Inhibition of type 1 diabetes correlated to a Lactobacillus johnsonii N6.2-mediated Th17 bias

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3538-3546

  Lau, Kenneth ^a   Benitez, Patrick ^a   Ardissone, Alexandria ^a   Wilson, Tenisha D ^a   Collins, Erin L ^a   Lorca, Graciela ^a   Li, Nan ^b   Sankar, Dhyana ^b   Wasserfall, Clive ^b   Neu, Josef ^b   Atkinson, Mark A ^b   Shatz, Desmond ^b   Triplett, Eric W ^a   Larkin III, Joseph ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AXILLARY LYMPH NODE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE RESISTANCE; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE; LACTOBACILLUS JOHNSONII; LACTOBACILLUS REUTERI; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; TH17 CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; GASTROINTESTINAL TRACT; INTERLEUKIN-17; LACTOBACILLUS; LACTOBACILLUS REUTERI; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; RATS; RATS, INBRED BB; TH17 CELLS;

EID: 79953193748     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001864     Document Type: Article

References (59)

1. Zipris, D. 2009. Epidemiology of type 1 diabetes and what animal models teach us about the role of viruses in disease mechanisms. Clin. Immunol. 131: 11-23.
2. Metcalfe, K. A., G. A. Hitman, R. E. Rowe, M. Hawa, X. Huang, T. Stewart, and R. D. Leslie. 2001. Concordance for type 1 diabetes in identical twins is affected by insulin genotype. Diabetes Care 24: 838-842.
3. Redondo, M. J., L. Yu, M. Hawa, T. Mackenzie, D. A. Pyke, G. S. Eisenbarth, and R. D. Leslie. 2001. Heterogeneity of type I diabetes: analysis of monozygotic twins in Great Britain and the United States. Diabetologia 44: 354-362.
4. Hyttinen, V., J. Kaprio, L. Kinnunen, M. Koskenvuo, and J. Tuomilehto. 2003. Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: a nationwide follow-up study. Diabetes 52: 1052-1055. (Pubitemid 36384278)
5. Vaarala, O., M. A. Atkinson, and J. Neu. 2008. The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 57: 2555-2562.
6. Wen, L., R. E. Ley, P. Y. Volchkov, P. B. Stranges, L. Avanesyan, A. C. Stonebraker, C. Hu, F. S. Wong, G. L. Szot, J. A. Bluestone, et al. 2008. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455: 1109-1113.
7. Macpherson, A. J., and T. Uhr. 2004. Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Ann. N. Y. Acad. Sci. 1029: 36-43.
8. Umesaki, Y., and H. Setoyama. 2000. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect. 2: 1343-1351.
9. Ozdemir, O. 2010. Various effects of different probiotic strains in allergic disorders: an update from laboratory and clinical data. Clin. Exp. Immunol. 160: 295-304.
10. Tang, M. L., S. J. Lahtinen, and R. J. Boyle. 2010. Probiotics and prebiotics: clinical effects in allergic disease. Curr. Opin. Pediatr. 22: 626-634.
11. Bischoff, S. C., and M. Zeitz. 2010. Scientific evidence for the medical use of probiotics. Ann. Nutr. Metab. 57: 1-5.
12. Huynh, H. Q., J. deBruyn, L. Guan, H. Diaz, M. Li, S. Girgis, J. Turner, R. Fedorak, and K. Madsen. 2009. Probiotic preparation VSL#3 induces remission in children with mild to moderate acute ulcerative colitis: a pilot study. Inflamm. Bowel Dis. 15: 760-768.
13. Bibiloni, R., R. N. Fedorak, G. W. Tannock, K. L. Madsen, P. Gionchetti, M. Campieri, C. De Simone, and R. B. Sartor. 2005. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 100: 1539-1546.
14. Calderon, B., A. Suri, X. O. Pan, J. C. Mills, and E. R. Unanue. 2008. IFN-gamma-dependent regulatory circuits in immune inflammation highlighted in diabetes. J. Immunol. 181: 6964-6974.
15. Christianson, S. W., L. D. Shultz, and E. H. Leiter. 1993. Adoptive transfer of diabetes into immunodeficient NOD-scid/scid mice: relative contributions of CD4+ and CD8+ T-cells from diabetic versus prediabetic NOD.NON-Thy-1a donors. Diabetes 42: 44-55.
