Table of Contents
ISRN Gastroenterology
Volume 2011, Article ID 513514, 8 pages
http://dx.doi.org/10.5402/2011/513514
Review Article

Are Dysregulated Inflammatory Responses to Commensal Bacteria Involved in the Pathogenesis of Hepatobiliary-Pancreatic Autoimmune Disease? An Analysis Using Mice Models of Primary Biliary Cirrhosis and Autoimmune Pancreatitis

1Departments of Microbiology and Immunology, Tokyo Women’s Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, Japan
2Department of Infection Control Science, Faculty of Medicine, Juntendo University, Tokyo, Japan
3Department of Pathology, Tokyo Women’s Medical University, Tokyo, Japan

Received 28 April 2011; Accepted 17 May 2011

Academic Editors: A. Armuzzi and C.-T. Shun

Copyright © 2011 Naoko Yanagisawa 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. C. Selmi, M. J. Mayo, N. Bach et al., “Primary biliary cirrhosis in monozygotic and dizygotic twins: genetics, epigenetics, and environment,” Gastroenterology, vol. 127, no. 2, pp. 485–492, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Gasbarrini, F. Franceschi, R. Tartaglione, R. Landolfi, P. Pola, and G. Gasbarrini, “Regression of autoimmune thrombocytopenia after eradication of Helicobacter pylori,” The Lancet, vol. 352, no. 9131, p. 878, 1998. View at Google Scholar · View at Scopus
  3. N. Yuki, K. Susuki, M. Koga et al., “Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain-Barré syndrome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 31, pp. 11404–11409, 2004. View at Publisher · View at Google Scholar
  4. R. S. Houliston, E. Vinogradov, M. Dzieciatkowska et al., “Lipooligosaccharide of Campylobacter jejuni: similarity with multiple types of mammalian glycans beyond gangliosides,” The Journal of Biological Chemistry, vol. 286, no. 14, pp. 12361–12370, 2011. View at Publisher · View at Google Scholar
  5. H. Tlaskalová-Hogenova, R. Štepánková, T. Hudcovic et al., “Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases,” Immunology Letters, vol. 93, no. 2-3, pp. 97–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Aoki, “Rheumatoid arthritis and enteric bacteria,” Japanese Journal of Rheumatology, vol. 9, no. 4, pp. 325–352, 1999. View at Google Scholar · View at Scopus
  7. M. M. Kaplan and M. E. Gershwin, “Primary biliary cirrhosis,” The New England Journal of Medicine, vol. 353, no. 12, pp. 1261–1273, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Selmi, I. R. MacKay, and M. E. Gershwin, “The autoimmunity of primary biliary cirrhosis and the clonal selection theory,” Immunology and Cell Biology, vol. 89, no. 1, pp. 70–80, 2011. View at Publisher · View at Google Scholar
  9. K. Harada, K. Tsuneyama, Y. Sudo, S. Masuda, and Y. Nakanuma, “Molecular identification of bacterial 16S ribosomal RNA gene in liver tissue of primary biliary cirrhosis: is Propionibacterium acnes involved in granuloma formation?” Hepatology, vol. 33, no. 3, pp. 530–536, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. D. P. Bogdanos, H. Baum, A. Grasso et al., “Microbial mimics are major targets of crossreactivity with human pyruvate dehydrogenase in primary biliary cirrhosis,” Journal of Hepatology, vol. 40, no. 1, pp. 31–39, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Olafsson, H. Gudjonsson, C. Selmi et al., “Antimitochondrial antibodies and reactivity to N. aromaticivorans proteins in icelandic patients with primary biliary cirrhosis and their relatives,” The American Journal of Gastroenterology, vol. 99, no. 11, pp. 2143–2146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Bogdanos, T. Pusl, C. Rust, D. Vergani, and U. Beuers, “Primary biliary cirrhosis following lactobacillus vaccination for recurrent vaginitis,” Journal of Hepatology, vol. 49, no. 3, pp. 466–473, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. A. I. P. Wang, K. Migita, M. Ito et al., “Hepatic expression of toll-like receptor 4 in primary