y. et al.: A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 2010; 3: 487-495.
47. Ochoa-Repáraz J., Mielcarz D.W., Haque-Begum S. et al.: Induction of a regulatory B cell population in experimental allergic encephalomyelitis by alteration of the gut commensal microflora. Gut Microbes 2010; 1: 103-108.
48. Begum-Haque S., Christy M., Ochoa-Repáraz J. et al.: Augmentation of regulatory B cell activity in experimental allergic encephalomyelitis by glatiramer acetate. J. Neuroimmunol. 2011; 232: 136-144.
49. Yokote H., Miyake S., Croxford J.L. et al.: NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am. J. Pathol. 2008; 173: 1714-1723.
50. Lee Y.K., Menezes J.S., Umesaki Y. et al.: Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 2011; 108(supl.): 4615-4622.
51. Davis C.P., Savage D.C.: Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect. Immun. 1974; 10: 948-956.
52. Westall F.C.: Molecular mimicry revisited: gut bacteria and multiple sclerosis. J. Clin. Microbiol. 2006; 44: 2099-2104.
53. 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: e9009.
54. Takata K., Kinoshita M., Okuno 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.
55. Maassen C.B., Claassen E.: Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine 2008; 26: 2056-2057.
56. Kwon H.K., Kim G.C., Kim Y. et al.: 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.
57. Mowry E., Waubant E., Chehoud C. et al.: Gut bacterial populations in multiple sclerosis and in health. Neurology 2012; 78: P05.106.
58. Jhangi S., Roopali G., Bonnie G. et al.: Increased Archaea species and changes with therapy in gut microbiome of multiple sclerosis subjects. Neurology 2014; 82: S24.001.
59. Tremlett H., Douglas F., Susan L. et al.: Gut microbiome in early pediatric multiple sclerosis: a case-control study. Neurology 2015; 84: P4.027.
60. Rumah K.R., Linden J., Fischetti V.A. et al.: 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: e76359.
61. Saemann M.D., Bohmig G.A., Osterreicher C.H. et al.: Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000; 14: 2380-2382.
62. Miyake S., Kim S., Suda 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.
63. Atarashi K., Tanoue T., Shima T. et al.: Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337-341.
64. Atarashi K., Tanoue T., Oshima K. et al.: Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500: 232-236.
65. Galland L.: The gut microbiome and the brain. J. Med. Food 2014; 17(12): 1261-1272.
2. Backhed F., Ley R.E., Sonnenburg J.L. et al.: Host-bacterial mutualism in the human intestine. Science 2005; 307: 1915-1920.
3. Wang Y., Kasper L.H.: The role of microbiome in central nervous system disorders. Brain Behav. Immun. 2014; 38: 1-12.
4. Joscelyn J., Kasper L.H.: Digesting the emerging role for the gut microbiome in central nervous system demyelination. Mult. Scler. 2014; 20(12): 1553-1559.
5. Strachan D.P.: Family size, infection and atopy: the first decade of the ‘hygiene hypothesis’. Thorax 2000; 55: S2-10.
6. Bhargava P., Mowry E.M.: Gut microbiome and multiple sclerosis. Curr. Neurol. Neurosci. Rep. 2014; 14: 492.
7. Mielcarz D.W., Kasper L.H.: The gut microbiome in multiple sclerosis. Curr. Treat. Options Neurol. 2015; 17(4): 344.
8. Compston A., Coles A.: Multiple sclerosis. Lancet 2008; 372: 1502-1517.
9. Ochoa-Repáraz J., Kasper L.H.: Gut microbiome and the risk factors in central nervous system autoimmunity. FEBS Lett. 2014; 588(22): 4214-4222.
10. Fazekas F., Enzinger C., Wallner-Blazek M. et al.: Gender differences in MRI studies on multiple sclerosis. J. Neurol. Sci. 2009; 286: 28-30.
11. Trojano M., Lucchese G., Graziano G. et al.: Geographical variations in sex ratio trends over time in multiple sclerosis. PLoS One 2012; 7: e48078.
12. Maranduba C.M., De Castro S.B., de Souza G.T. et al.: Intestinal Microbiota as Modulators of the Immune System and Neuroimmune System: Impact on the Host Health and Homeostasis. J. Immunol. Res. 2015; 2015: 931574.
13. Maynard C.L., Elson C.O., Hatton R.D. et al.: Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489(7415): 231-224.
14. Goto Y., Ivanov I.I.: Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol. Cell Biol. 2013; 91(3): 204-214.
15. Collins S.M., Surette M., Bercik P.: The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012; 10(11): 735-742.
16. Hooper L.V., Littman D.R., Macpherson A.J.: Interactions between the microbiota and the immune system. Science 2012; 336: 1268-1273.
17. Kamada N., Seo S., Chen G. et al.: Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 2013; 13(5): 321-335.
18. Macpherson A.J., Harris N.L.: Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 2004; 4: 478-485.
19. Round J.L., Mazmanian S.K.: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. of Sci. USA. 2010; 107: 12204-12209.
20. Furusawa Y., Obata Y., Fukuda S. et al.: Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504(7480): 446-450.
21. Cryan J.F., Dinan T.G.: Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012; 13(10): 701-712.
22. Romijn J.A., Corssmit E.P., Havekes L.M. et al.: Gut-brain axis. Curr. Opin. Clin. Nutr. Metab. Care 2008; 11: 518-521.
23. Barrett E., Ross R.P., O’Toole P.W. et al.: γ-Aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 2012; 113: 411-417.
