Table of Contents Author Guidelines Submit a Manuscript
International Journal of Microbiology
Volume 2010, Article ID 917075, 12 pages
http://dx.doi.org/10.1155/2010/917075
Review Article

The Modulation of Adaptive Immune Responses by Bacterial Zwitterionic Polysaccharides

1Department of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
2Institute for Medical Microbiology, Immunology, and Hygiene, Medical Centre, University of Cologne, Goldenfelsstraße 19-21, 50935 Cologne, Germany
3Department of Internal Medicine, Evangelisches Krankenhaus, Weyertal, 50931 Cologne, Germany
4MVZ Dr. Stein + Kollegen, Wallstraße 10, 41061 Moenchengladbach, Germany

Received 17 June 2010; Revised 15 September 2010; Accepted 5 October 2010

Academic Editor: Charlene Kahler

Copyright © 2010 Tom Li Stephen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Z. Pancer and M. D. Cooper, “The evolution of adaptive immunity,” Annual Review of Immunology, vol. 24, pp. 497–518, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. P. G. Gell and B. Benacerraf, “Studies on hypersensitivity. II. Delayed hypersensitivity to denatured proteins in guinea pigs,” Immunology, vol. 2, pp. 64–70, 1959. View at Google Scholar
  3. H. Li, A. Llera, E. L. Malchiodi, and R. A. Mariuzza, “The structural basis of T cell activation by superantigens,” Annual Review of Immunology, vol. 17, pp. 435–466, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. E. J. Sundberg, L. Deng, and R. A. Mariuzza, “TCR recognition of peptide/MHC class II complexes and superantigens,” Seminars in Immunology, vol. 19, no. 4, pp. 262–271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. E. S. Trombetta and I. Mellman, “Cell biology of antigen processing in vitro and in vivo,” Annual Review of Immunology, vol. 23, pp. 975–1028, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Watts, “The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules,” Nature Immunology, vol. 5, no. 7, pp. 685–692, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. P. E. Jensen, “Recent advances in antigen processing and presentation,” Nature Immunology, vol. 8, no. 10, pp. 1041–1048, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. K. M. Murphy, P. Travers, and M. Walport, Janeway's Immunobiology, Garland Science, 2007.
  9. J. M. Vyas, A. G. van der Veen, and H. L. Ploegh, “The known unknowns of antigen processing and presentation,” Nature Reviews Immunology, vol. 8, no. 8, pp. 607–618, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. E. R. Unanue, “Perspective on antigen processing and presentation,” Immunological Reviews, vol. 185, pp. 86–102, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. G. Rudolph, R. L. Stanfield, and I. A. Wilson, “How TCRs bind MHCs, peptides, and coreceptors,” Annual Review of Immunology, vol. 24, pp. 419–466, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Joyce and L. van Kaer, “CD1-restricted antigen presentation: an oily matter,” Current Opinion in Immunology, vol. 15, no. 1, pp. 95–104, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Brigl and M. B. Brenner, “CD1: antigen presentation and T cell function,” Annual Review of Immunology, vol. 22, pp. 817–890, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Bendelac, P. B. Savage, and L. Teyton, “The biology of NKT cells,” Annual Review of Immunology, vol. 25, pp. 297–336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Monzavi-Karbassi, G. Cunto-Amesty, P. Luo, and T. Kieber-Emmons, “Peptide mimotopes as surrogate antigens of carbohydrates in vaccine discovery,” Trends in Biotechnology, vol. 20, no. 5, pp. 207–214, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. A. K. Abbas, A. H. Lichtman, and J. S. Pober, Cellular and Molecular Immunolog, W.B. Saunders, New York, NY, USA, 2000.