biliary cirrhosis,” Journal of Autoimmunity, vol. 25, no. 1, pp. 85–91, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Yokoyama, A. Komori, M. Nakamura et al., “Human intrahepatic biliary epithelial cells function in innate immunity by producing IL-6 and IL-8 via the TLR4-NF-κB and -MAPK signaling pathways,” Liver International, vol. 26, no. 4, pp. 467–476, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Moritoki, Z. X. Lian, H. Wulff et al., “AMA production in primary biliary cirrhosis is promoted by the TLR9 ligand CpG and suppressed by potassium channel blockers,” Hepatology, vol. 45, no. 2, pp. 314–322, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Shimoda, K. Harada, H. Niiro et al., “Biliary epithelial cells and primary biliary cirrhosis: the role of liver-infiltrating mononuclear cells,” Hepatology, vol. 47, no. 3, pp. 958–965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. K. Mao, Z. X. Lian, C. Selmi et al., “Altered monocyte responses to defined TLR ligands in patients with primary biliary cirrhosis,” Hepatology, vol. 42, no. 4, pp. 802–808, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Kikuchi, Z. X. Lian, G. X. Yang et al., “Bacterial CpG induces hyper-IgM production in CD27+ memory B cells in primary biliary cirrhosis,” Gastroenterology, vol. 128, no. 2, pp. 304–312, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Haruta, E. Hashimoto, N. Shibata, Y. Kato, M. Kobayashi, and K. Shiratori, “Lipoteichoic acid may affect the pathogenesis of PBC-like bile duct damage and might be involved in systemic multifocal epithelial inflammations in chronic colitis-harboring TCRα-/- × AIM-/- mice,” Autoimmunity, vol. 40, no. 5, pp. 372–379, 2007. View at Publisher · View at Google Scholar
  20. I. Haruta, K. Kikuchi, E. Hashimoto et al., “A possible role of histone-like DNA-binding protein of Streptococcus intermedius in the pathogenesis of bile duct damage in primary biliary cirrhosis,” Clinical Immunology, vol. 127, no. 2, pp. 245–251, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Selmi, A. Diana, C. A. Cocchi, M. Zuin, and M. E. Gershwin, “Environmental factors and the induction of autoimmunity in primary biliary cirrhosis,” Expert Review of Clinical Immunology, vol. 4, no. 2, pp. 239–245, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. R. A. Whiley, D. Beighton, T. G. Winstanley, H. Y. Fraser, and J. M. Hardie, “Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections,” Journal of Clinical Microbiology, vol. 30, no. 1, pp. 243–244, 1992. View at Google Scholar · View at Scopus
  23. F. C. Petersen, D. Pecharki, and A. A. Scheie, “Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide,” The Journal of Bacteriology, vol. 186, no. 18, pp. 6327–6331, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. J. J. Feld, J. Meddings, and E. J. Heathcote, “Abnormal intestinal permeability in primary biliary cirrhosis,” Digestive Diseases and Sciences, vol. 51, no. 9, pp. 1607–1613, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Haruta, K. Kikuchi, E. Hashimoto et al., “Long-term bacterial exposure can trigger nonsuppurative destructive cholangitis associated with multifocal epithelial inflammation,” Laboratory Investigation, vol. 90, no. 4, pp. 577–588, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Nakamura, H. Kondo, T. Mori et al., “Anti-gp210 and anti-centromere antibodies are different risk factors for the progression of primary biliary cirrhosis,” Hepatology, vol. 45, no. 1, pp. 118–127, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Okazaki, K. Uchida, H. Miyoshi, T. Ikeura, M. Takaoka, and A. Nishio, “Recent concepts of autoimmune pancreatitis and IgG4-related disease,” Clinical Reviews in Allergy and Immunology. In press. View at Publisher · View at Google Scholar
