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International Journal of Inflammation
Volume 2012, Article ID 504128, 12 pages
http://dx.doi.org/10.1155/2012/504128
Research Article

Cytosolic Double-Stranded DNA as a Damage-Associated Molecular Pattern Induces the Inflammatory Response in Rat Pancreatic Stellate Cells: A Plausible Mechanism for Tissue Injury-Associated Pancreatitis

1Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
2Leprosy Research Center, National Institute of Infectious Diseases, Tokyo 189-0002, Japan
3Cell Biology Section, NIDDK, National Institutes of Health, Bethesda, MD 20892, USA

Received 25 November 2011; Revised 9 January 2012; Accepted 14 January 2012

Academic Editor: Zoltan Rakonczay

Copyright © 2012 Taichi Nakamura 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. M. V. Apte, P. S. Haber, T. L. Applegate et al., “Periacinar stellate shaped cells in rat pancreas: Identification, isolation, and culture,” Gut, vol. 43, no. 1, pp. 128–133, 1998. View at Google Scholar · View at Scopus
  2. M. G. Bachem, E. Schneider, H. Gross et al., “Identification, culture, and characterization of pancreatic stellate cells in rats and humans,” Gastroenterology, vol. 115, no. 2, pp. 421–432, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. M. B. Omary, A. Lugea, A. W. Lowe, and S. J. Pandol, “The pancreatic stellate cell: a star on the rise in pancreatic diseases,” Journal of Clinical Investigation, vol. 117, no. 1, pp. 50–59, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Shimizu, “Mechanisms of pancreatic fibrosis and applications to the treatment of chronic pancreatitis,” Journal of Gastroenterology, vol. 43, no. 11, pp. 823–832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Masamune, T. Watanabe, K. Kikuta, and T. Shimosegawa, “Roles of pancreatic stellate cells in pancreatic inflammation and fibrosis,” Clinical Gastroenterology and Hepatology, vol. 7, supplement 11, pp. S48–S54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Tahara, K. Shimizu, and K. Shiratori, “Engulfment of necrotic acinar cells by pancreatic stellate cells inhibits pancreatic fibrogenesis,” Pancreas, vol. 37, no. 1, pp. 69–74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Isaacs, R. A. Cox, and Z. Rotem, “Foreign nucleic acids as the stimulus to make interferon,” The Lancet, vol. 282, no. 7299, pp. 113–116, 1963. View at Google Scholar · View at Scopus
  8. T. Tokunaga, H. Yamamoto, S. Shimada et al., “Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity,” Journal of the National Cancer Institute, vol. 72, no. 4, pp. 955–962, 1984. View at Google Scholar
  9. A. M. Krieg, A. K. Yi, S. Matson et al., “CpG motifs in bacterial DNA trigger direct B-cell activation,” Nature, vol. 374, no. 6522, pp. 546–549, 1995. View at Google Scholar · View at Scopus
  10. M. Bauer, V. Redecke, J. W. Ellwart et al., “Bacterial CpG-DNA triggers activation and maturation of human CD11c-, CD123+ dendritic cells,” Journal of Immunology, vol. 166, no. 8, pp. 5000–5007, 2001. View at Google Scholar · View at Scopus
  11. T. Nakamura, T. Ito, T. Oono et al., “Bacterial DNA promotes proliferation of rat pancreatic stellate cells thorough toll-like receptor 9: potential mechanisms for bacterially induced fibrosis,” Pancreas, vol. 40, no. 6, pp. 823–831, 2011. View at Publisher · View at Google Scholar
  12. K. Suzuki, A. Mori, K. J. Ishii et al., “Activation of target-tissue immune-recognition molecules by double-stranded polynucleotides,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 5, pp. 2285–2290, 1999. View at Google Scholar · View at Scopus
  13. K. Kawane, H. Fukuyama, G. Kondoh et al., “Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver,” Science, vol. 292, no. 5521, pp. 1546–1549, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. H. Chiu, J. B. MacMillan, and Z. J. Chen, “RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway,” Cell, vol. 138, no. 3, pp. 576–591, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Shimizu, M. Kobayashi, J. Tahara, and K. Shiratori, “Cytokines and peroxisome proliferator-activated receptor γ ligand regulate phagocytosis by pancreatic stellate cells,” Gastroenterology, vol. 128, no. 7, pp. 2105–2118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Vonlaufen, M. V. Apte, B. A. Imhof, and J. L. Frossard, “The role of inflammatory and parenchymal cells in acute pancreatitis,” Journal of Pathology, vol. 213, no. 