  17. H. Baumann, A. O. Tzianabos, J.-R. Brisson, D. L. Kasper, and H. J. Jennings, “Structural elucidation of two capsular polysaccharides from one strain of Bacteroides fragilis using high-resolution NMR spectroscopy,” Biochemistry, vol. 31, no. 16, pp. 4081–4089, 1992. View at Publisher · View at Google Scholar · View at Scopus
  18. A. O. Tzianabos, A. Pantosti, H. Baumann, J.-R. Brisson, H. J. Jennings, and D. L. Kasper, “The capsular polysaccharide of Bacteroides fragilis comprises two ionically linked polysaccharides,” Journal of Biological Chemistry, vol. 267, no. 25, pp. 18230–18235, 1992. View at Google Scholar · View at Scopus
  19. A. Pantosti, A. O. Tzianabos, A. B. Onderdonk, and D. L. Kasper, “Immunochemical characterization of two surface polysaccharides of Bacteroides fragilis,” Infection and Immunity, vol. 59, no. 6, pp. 2075–2082, 1991. View at Google Scholar · View at Scopus
  20. A. O. Tzianabos, A. Pantosti, H. Baumann et al., “Structural characterization of two surface polysaccharides of Bacteroides fragilis,” Transactions of the Association of American Physicians, vol. 104, pp. 285–295, 1991. View at Google Scholar · View at Scopus
  21. M. J. Coyne, W. Kalka-Moll, A. O. Tzianabos, D. L. Kasper, and L. E. Comstock, “Bacteroides fragilis NCTC9343 produces at least three distinct capsular polysaccharides: cloning, characterization, and reassignment of polysaccharide B and C biosynthesis loci,” Infection and Immunity, vol. 68, no. 11, pp. 6176–6181, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. W. M. Kalka-Moll, Y. Wang, L. E. Comstock, S. E. Gonzalez, A. O. Tzianabos, and D. L. Kasper, “Immunochemical and biological characterization of three capsular polysaccharides from a single Bacteroides fragilis strain,” Infection and Immunity, vol. 69, no. 4, pp. 2339–2344, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. A. O. Tzianabos, J. Y. Wang, and J. C. Lee, “Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 16, pp. 9365–9370, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. W. M. Kalka-Moll, A. O. Tzianabos, P. W. Bryant, M. Niemeyer, H. L. Ploegh, and D. L. Kasper, “Zwitterionic polysaccharides stimulate T cells by MHC class II-dependent interactions,” Journal of Immunology, vol. 169, no. 11, pp. 6149–6153, 2002. View at Google Scholar · View at Scopus
  25. Y. Wang, W. M. Kalka-Moll, M. H. Roehrl, and D. L. Kasper, “Structural basis of the abscess-modulating polysaccharide A2 from Bacteroides fragilis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13478–13483, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. A. O. Tzianabos, A. B. Onderdonk, B. Rosner, R. L. Cisneros, and D. L. Kasper, “Structural features of polysaccharides that induce intra-abdominal abscesses,” Science, vol. 262, no. 5132, pp. 416–419, 1993. View at Google Scholar · View at Scopus
  27. A. O. Tzianabos, R. W. Finberg, Y. Wang et al., “T cells activated by zwitterionic molecules prevent abscesses induced by pathogenic bacteria,” Journal of Biological Chemistry, vol. 275, no. 10, pp. 6733–6740, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. S. K. Mazmanian, H. L. Cui, A. O. Tzianabos, and D. L. Kasper, “An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system,” Cell, vol. 122, no. 1, pp. 107–118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. A. O. Tzianabos, A. B. Onderdonk, R. S. Smith, and D. L. Kasper, “Structure-function relationships for polysaccharide-induced intra- abdominal abscesses,” Infection and Immunity, vol. 62, no. 8, pp. 3590–3593, 1994. View at Google Scholar · View at Scopus
  30. A. O. Tzianabos, A. B. Onderdonk, D. F. Zaleznik, R. S. Smith, and D. L. Kasper, “Structural characteristics of polysaccharides that induce protection against intra-abdominal abscess formation,” Infection and Immunity, vol. 62, no. 11, pp. 4881–4886, 1994. View at Google Scholar · View at Scopus
  31. A. B. Onderdonk, M. E. Shapiro, R. W. Finberg, D. F. Zaleznik, and D. L. Kasper, “Use of a model of intraabdominal sepsis for studies of the pathogenicity of Bacteroides fragilis,” Reviews of Infectious Diseases, vol. 6, pp. S91–S95, 1984. View at Google Scholar · View at Scopus
  32. M. E. Shapiro, D. L. Kasper, D. F. Zaleznik, S. Spriggs, A. B. Onderdonk, and R. W. Finberg, “Cellular control of abscess formation: role of T cells in the regulation of abscesses formed in response to Bacteroides fragilis,” Journal of Immunology, vol. 137, no. 1, pp. 341–346, 1986. View at Google Scholar
  33. D. R. Chung, D. L. Kasper, R. J. Panzo et al., “CD4+ T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism,” Journal of Immunology, vol. 170, no. 4, pp. 1958–1963, 2003. View at Google Scholar · View at Scopus