  28. D. H. Park, M. H. Kim, and S. T. Chari, “Recent advances in autoimmune pancreatitis,” Gut, vol. 58, no. 12, pp. 1680–1689, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Okazaki, K. Uchida, and T. Fukui, “Recent advances in autoimmune pancreatitis: concept, diagnosis, and pathogenesis,” Journal of Gastroenterology, vol. 43, no. 6, pp. 409–418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Okazaki, K. Uchida, M. Koyabu, H. Miyoshi, and M. Takaoka, “Recent advances in the concept and diagnosis of autoimmune pancreatitis and IgG4-related disease,” Journal of Gastroenterology, vol. 46, no. 3, pp. 277–288, 2011. View at Publisher · View at Google Scholar
  31. T. Shimosegawa and A. Kanno, “Autoimmune pancreatitis in Japan: overview and perspective,” Journal of Gastroenterology, vol. 44, no. 6, pp. 503–517, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Ota, Y. Katsuyama, H. Hamano et al., “Two critical genes (HLA-DRB1 and ABCF1) in the HLA region are associated with the susceptibility to autoimmune pancreatitis,” Immunogenetics, vol. 59, no. 1, pp. 45–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Muraki, H. Hamano, Y. Ochi et al., “Autoimmune pancreatitis and complement activation system,” Pancreas, vol. 32, no. 1, pp. 16–21, 2006. View at Google Scholar · View at Scopus
  34. S. Kawa, M. Ota, K. Yoshizawa et al., “HLA DRB10405-DQB10401 haplotype is associated with autoimmune pancreatitis in the Japanese population,” Gastroenterology, vol. 122, no. 5, pp. 1264–1269, 2002. View at Google Scholar · View at Scopus
  35. M. Kojima, B. Sipos, W. Klapper et al., “Autoimmune pancreatitis: frequency, IgG4 expression, and clonality of T and B cells,” The American Journal of Surgical Pathology, vol. 31, no. 4, pp. 521–528, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Umemura, M. Ota, H. Hamano et al., “Association of autoimmune pancreatitis with cytotoxic T-lymphocyte antigen 4 gene polymorphisms in Japanese patients,” The American Journal of Gastroenterology, vol. 103, no. 3, pp. 588–594, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Hamano, S. Kawa, A. Horiuchi et al., “High serum IgG4 concentrations in patients with sclerosing pancreatitis,” The New England Journal of Medicine, vol. 344, no. 10, pp. 732–738, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Aoki, T. Nakazawa, H. Ohara et al., “Immunohistochemical study of autoimmune pancreatitis using anti-IgG4 antibody and patients' sera,” Histopathology, vol. 47, no. 2, pp. 147–158, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Detlefsen, J. H. Bräsen, G. Zamboni, P. Capelli, and G. Klöppel, “Deposition of complement C3c, immunoglobulin (Ig)G4 and IgG at the basement membrane of pancreatic ducts and acini in autoimmune pancreatitis,” Histopathology, vol. 57, no. 6, pp. 825–835, 2010. View at Publisher · View at Google Scholar
  40. S. Kawa, K. Kitahara, H. Hamano et al., “A novel immunoglobulin-immunoglobulin interaction in autoimmunity,” PLoS One, vol. 3, no. 2, article e1637, 2008. View at Publisher · View at Google Scholar
  41. T. Ito, K. Kitahara, T. Umemura et al., “A novel heterophilic antibody interaction involves igG4,” Scandinavian Journal of Immunology, vol. 71, no. 2, pp. 109–114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Kanno, M. Nose, J. Itoh, Y. Taniguchi, and M. Kyogoku, “Spontaneous development of pancreatitis in the MRL/Mp strain of mice in autoimmune mechanism,” Clinical and Experimental Immunology, vol. 89, no. 1, pp. 68–73, 1992. View at Google Scholar · View at Scopus