16. Kanagawa, O., G. Xu, A. Tevaarwerk, and B. A. Vaupel. 2000. Protection of nonobese diabetic mice from diabetes by gene(s) closely linked to IFN-gamma receptor loci. J. Immunol. 164: 3919-3923.
17. Wang, B., I. André, A. Gonzalez, J. D. Katz, M. Aguet, C. Benoist, and D. Mathis. 1997. Interferon-gamma impacts at multiple points during the progression of autoimmune diabetes. Proc. Natl. Acad. Sci. USA 94: 13844-13849.
18. Debray-Sachs, M., C. Carnaud, C. Boitard, H. Cohen, I. Gresser, P. Bedossa, and J. F. Bach. 1991. Prevention of diabetes in NOD mice treated with antibody to murine IFN gamma. J. Autoimmun. 4: 237-248.
19. Jaeckel, E., N. Mpofu, N. Saal, and M. P. Manns. 2008. Role of regulatory T cells for the treatment of type 1 diabetes mellitus. Horm. Metab. Res. 40: 126-136.
20. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527.
21. Happel, K. I., P. J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L. J. Quinton, A. R. Odden, J. E. Shellito, G. J. Bagby, S. Nelson, and J. K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202: 761-769.
22. Higgins, S. C., A. G. Jarnicki, E. C. Lavelle, and K. H. Mills. 2006. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177: 7980-7989.
23. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
24. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748. (Pubitemid 36227625)
25. Tzartos, J. S., M. A. Friese, M. J. Craner, J. Palace, J. Newcombe, M. M. Esiri, and L. Fugger. 2008. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 172: 146-155.
26. Rovedatti, L., T. Kudo, P. Biancheri, M. Sarra, C. H. Knowles, D. S. Rampton, G. R. Corazza, G. Monteleone, A. Di Sabatino, and T. T. Macdonald. 2009. Differential regulation of interleukin 17 and interferon gamma production in inflammatory bowel disease. Gut 58: 1629-1636.
27. Emamaullee, J. A., J. Davis, S. Merani, C. Toso, J. F. Elliott, A. Thiesen, and A. M. Shapiro. 2009. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 58: 1302-1311.
28. Bradshaw, E. M., K. Raddassi, W. Elyaman, T. Orban, P. A. Gottlieb, S. C. Kent, and D. A. Hafler. 2009. Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J. Immunol. 183: 4432-4439.
29. O'Connor, W., Jr., M. Kamanaka, C. J. Booth, T. Town, S. Nakae, Y. Iwakura, J. K. Kolls, and R. A. Flavell. 2009. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10: 603-609.
30. Nikoopour, E., J. A. Schwartz, K. Huszarik, C. Sandrock, O. Krougly, E. Lee-Chan, and B. Singh. 2010. Th17 polarized cells from nonobese diabetic mice following mycobacterial adjuvant immunotherapy delay type 1 diabetes. J. Immunol. 184: 4779-4788.
31. Han, G., R. Wang, G. Chen, J. Wang, R. Xu, L. Wang, J. Feng, X. Li, R. Guo, L. Fu, et al. 2010. Interleukin-17-producing gammadelta(+) T cells protect NOD mice from type 1 diabetes through a mechanism involving transforming growth factor-beta. Immunology 129: 197-206.
32. Malaisse, W. J., P. Courtois, and F. W. Scott. 2004. Insulin-dependent diabetes and gut dysfunction: the BB rat model. Horm. Metab. Res. 36: 585-594.
33. Lam-Tse, W. K., A. Lernmark, and H. A. Drexhage. 2002. Animal models of endocrine/organ-specific autoimmune diseases: do they really help us to understand human autoimmunity? Springer Semin. Immunopathol. 24: 297-321. (Pubitemid 35447458)
34. Like, A. A., D. L. Guberski, and L. Butler. 1991. Influence of environmental viral agents on frequency and tempo of diabetes mellitus in BB/Wor rats. Diabetes 40: 259-262.
35. Roesch, L. F., G. L. Lorca, G. Casella, A. Giongo, A. Naranjo, A. M. Pionzio, N. Li, V. Mai, C. H. Wasserfall, D. Schatz, et al. 2009. Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. ISME J. 3: 536-548.
36. Valladares, R., D. Sankar, N. Li, E. Williams, K. K. Lai, A. S. Abdelgeliel, C. F. Gonzalez, C. H. Wasserfall, J. Larkin, D. Schatz, et al. 2010. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS One 5: e10507.
