Gut-associated lymphoid tissue, gut microbes and susceptibility to experimental autoimmune encephalomyelitis

Beneficial Microbes

Volumn 7, Issue 3, 2016, Pages 363-373

  Stanisavljevic S ^a   Lukic J ^a   Momcilovic M ^a   Miljkovic M ^a   Jevtic B ^a   Kojic M ^a   Golic N ^a   Mostarica Stojkovic M ^b   Miljkovic D ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Animal models; Cytokine; DGGE; Faeces; Gut associated lymphoid tissues; Immune system

Indexed keywords

FREUND ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 17; TRANSCRIPTION FACTOR FOXP3; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPOSTIPES; BACTERIAL STRAIN; BACTERIUM; BACTERIUM EXAMINATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RESPONSE; DARK AGOUTI RAT; DISEASE PREDISPOSITION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; LACTOBACILLUS; LACTOBACILLUS MURINUS; MALE; MESENTERY LYMPH NODE; MULTIPLE SCLEROSIS; NONHUMAN; PEYER PATCH; PHENOTYPE; RAT; REGULATORY T LYMPHOCYTE; TURICIBACTER; ANIMAL; CLASSIFICATION; COMPARATIVE STUDY; DISEASE MODEL; FECES; FIRMICUTES; GASTROINTESTINAL TRACT; IMMUNOLOGY; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; LYMPH NODE; MICROBIOLOGY; SECRETION (PROCESS);

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FECES; FIRMICUTES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; INTESTINAL MUCOSA; LYMPH NODES; PEYER'S PATCHES; RATS; T-LYMPHOCYTES, REGULATORY;

EID: 84971646866     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2015.0159     Document Type: Article

References (50)