  43. N. Hosaka, M. Nose, M. Kyogoku et al., “Thymus transplantation, a critical factor for correction of autoimmune disease in aging MRL/+ mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 16, pp. 8558–8562, 1996. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Tsubata, T. Tsubata, H. Hiai et al., “Autoimmune disease of exocrine organs in immunodeficient alymphoplasia mice: a spontaneous model for Sjogren's syndrome,” European Journal of Immunology, vol. 26, no. 11, pp. 2742–2748, 1996. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Nakamura, S. Q. Yi, H. Terayama et al., “Sequential histopathology of pancreatic tissues in aly/aly mice,” Cells Tissues Organs, vol. 186, no. 3, pp. 204–209, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. H. X. Wang, S. Q. Yi, J. Li et al., “Effects of splenectomy on spontaneously chronic pancreatitis in aly/aly mice,” Clinical and Developmental Immunology, vol. 2010, Article ID 614890, 8 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Sakaguchi, M. Inaba, M. Tsuda et al., “The Wistar Bonn Kobori rat, a unique animal model for autoimmune pancreatitis with extrapancreatic exocrinopathy,” Clinical and Experimental Immunology, vol. 152, no. 1, pp. 1–12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. B. A. Vallance, B. R. Hewlett, D. P. Snider, and S. M. Collins, “T cell-mediated exocrine pancreatic damage in major histocompatibility complex class II-deficient mice,” Gastroenterology, vol. 115, no. 4, pp. 978–987, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. T. L. Freitag, C. Cham, H. H. Sung et al., “Human risk Allele HLA-DRB1*0405 predisposes class II transgenic Ab0 NOD mice to autoimmune pancreatitis,” Gastroenterology, vol. 139, no. 1, pp. 281–291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. C. S. Boomershine, A. Chamberlain, P. Kendall et al., “Autoimmune pancreatitis results from loss of TGFβ signalling in S100A4-positive dendritic cells,” Gut, vol. 58, no. 9, pp. 1267–1274, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Meagher, Q. Tang, B. T. Fife et al., “Spontaneous development of a pancreatic exocrine disease in CD28-deficient NOD mice,” The Journal of Immunology, vol. 180, no. 12, pp. 7793–7803, 2008. View at Google Scholar · View at Scopus
  52. T. S. Davidson, D. S. Longnecker, and W. F. Hickey, “An experimental model of autoimmune pancreatitis in the rat,” The American Journal of Pathology, vol. 166, no. 3, pp. 729–736, 2005. View at Google Scholar · View at Scopus
  53. I. Nishimori, T. Bratanova, I. Toshkov et al., “Induction of experimental autoimmune sialoadenitis by immunization of PL/J mice with carbonic anhydrase II,” The Journal of Immunology, vol. 154, no. 9, pp. 4865–4873, 1995. View at Google Scholar · View at Scopus
  54. K. Uchida, K. Okazaki, T. Nishi et al., “Experimental immune-mediated pancreatitis in neonatally thymectomized mice immunized with carbonic anhydrase II and lactoferrin,” Laboratory Investigation, vol. 82, no. 4, pp. 411–424, 2002. View at Google Scholar · View at Scopus
  55. A. Nishio, M. Asada, K. Uchida, T. Fukui, T. Chiba, and K. Okazaki, “The role of innate immunity in the pathogenesis of experimental autoimmune pancreatitis in mice,” Pancreas, vol. 40, no. 1, pp. 95–102, 2011. View at Publisher · View at Google Scholar
  56. Y. Soga, H. Komori, T. Miyazaki et al., “Toll-like receptor 3 signaling induces chronic pancreatitis through the Fas/Fas ligand-mediated cytotoxicity,” Tohoku Journal of Experimental Medicine, vol. 217, no. 3, pp. 175–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. W. M. Qu, T. Miyazaki, M. Terada et al., “A novel autoimmune pancreatitis model in MRL mice treated with polyinosinic:polycytidylic acid,” Clinical and Experimental Immunology, vol. 129, no. 1, pp. 27–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Asada, A. Nishio, T. Akamatsu et al., “Analysis of humoral immune response in experimental autoimmune pancreatitis in mice,” Pancreas, vol. 39, no. 2, pp. 224–231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Watanabe, K. Suzuki, Y. Kawauchi et al., “Kinetic analysis of the development of pancreatic lesions in mice infected with a murine retrovirus,” Clinical Immunology, vol. 109, no. 2, pp. 212–223, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Suzuki, M. Makino, Y. Okada et al., “Exocrinopathy resembling Sjogren's syndrome induced by a murine retrovirus,” Laboratory Investigation, vol. 69, no. 4, pp. 430–435, 1993. View at Google Scholar · View at Scopus