  34. A. O. Tzianabos, D. L. Kasper, R. L. Cisneros, R. S. Smith, and A. B. Onderdonk, “Polysaccharide-mediated protection against abscess formation in experimental intra-abdominal sepsis,” Journal of Clinical Investigation, vol. 96, no. 6, pp. 2727–2731, 1995. View at Google Scholar · View at Scopus
  35. M. J. Coyne, A. O. Tzianabos, B. C. Mallory, V. J. Carey, D. L. Kasper, and L. E. Comstock, “Polysaccharide biosynthesis locus required for virulence of Bacteroides fragilis,” Infection and Immunity, vol. 69, no. 7, pp. 4342–4350, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Gallorini, F. Berti, G. Mancuso et al., “Toll-like receptor 2 dependent immunogenicity of glycoconjugate vaccines containing chemically derived zwitterionic polysaccharides,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17481–17486, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Boes, J. Cerny, R. Massol et al., “T-cell engagement of dendritic cells rapidly rearranges MHC class II transport,” Nature, vol. 418, no. 6901, pp. 983–988, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Chow, D. Toomre, W. Garrett, and I. Mellman, “Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane,” Nature, vol. 418, no. 6901, pp. 988–994, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. T. L. Stephen, M. Fabri, L. Groneck et al., “Transport of Streptococcus pneumoniae capsular polysaccharide in MHC class II tubules,” PLoS Pathogens, vol. 3, no. 3, article e32, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. B. A. Cobb, Q. Wang, A. O. Tzianabos, and D. L. Kasper, “Polysaccharide processing and presentation by the MHCII pathway,” Cell, vol. 117, no. 5, pp. 677–687, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. T. L. Stephen, M. Niemeyer, A. O. Tzianabos, M. Kroenke, D. L. Kasper, and W. M. Kalka-Moll, “Effect of B7-2 and CD40 signals from activated antigen-presenting cells on the ability of zwitterionic polysaccharides to induce T-cell stimulation,” Infection and Immunity, vol. 73, no. 4, pp. 2184–2189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. C. J. Lewis and B. A. Cobb, “Carbohydrate oxidation acidifies endosomes, regulating antigen processing and TLR9 signaling,” Journal of Immunology, vol. 184, no. 7, pp. 3789–3800, 2010. View at Publisher · View at Google Scholar
  43. C. D. Velez, C. J. Lewis, D. L. Kasper, and B. A. Cobb, “Type i Streptococcus pneumoniae carbohydrate utilizes a nitric oxide and MHC II-dependent pathway for antigen presentation,” Immunology, vol. 127, no. 1, pp. 73–82, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Herman, J. W. Kappler, P. Marrack, and A. M. Pullen, “Superantigens: mechanism of T-cell stimulation and role in immune responses,” Annual Review of Immunology, vol. 9, pp. 745–772, 1991. View at Google Scholar · View at Scopus
  45. L. Groneck, D. Schrama, M. Fabri et al., “Oligoclonal CD4+ T cells promote host memory immune responses to zwitterionic polysaccharide of Streptococcus pneumoniae,” Infection and Immunity, vol. 77, no. 9, pp. 3705–3712, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Stingele, B. Corthésy, N. Kusy, S. A. Porcelli, D. L. Kasper, and A. O. Tzianabos, “Zwitterionic polysaccharides stimulate T cells with no preferential Vβ usage and promote anergy, resulting in protection against experimental abscess formation,” Journal of Immunology, vol. 172, no. 3, pp. 1483–1490, 2004. View at Google Scholar · View at Scopus
  47. Q. Wang, R. M. McLoughlin, B. A. Cobb et al., “A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2,” Journal of Experimental Medicine, vol. 203, no. 13, pp. 2853–2863, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. L. J. Stern, J. H. Brown, T. S. Jardetzky et al., “Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide,” Nature, vol. 368, no. 6468, pp. 215–221, 1994. View at Publisher · View at Google Scholar · View at Scopus
  49. Y. Zhu, A. Y. Rudensky, A. L. Corper, L. Teyton, and I. A. Wilson, “Crystal structure of MHC class II I-Ab in complex with a human CLIP peptide: prediction of an I-Ab peptide-binding motif,” Journal of Molecular Biology, vol. 326, no. 4, pp. 1157–1174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Wang, J. Sidney, C. Dow, B. Mothé, A. Sette, and B. Peters, “A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach,” PLoS Computational Biology, vol. 4, no. 4, Article ID e1000048, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. L. S. C. Kreisman, J. H. Friedman, A. Neaga, and B. A. Cobb, “Structure and function relations with a T-cell-activating polysaccharide antigen using circular dichroism,” Glycobiology, vol. 17, no. 1, pp. 46–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Meemboor, J. Mertens, E. Flenner et al., “Interleukin-6 is essential for zwitterionic polysaccharide-mediated abscess formation,” Innate Immunity, vol. 16, no. 5, pp. 310–321, 2010. View at Publisher · View at Google Scholar