1. Bartholomäus, I., Kawakami, N., Odoardi, F., Schläger, C., Miljkovic, D., Ellwart, J.W., Klinkert, W.E., Flügel-Koch, C., Issekutz, T.B., Wekerle, H. and Flügel, A., 2009. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462: 94-98.
2. Benson, A.K., Kelly, S.A., Legge, R., Ma, F., Low, S.J., Kim, J., Zhang, M., Oh, P.L., Nehrenberg, D., Hua, K., Kachman, S.D., Moriyama, E.N., Walter, J., Peterson, D.A. and Pomp, D., 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Science of the USA 107: 18933-18938.
3. Berer, K., Boziki, M. and Krishnamoorthy, G., 2014. Selective accumulation of pro-inflammatory T cells in the intestine contributes to the resistance to autoimmune demyelinating disease. PLoS One 9: e87876.
4. Berer, K., Mues, M., Koutrolos, M., Rasbi, Z.A., Boziki, M., Johner, C., Wekerle, H. and Krishnamoorthy, G., 2011. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479: 538-541.
5. Bhargava, P. and Mowry, E.M., 2014. Gut microbiome and multiple sclerosis. Current Neurology and Neuroscience Report 14: 492.
6. Bienenstock, J., Kunze, W. and Forsythe, P., 2015. Microbiota and the gut-brain axis. Nutrition Reviews 73: 28-31.
7. Bosshard, P.P., Zbinden, R. and Altwegg, M., 2002. Turicibacter sanguinis gen. nov., sp. nov., a novel anaerobic, Gram-positive bacterium. International Journal of Systematic and Evolutionary Microbiology 52: 1263-1266.
8. Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A., Bakocevic, N., Ng, L.G., Kundu, P., Gulyás, B., Halldin, C., Hultenby, K., Nilsson, H., Hebert, H., Volpe, B.T., Diamond, B. and Pettersson, S., 2014. The gut microbiota influences blood-brain barrier permeability in mice. Science Translational Medicine 6: 263ra158.
9. Califano, D., Sweeney, K.J., Le, H., VanValkenburgh, J., Yager, E., O'Connor Jr, W., Kennedy, J.S., Jones, D.M. and Avram, D., 2014. Diverting T helper cell trafficking through increased plasticity attenuates autoimmune encephalomyelitis. Journal of Clinical Investigation 124: 174-187.
10. Cording, S., Fleissner, D., Heimesaat, M.M., Bereswill, S., Loddenkemper, C., Uematsu, S., Akira, S., Hamann, A. and Huehn, J., 2013. Commensal microbiota drive proliferation of conventional and Foxp3(+) regulatory CD4(+) T cells in mesenteric lymph nodes and Peyer's patches. European Journal of Microbiology and Immunology 3: 1-10.
11. Cotta, M.A., Whitehead, T.R., Collins, M.D. and Lawson, P.A., 2004. Atopostipes suicloacale gen. nov., sp. nov., isolated from an underground swine manure storage pit. Anaerobe 10: 191-195.
12. Dendrou, C.A., Fugger, L. and Friese, M.A., 2015. Immunopathology of multiple sclerosis. Nature Reviews Immunology 15: 545-558.
13. Erny, D., Hrabě de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermöhlen, O., Chun, E., Garrett, W.S., McCoy, K.D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I. and Prinz, M., 2015. Host microbiota constantly control maturation and function of microglia in the CNS. Nature Neuroscience 18: 965-977.
14. Esplugues, E., Huber, S., Gagliani, N., Hauser, A.E., Town, T., Wan, Y.Y., O'Connor Jr., W., Rongvaux, A., Van Rooijen, N., Haberman, A.M., Iwakura, Y., Kuchroo, V.K., Kolls, J.K., Bluestone, J.A., Herold, K.C. and Flavell, R.A., 2011. Control of TH17 cells occurs in the small intestine. Nature 475: 514-518.
15. Falk, A., Olsson, C., Ahrné, S., Molin, G., Adawi, D. and Jeppsson, B., 2007. Ileal pelvic pouch microbiota from two former ulcerative colitis patients, analysed by DNA-based methods, were unstable over time and showed the presence of Clostridium perfringens. Scandinavian Journal of Gastroenterology 42: 973-985.
16. Furusawa, Y., Obata, Y., Fukuda, S., Endo, T.A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., Takahashi, M., Fukuda, N.N., Murakami, S., Miyauchi, E., Hino, S., Atarashi, K., Onawa, S., Fujimura, Y., Lockett, T., Clarke, J.M., Topping, D.L., Tomita, M., Hori, S., Ohara, O., Morita, T., Koseki, H., Kikuchi, J., Honda, K., Hase, K. and Ohno, H., 2013. Commensal microbederived butyrate induces the differentiation of colonic regulatory T cells. Nature 504: 446-450.
17. Galley, J.D., Yu, Z., Kumar, P., Dowd, S.E., Lyte, M. and Bailey, M.T., 2014. The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes 5: 748-760.
18. Hanahan, D., 1983. Studies on transformation of Escherichia coli with plasmids. Journal of Molecular Biology 166: 557-580.
19. Heilig, H.G.H.J., Zoetendal, E.G., Vaughan, E.E., Marteau, P., Akkermans, A.D.L. and De Vos, W.D.L., 2002. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine by specific amplification of 16S ribosomal DNA. Applied Environmental Microbiology 68: 114-123.
20. Jounai, K., Ikado, K., Sugimura, T., Ano, Y., Braun, J. and Fujiwara, D., 2012. Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS One 7: e32588.
21. Kebir, H., Kreymborg, K., Ifergan, I., Dodelet-Devillers, A., Cayrol, R., Bernard, M., Giuliani, F., Arbour, N., Becher, B. and Prat, A., 2007. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nature Medicine 13: 1173-1175.
22. Kovačević-Jovanović, V., Miletić, T., Stanojević, S., Mitić, K. and Dimitrijević, M., 2013. Strain differences in the humoral immune response to commensal bacterial antigens in rats. Acta Microbiologica et Immunologica Hungarica Journal 60: 271-288.
23. Kurschus, F.C., 2015. T cell mediated pathogenesis in EAE: molecular mechanisms. Biomedical Journal 38: 183-193.
24. Lee, Y.K. and Mazmanian, S.K., 2010. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330: 1768-1773.
25. Lee, Y.K., Menezes, J.S., Umesaki, Y. and Mazmanian, S.K., 2011. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proceedings of the National Academy of Sciences of the USA 108: 4615-4622.