37. Guay, H. M., J. Larkin, III, C. C. Picca, L. Panarey, and A. J. Caton. 2007. Spontaneous autoreactive memory B cell formation driven by a high frequency of autoreactive CD4+ T cells. J. Immunol. 178: 4793-4802.
38. Larkin, J., III, C. C. Picca, and A. J. Caton. 2007. Activation of CD4+ CD25+ regulatory T cell suppressor function by analogs of the selecting peptide. Eur. J. Immunol. 37: 139-146.
39. Lerman, M. A., J. Larkin, III, C. Cozzo, M. S. Jordan, and A. J. Caton. 2004. CD4+ CD25+ regulatory T cell repertoire formation in response to varying expression of a neo-self-antigen. J. Immunol. 173: 236-244.
40. Motulsky, H. 2010. Intuitive Biostatistics, 2nd Ed. Oxford University Press, New York, p. 447.
41. Neu, J., C. M. Reverte, A. D. Mackey, K. Liboni, L. M. Tuhacek-Tenace, M. Hatch, N. Li, R. A. Caicedo, D. A. Schatz, and M. Atkinson. 2005. Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J. Pediatr. Gastroenterol. Nutr. 40: 589-595.
42. Meddings, J. B., J. Jarand, S. J. Urbanski, J. Hardin, and D. G. Gall. 1999. Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am. J. Physiol. 276: G951-G957.
43. Graham, S., P. Courtois, W. J. Malaisse, J. Rozing, F. W. Scott, and A. M. Mowat. 2004. Enteropathy precedes type 1 diabetes in the BB rat. Gut 53: 1437-1444.
44. Zhao, L., L. Sun, H. Wang, H. Ma, G. Liu, and Y. Zhao. 2007. Changes of CD4+CD25+Foxp3+ regulatory T cells in aged Balb/c mice. J. Leukoc. Biol. 81: 1386-1394.
45. Lages, C. S., I. Suffia, P. A. Velilla, B. Huang, G. Warshaw, D. A. Hildeman, Y. Belkaid, and C. Chougnet. 2008. Functional regulatory T cells accumulate in aged hosts and promote chronic infectious disease reactivation. J. Immunol. 181: 1835-1848.
46. Dong, C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8: 337-348.
47. Serada, S., M. Fujimoto, M. Mihara, N. Koike, Y. Ohsugi, S. Nomura, H. Yoshida, T. Nishikawa, F. Terabe, T. Ohkawara, et al. 2008. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 105: 9041-9046.
48. Fujimoto, M., S. Serada, M. Mihara, Y. Uchiyama, H. Yoshida, N. Koike, Y. Ohsugi, T. Nishikawa, B. Ripley, A. Kimura, et al. 2008. Interleukin-6 blockade suppresses autoimmune arthritis in mice by the inhibition of inflammatory Th17 responses. Arthritis Rheum. 58: 3710-3719.
49. Diehl, S., and M. Rincón. 2002. The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39: 531-536.
50. Sofi, M. H., W. Li, M. H. Kaplan, and C. H. Chang. 2009. Elevated IL-6 expression in CD4 T cells via PKCtheta and NF-kappaB induces Th2 cytokine production. Mol. Immunol. 46: 1443-1450.
51. Clark, E. A., and K. E. Draves. 1987. Activation of macaque T cells and B cells with agonistic monoclonal antibodies. Eur. J. Immunol. 17: 1799-1805.
52. Leser, T. D., and L. Mølbak. 2009. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 11: 2194-2206.
53. Lo, J., and M. J. Clare-Salzler. 2006. Dendritic cell subsets and type I diabetes: focus upon DC-based therapy. Autoimmun. Rev. 5: 419-423.
54. Ivanov, I. I., Rde. L. Frutos, N. Manel, K. Yoshinaga, D. B. Rifkin, R. B. Sartor, B. B. Finlay, and D. R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
55. Round, J. L., and S. K. Mazmanian. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9: 313-323.
56. Matsuzaki, T., Y. Nagata, S. Kado, K. Uchida, I. Kato, S. Hashimoto, and T. Yokokura. 1997. Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. APMIS 105: 643-649. (Pubitemid 27380828)
57. Bending, D., H. De La Pena, M. Veldhoen, J. M. Phillips, C. Uyttenhove, B. Stockinger, and A. Cooke. 2009. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 119: 565-572.
58. Martin-Orozco, N., Y. Chung, S. H. Chang, Y. H. Wang, and C. Dong. 2009. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur. J. Immunol. 39: 216-224.
59. Turley, S. J., J. W. Lee, N. Dutton-Swain, D. Mathis, and C. Benoist. 2005. Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc. Natl. Acad. Sci. USA 102: 17729-17733.