  61. I. Haruta, N. Yanagisawa, S. Kawamura et al., “A mouse model of autoimmune pancreatitis with salivary gland involvement triggered by innate immunity via persistent exposure to avirulent bacteria,” Laboratory Investigation, vol. 90, no. 12, pp. 1757–1769, 2010. View at Publisher · View at Google Scholar
  62. K. Okazaki, K. Uchida, M. Ohana et al., “Autoimmune-related pancreatitis is associated with autoantibodies and a Th1/Th2-type cellular immune response,” Gastroenterology, vol. 118, no. 3, pp. 573–581, 2000. View at Google Scholar · View at Scopus
  63. I. Nishimori, E. Miyaji, K. Morimoto, K. Nagao, M. Kamada, and S. Onishi, “Serum antibodies to carbonic anhydrase IV in patients with autoimmune pancreatitis,” Gut, vol. 54, no. 2, pp. 274–281, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Asada, A. Nishio, K. Uchida et al., “Identification of a novel autoantibody against pancreatic secretory trypsin inhibitor in patients with autoimmune pancreatitis,” Pancreas, vol. 33, no. 1, pp. 20–26, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Takizawa, T. Endo, X. Wanjia, S. Tanaka, M. Takahashi, and T. Kobayashi, “HSP 10 is a new autoantigen in both autoimmune pancreatitis and fulminant type 1 diabetes,” Biochemical and Biophysical Research Communications, vol. 386, no. 1, pp. 192–196, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. F. Guarneri, C. Guarneri, and S. Benvenga, “Helicobacter pylori and autoimmune pancreatitis: role of carbonic anhydrase via molecular mimicry?” Journal of Cellular and Molecular Medicine, vol. 9, no. 3, pp. 741–744, 2005. View at Google Scholar · View at Scopus
  67. L. Frulloni, C. Lunardi, R. Simone et al., “Identification of a novel antibody associated with autoimmune pancreatitis,” The New England Journal of Medicine, vol. 361, no. 22, pp. 2135–2142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Li, Y. Zhou, G. Feng, and S. B. Su, “The critical role of toll-like receptor signaling pathways in the induction and progression of autoimmune disease,” Current Molecular Medicine, vol. 9, no. 3, pp. 365–374, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. N. R. Rose and C. Bona, “Defining criteria for autoimmune diseases (Witebsky's postulates revisited),” Immunology Today, vol. 14, no. 9, pp. 426–430, 1993. View at Google Scholar · View at Scopus
  70. J. Irie, Y. Wu, L. S. Wicker et al., “NOD.c3c4 congenic mice develop autoimmune biliary disease that serologically and pathogenetically models human primary biliary cirrhosis,” Journal of Experimental Medicine, vol. 203, no. 5, pp. 1209–1219, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Oertelt, Z. X. Lian, C. M. Cheng et al., “Anti-mitochondrial antibodies and primary biliary cirrhosis in TGF-βreceptor II dominant-negative mice,” The Journal of Immunology, vol. 177, no. 3, pp. 1655–1660, 2006. View at Google Scholar · View at Scopus
  72. K. Wakabayashi, Z. X. Lian, Y. Moritoki et al., “IL-2 receptor α mice and the development of primary biliary cirrhosis,” Hepatology, vol. 44, no. 5, pp. 1240–1249, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. J. T. Salas, J. M. Banales, S. Sarvide et al., “Ae2-deficient mice develop antimitochondrial antibodies and other features resembling primary biliary cirrhosis,” Gastroenterology, vol. 134, no. 5, pp. 1482–1493, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. A. de Moreno de LeBlanc, S. del Carmen, M. Zurita-Turk et al., “Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases,” ISRN Gastroenterology, vol. 2011, Article ID 892971, 11 pages, 2011. View at Publisher · View at Google Scholar
  75. R. M. McLoughlin and K. H. G. Mills, “Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma,” Journal of Allergy and Clinical Immunology, vol. 127, no. 5, pp. 1097–1107, 2011. View at Publisher · View at Google Scholar