24. Rhee S.H., Pothoulakis C., Mayer E.A.: Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009; 6: 306-314.
25. Brun P., Giron M.C., Qesari M. et al.: Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 2013; 145(6): 1323-1333.
26. Barajon I., Serrao G., Arnaboldi F. et al.: Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 2009; 57: 1013-1023.
27. Keast J.R., Furness J.B., Costa M.: Somatostatin in human enteric nerves. Distribution and characterization. Cell Tissue Res. 1984; 237(2): 299-308.
28. Ekblad E., Winther C., Ekman R. et al.: Projections of peptide-containing neurons in rat small intestine. Neuroscience 1987; 20(1): 169-188.
29. Kunze W.A., Mao Y.K., Wang B. et al.: Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J. Cell Mol. Med. 2009; 13(8 B): 2261-2270.
30. Rousseaux C., Thuru X., Gelot A. et al.: Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 2007; 13(1): 35-37.
31. Sudo N., Chida Y., Aiba Y. et al.: Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 2004; 558(1): 263-275.
32. Sudo N.: Role of microbiome in regulating the HPA axis and its relevance to allergy. Chem. Immunol. Allergy. 2012; 98: 163-175.
33. Velickovic K., Markelic M., Golic I. et al.: Long-term dietary L-arginine supplementation increases endothelial nitric oxide synthase and vasoactive intestinal peptide immunoexpression in rat small intestine. Eur. J. Nutr. 2014; 53(3): 813-821.
34. Gonzalez-Rey E., Fernandez-Martin A., Chorny A. et al.: Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am. J. Pathol. 2006; 168: 1179-1188.
35. Gonzalez D.A., Diaz B.B., Rodriguez Perez Mdel C. et al.: Sex hormones and autoimmunity. Immunol. Lett. 2010; 133(1): 6-13.
36. Klein S.L., Jedlicka A., Pekosz A.: The Xs and Y of immune responses to viral vaccines. Lancet Infect. Dis. 2010; 10: 338-349.
37. Chervonsky A.V.: Influence of microbial environment on autoimmunity. Nat. Immunol. 2010; 11: 28-35.
38. Gomez A., Luckey D., Taneja V.: The gut microbiome in autoimmunity: Sex matters. Clin. Immunol. 2015; 159(2): 154-162.
39. Ridlon J.M., Ikegawa S., Alves J.M. et al.: Clostridium scindens: a human gut microbe with a high potential to convert glucocorticoids into androgens. J. Lipid Res. 2013; 54: 2437-2449.
40. Yurkovetskiy L., Burrows M., Khan A.A. et al.: Gender bias in autoimmunity is influenced by microbiota. Immunity 2013; 39: 400-412.
41. Markle J.G., Frank D.N., Mortin-Toth S. et al.: Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013; 339: 1084-1088.
42. Mangalam A.K., Taneja V., David C.S.: HLA class II molecules influence susceptibility versus protection in inflammatory diseases by determining the cytokine profile. J. Immunol. 2013; 190(2): 513-518.
43. Ochoa-Repáraz J., Riccardi C., Rynda A. et al.: Regulatory T cell vaccination without autoantigen protects against experimental autoimmune encephalomyelitis. J. Immunol. 2007; 178: 1791-1799.
44. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E. et al.: Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009; 183: 6041-6050.
45. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E. et al.: Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J. Immunol. 2010; 185: 4101-4108.
46. Ochoa-Repáraz J., Mielcarz D.W., Wang Y. et al.: A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 2010; 3: 487-495.
47. Ochoa-Repáraz J., Mielcarz D.W., Haque-Begum S. et al.: Induction of a regulatory B cell population in experimental allergic encephalomyelitis by alteration of the gut commensal microflora. Gut Microbes 2010; 1: 103-108.
48. Begum-Haque S., Christy M., Ochoa-Repáraz J. et al.: Augmentation of regulatory B cell activity in experimental allergic encephalomyelitis by glatiramer acetate. J. Neuroimmunol. 2011; 232: 136-144.
49. Yokote H., Miyake S., Croxford J.L. et al.: NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am. J. Pathol. 2008; 173: 1714-1723.
50. Lee Y.K., Menezes J.S., Umesaki Y. et al.: Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 2011; 108(supl.): 4615-4622.
51. Davis C.P., Savage D.C.: Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect. Immun. 1974; 10: 948-956.
52. Westall F.C.: Molecular mimicry revisited: gut bacteria and multiple sclerosis. J. Clin. Microbiol. 2006; 44: 2099-2104.
53. 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: e9009.
54. Takata K., Kinoshita M., Okuno 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.
55. Maassen C.B., Claassen E.: Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine 2008; 26: 2056-2057.
56. Kwon H.K., Kim G.C., Kim Y. et al.: 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.
57. Mowry E., Waubant E., Chehoud C. et al.: Gut bacterial populations in multiple sclerosis and in health. Neurology 2012; 78: P05.106.
58. Jhangi S., Roopali G., Bonnie G. et al.: Increased Archaea species and changes with therapy in gut microbiome of multiple sclerosis subjects. Neurology 2014; 82: S24.001.
59. Tremlett H., Douglas F., Susan L. et al.: Gut microbiome in early pediatric multiple sclerosis: a case-control study. Neurology 2015; 84: P4.027.
60. Rumah K.R., Linden J., Fischetti V.A. et al.: 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: e76359.
61. Saemann M.D., Bohmig G.A., Osterreicher C.H. et al.: Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000; 14: 2380-2382.
62. Miyake S., Kim S., Suda 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.
63. Atarashi K., Tanoue T., Shima T. et al.: Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337-341.
64. Atarashi K., Tanoue T., Oshima K. et al.: Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500: 232-236.
65. Galland L.: The gut microbiome and the brain. J. Med. Food 2014; 17(12): 1261-1272.