  53. M. E. Cosulich, A. Rubartelli, A. Risso, F. Cozzolino, and A. Bargellesi, “Functional characterization of an antigen involved in an early step of T-cell activation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 12, pp. 4205–4209, 1987. View at Google Scholar · View at Scopus
  54. D. D'Ambrosio, D. A. Cantrell, L. Frat, A. Santoni, and R. Testi, “Involvement of p21(ras) activation in T cell CD69 expression,” European Journal of Immunology, vol. 24, no. 3, pp. 616–620, 1994. View at Google Scholar · View at Scopus
  55. E. H. Palacios and A. Weiss, “Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation,” Oncogene, vol. 23, no. 48, pp. 7990–8000, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. B. Ruiz-Perez, D. R. Chung, A. H. Sharpe et al., “Modulation of surgical fibrosis by microbial zwitterionic polysaccharides,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 46, pp. 16753–16758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Mertens, M. Fabri, A. Zingarelli et al., “Streptococcus pneumoniae serotype 1 capsular polysaccharide induces CD8+CD28- regulatory T lymphocytes by TCR crosslinking,” PLoS Pathogens, vol. 5, no. 9, Article ID e1000596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. S. K. Mazmanian, J. L. Round, and D. L. Kasper, “A microbial symbiosis factor prevents intestinal inflammatory disease,” Nature, vol. 453, no. 7195, pp. 620–625, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. J. L. Round and S. K. Mazmanian, “Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 27, pp. 12204–12209, 2010. View at Publisher · View at Google Scholar
  60. J. Ochoa-Repáraz, D. W. Mielcarz, Y. Wang et al., “A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease,” Mucosal Immunology, vol. 3, no. 5, pp. 487–495, 2010. View at Publisher · View at Google Scholar
  61. S. A. Joosten and T. H. M. Ottenhoff, “Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination,” Human Immunology, vol. 69, no. 11, pp. 760–770, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. Y.-G. Tsai, K. D. Yang, D.-M. Niu, J.-W. Chien, and C.-Y. Lin, “TLR2 agonists enhance CD8+Foxp3+ regulatory T cells and suppress Th2 immune responses during allergen immunotherapy,” Journal of Immunology, vol. 184, no. 12, pp. 7229–7237, 2010. View at Publisher · View at Google Scholar
  63. S. L. Gorbach and J. G. Bartlett, “Anaerobic infections (second of three parts),” New England Journal of Medicine, vol. 290, no. 22, pp. 1237–1245, 1974. View at Google Scholar · View at Scopus
  64. B. Frank Polk and D. L. Kasper, “Bacteroides fragilis subspecies in clinical isolates,” Annals of Internal Medicine, vol. 86, no. 5, pp. 569–571, 1977. View at Google Scholar · View at Scopus
  65. F. C. Gibson III, A. O. Tzianabos, and A. B. Onderdonk, “The capsular polysaccharide complex of Bacteroides fragilis induces cytokine production from human and murine phagocytic cells,” Infection and Immunity, vol. 64, no. 3, pp. 1065–1069, 1996. View at Google Scholar · View at Scopus
  66. F. C. Gibson III, A. B. Onderdonk, D. L. Kasper, and A. O. Tzianabos, “Cellular mechanism of intraabdominal abscess formation by Bacteroides fragilis,” Journal of Immunology, vol. 160, no. 10, pp. 5000–5006, 1998. View at Google Scholar · View at Scopus
  67. M. Lotz, F. Jirik, P. Kabouridis et al., “B cell stimulating factor 2/interleukin 6 is a costimulant for human thymocytes and T lymphocytes,” Journal of Experimental Medicine, vol. 167, no. 3, pp. 1253–1258, 1988. View at Google Scholar · View at Scopus
  68. J. van Snick, “Interleukin-6: an overview,” Annual Review of Immunology, vol. 8, pp. 253–278, 1990. View at Google Scholar · View at Scopus
  69. K. Takeda, T. Kaisho, N. Yoshida, J. Takeda, T. Kishimoto, and S. Akira, “Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell- specific stat3-deficient mice,” Journal of Immunology, vol. 161, no. 9, pp. 4652–4660, 1998. View at Google Scholar · View at Scopus
  70. T. K. Teague, P. Marrack, J. W. Kappler, and A. T. Vella, “IL-6 rescues resting mouse T cells from apoptosis,” Journal of Immunology, vol. 158, no. 12, pp. 5791–5796, 1997. View at Google Scholar · View at Scopus