26. Licht, T.R., Madsen, B. and Wilcks, A., 2007. Selection of bacteria originating from a human intestinal microbiota in the gut of previously germ-free rats. FEMS Microbiology Letters 277: 205-209.
27. Liu, J., Xu, T., Zhu, W. and Mao, S., 2014. High-grain feeding alters caecal bacterial microbiota composition and fermentation and results in caecal mucosal injury in goats. British Journal of Nutrition 112: 416-427.
28. Lukic, J., Strahinic, I., Milenkovic, M., Golic, N., Kojic, M., Topisirovic, L. and Begovic, J., 2013. Interaction of Lactobacillus fermentum BGHI14 with rat colonic mucosa: implications for colitis induction. Applied Environmental Microbiology 79: 5735-5744.
29. Maslowski, K.M., Vieira, A.T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H.C., Rolph, M.S., Mackay, F., Artis, D., Xavier, R.J., Teixeira, M.M. and Mackay, C.R., 2009. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-1286.
30. Maynard, C.L., Elson, C.O., Hatton, R.D. and Weaver, C.T., 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489: 231-241.
31. Mielcarz, D.W. and Kasper, L.H., 2015. The gut microbiome in multiple sclerosis. Current Treatment Options in Neurology 17: 344.
32. Miljković, D., Stanojević, Z., Momcilović, M., Odoardi, F., Flügel, A. and Mostarica-Stojković, M., 2011. CXCL12 expression within the CNS contributes to the resistance against experimental autoimmune encephalomyelitis in Albino Oxford rats. Immunobiology 216: 979-987.
33. Miljkovic, D., Stosic-Grujicic, S., Markovic, M., Momcilovic, M., Ramic, Z., Maksimovic-Ivanic, D., Mijatovic, S., Popadic, D., Cvetkovic, I. and Mostarica-Stojkovic, M., 2006. Strain difference in susceptibility to experimental autoimmune encephalomyelitis between Albino Oxford and Dark Agouti rats correlates with disparity in production of IL-17, but not nitric oxide. Journal of Neuroscience Research 84: 379-388.
34. Ochoa-Repáraz, J., Mielcarz, D.W., Ditrio, L.E., Burroughs, A.R., Foureau, D.M., Haque-Begum, S. and Kasper, L.H., 2009. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. Journal of Immunology 183: 6041-6050.
35. Petermann, F. and Korn, T., 2011. Cytokines and effector T cell subsets causing autoimmune CNS disease. FEBS Letters 585: 3747-3757.
36. Presley, L.L., Wei, B., Braun, J. and Borneman, J., 2010. Bacteria associated with immunoregulatory cells in mice. Applied Environmental Microbiology 76: 936-941.
37. Santos, L.M., Al-Sabbagh, A., Londono, A. and Weiner, H.L., 1994. Oral tolerance to myelin basic protein induces regulatory TGF-betasecreting T cells in Peyer's patches of SJL mice. Cellular Immunology 157: 439-447.
38. Sheridan, B.S. and Lefrançois, L., 2012. Isolation of mouse lymphocytes from small intestine tissues. Current Protocols in Immunology 3: 19.
39. Song, F., Wardrop, R.M., Gienapp, I.E., Stuckman, S.S., Meyer, A.L., Shawler, T. and Whitacre, C.C., 2008. The Peyer's patch is a critical immunoregulatory site for mucosal tolerance in experimental autoimmune encephalomylelitis (EAE). Journal of Autoimmunology 30: 230-237.
40. Sosa, R.A. and Forsthuber, T.G., 2011. The critical role of antigenpresentation- induced cytokine crosstalk in the central nervous system in multiple sclerosis and experimental autoimmune encephalomyelitis. Journal of Interferon and Cytokine Research 31: 753-768.
41. Stosic-Grujicic, S., Ramic, Z., Bumbasirevic, V., Harhaji, L. and Mostarica-Stojkovic, M., 2004. Induction of experimental autoimmune encephalomyelitis in Dark Agouti rats without adjuvant. Clinical and Experimental Immunology 136: 49-55.
42. Suchodolski, J.S., Markel, M.E., Garcia-Mazcorro, J.F., Unterer, S., Heilmann, R.M., Dowd, S.E., Kachroo, P., Ivanov, I., Minamoto, Y., Dillman, E.M., Steiner, J.M., Cook, A.K. and Toresson, L., 2012. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One 7: e51907.
43. Uzelac, G., Miljkovic, M., Lozo, J., Radulovic, Z., Tosic, N. and Kojic, M., 2015. Expression of bacteriocin LsbB is dependent on a transcription terminator. Microbiology Research 179: 45-53.
44. Van den Abbeele, P., De Wiele, T., Verstraete, W. and Possemiers, S., 2011. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiology Reviews 35: 691-704.
45. Vartanian, T., Li, Y., Zhao, M. and Stefansson, K., 1995. Interferongamma- induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Molecular Medicine 1: 732-743.
46. Vukmanović, S., Mostarica-Stojković, M., Zalud, I., Ramić, Z. and Lukić, M.L., 1990. Analysis of T cell subsets after induction of experimental autoimmune encephalomyelitis in susceptible and resistant strains of rats. Journal of Neuroimmunology 27: 63-69.
47. Wang, Y., Begum-Haque, S., Telesford, K.M., Ochoa-Repáraz, J., Christy, M., Kasper, E.J., Kasper, D.L., Robson, S.C. and Kasper, L.H., 2014. A commensal bacterial product elicits and modulates migratory capacity of CD39(+) CD4 T regulatory subsets in the suppression of neuroinflammation. Gut Microbes 5: 552-561.
48. Werner, T., Wagner, S.J., Martínez, I., Walter, J., Chang, J.S., Clavel, T., Kisling, S., Schuemann, K. and Haller, D., 2011. Depletion of luminal iron alters the gut microbiota and prevents Crohn's disease-like ileitis. Gut 60: 325-333.
49. Yokote, H., Miyake, S., Croxford, J.L., Oki, S., Mizusawa, H. and Yamamura, T., 2008. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. American Journal of Pathology 173: 1714-1723.
50. Zhong, Y., Nyman, M. and Fåk, F., 2015. Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barley malt. Molecular and Nutrition Food Research 59: 2066-2076.