  71. M. J. McGeachy and D. J. Cua, “Th17 cell differentiation: the long and winding road,” Immunity, vol. 28, no. 4, pp. 445–453, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Dominitzki, M. C. Fantini, C. Neufert et al., “Cutting edge: trans-signaling via the soluble IL-6R abrogates the induction of FoxP3 in naive CD4+CD25- T cells,” Journal of Immunology, vol. 179, no. 4, pp. 2041–2045, 2007. View at Google Scholar · View at Scopus
  73. A. O. Tzianabos, P. R. Russell, A. B. Onderdonk et al., “IL-2 mediates protection against abscess formation in an experimental model of sepsis,” Journal of Immunology, vol. 163, no. 2, pp. 893–897, 1999. View at Google Scholar · View at Scopus
  74. C. Asseman, S. Mauze, M. W. Leach, R. L. Coffman, and F. Powrie, “An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation,” Journal of Experimental Medicine, vol. 190, no. 7, pp. 995–1003, 1999. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Kuhn, J. Lohler, D. Rennick, K. Rajewsky, and W. Muller, “Interleukin-10-deficient mice develop chronic enterocolitis,” Cell, vol. 75, no. 2, pp. 263–274, 1993. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Saraiva and A. O'Garra, “The regulation of IL-10 production by immune cells,” Nature Reviews Immunology, vol. 10, no. 3, pp. 170–181, 2010. View at Publisher · View at Google Scholar
  77. S. W. van Gool, J. Vermeiren, K. Rafiq, K. Loiré, M. de Boer, and J. L. Ceuppens, “Blocking CD40-CD154 and CD80/CD86-CD28 interactions during primary allogeneic stimulation results in T cell anergy and high IL-10 production,” European Journal of Immunology, vol. 29, no. 8, pp. 2367–2375, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Kronfeld, H. Abken, and B. Seliger, “B7-1 and B7-2 act differentially in the induction of a T cell response: their impact for a HLA-matched and HLA-mismatched anti-tumor immunotherapy,” International Journal of Cancer, vol. 117, no. 5, pp. 794–799, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. I. Brook, “Microbiology and management of abdominal infections,” Digestive Diseases and Sciences, vol. 53, no. 10, pp. 2585–2591, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. C. C. A. Bernard, J. Leydon, and I. R. Mackay, “T cell necessity in the pathogenesis of experimental autoimmune encephalomyelitis in mice,” European Journal of Immunology, vol. 6, no. 9, pp. 655–660, 1976. View at Google Scholar · View at Scopus
  81. M. K. Kennedy, D. S. Torrance, K. S. Picha, and K. M. Mohler, “Analysis of cytokine mRNA expression in the central nervous system of mice with experimental autoimmune encephalomyelitis reveals that IL-10 mRNA expression correlates with recovery,” Journal of Immunology, vol. 149, no. 7, pp. 2496–2505, 1992. View at Google Scholar · View at Scopus
  82. K. E. Balashov, M. Comabella, T. Ohashi, S. J. Khoury, and H. L. Weiner, “Defective regulation of IFNγ and IL-12 by endogenous IL-10 in progressive MS,” Neurology, vol. 55, no. 2, pp. 192–198, 2000. View at Google Scholar · View at Scopus
  83. E. Bettelli, M. P. Das, E. D. Howard, H. L. Weiner, R. A. Sobel, and V. K. Kuchroo, “IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice,” Journal of Immunology, vol. 161, no. 7, pp. 3299–3306, 1998. View at Google Scholar · View at Scopus
  84. E. B. Samoilova, J. L. Horton, and Y. Chen, “Acceleration of experimental autoimmune encephalomyelitis in interleukin-10-deficient mice: roles of interleukin-10 in disease progression and recovery,” Cellular Immunology, vol. 188, no. 2, pp. 118–124, 1998. View at Publisher · View at Google Scholar · View at Scopus
  85. D. J. Cua, H. Groux, D. R. Hinton, S. A. Stohlman, and R. L. Coffman, “Transgenic interleukin 10 prevents induction of experimental autoimmune encephalomyelitis,” Journal of Experimental Medicine, vol. 189, no. 6, pp. 1005–1010, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. G. M. Cobrin and M. T. Abreu, “Defects in mucosal immunity leading to Crohn's disease,” Immunological Reviews, vol. 206, pp. 277–295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  87. S. K. Mazmanian and D. L. Kasper, “The love-hate relationship between bacterial polysaccharides and the host immune system,” Nature Reviews Immunology, vol. 6, no. 11, pp. 849–858, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Agostillo, C. Jene, T. Boyle, P. A. Ramsland, and E. Yuriev, “Molecular docking of carbohydrate ligands to antibodies: structural validation against crystal structures,” Journal of Chemical Information and Modeling, vol. 49, no. 12, pp. 2749–2760, 2009. View at Publisher · View at Google Scholar