3, pp. 239–248, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Masamune, K. Kikuta, T. Watanabe, K. Satoh, A. Satoh, and T. Shimosegawa, “Pancreatic stellate cells express toll-like receptors,” Journal of Gastroenterology, vol. 43, no. 5, pp. 352–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. P. A. Phillips, J. A. McCarroll, S. Park et al., “Rat pancreatic stellate cells secrete matrix metalloproteinases: implications for extracellular matrix turnover,” Gut, vol. 52, no. 2, pp. 275–282, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M. E. Bianchi, “DAMPs, PAMPs and alarmins: all we need to know about danger,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 1–5, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Akira, “Innate immunity to pathogens: diversity in receptors for microbial recognition,” Immunological Reviews, vol. 227, no. 1, pp. 5–8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Saitoh and S. Akira, “Regulation of innate immune responses by autophagy-related proteins,” Journal of Cell Biology, vol. 189, no. 6, pp. 925–935, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Marichal, K. Ohata, D. Bedoret et al., “DNA released from dying host cells mediates aluminum adjuvant activity,” Nature Medicine, vol. 17, no. 8, pp. 996–1002, 2011. View at Publisher · View at Google Scholar
  23. Q. Zhang, M. Raoof, Y. Chen et al., “Circulating mitochondrial DAMPs cause inflammatory responses to injury,” Nature, vol. 464, no. 7285, pp. 104–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Pardo, N. Budick-Harmelin, B. Tirosh, and O. Tirosh, “Antioxidant defense in hepatic ischemia-reperfusion injury is regulated by damage-associated molecular pattern signal molecules,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1073–1083, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. K. P. Mollen, R. M. Levy, J. M. Prince et al., “Systemic inflammation and end organ damage following trauma involves functional TLR4 signaling in both bone marrow-derived cells and parenchymal cells,” Journal of Leukocyte Biology, vol. 83, no. 1, pp. 80–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Matzinger, “The danger model: a renewed sense of self,” Science, vol. 296, no. 5566, pp. 301–305, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Kawashima, K. Tanigawa, T. Akama et al., “Fragments of genomic DNA released by injured cells activate innate immunity and suppress endocrine function in the thyroid,” Endocrinology, vol. 152, no. 4, pp. 702–712, 2011. View at Google Scholar
  28. K. J. Ishii, K. Suzuki, C. Coban et al., “Genomic DNA released by dying cells induces the maturation of APCs,” Journal of Immunology, vol. 167, no. 5, pp. 2602–2607, 2001. View at Google Scholar · View at Scopus
  29. M. Napirei, H. Karsunky, B. Zevnik, H. Stephan, H. G. Mannherz, and T. Moroy, “Features of systemic lupus erythematosus in Dnase1-deficient mice,” Nature Genetics, vol. 25, no. 2, pp. 177–181, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Morita, G. Stamp, P. Robins et al., “Gene-targeted mice lacking the Trex1 (DNase III) 35 DNA exonuclease develop inflammatory myocarditis,” Molecular and Cellular Biology, vol. 24, no. 15, pp. 6719–6727, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Takaoka and S. Shinohara, “DNA sensors in innate immune system,” Uirusu, vol. 58, no. 1, pp. 37–46, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Vilaysane and D. A. Muruve, “The innate immune response to DNA,” Seminars in Immunology, vol. 21, no. 4, pp. 208–214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Kobiyama, F. Takeshita, N. Jounai et al., “Extrachromosomal histone H2B mediates innate antiviral immune responses induced by intracellular double-stranded DNA,” Journal of Virology, vol. 84, no. 2, pp. 822–832, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Kawashima, K. Tanigawa, T. Akama, A. Yoshihara, N. Ishii, and K. Suzuki, “Innate immune activation and thyroid autoimmunity,” Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 12, pp. 3661–3671, 2011. View at Publisher · View at Google Scholar
  35. A. Vonlaufen, Z. Xu, B. Daniel et al., “Bacterial endotoxin: a trigger factor for alcoholic pancreatitis? Evidence from a novel, physiologically relevant animal model,” Gastroenterology, vol. 133, no. 4, pp. 1293–1303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Morishita, K. Shimizu, I. Haruta, S. Kawamura, M. Kobayashi, and K. Shiratori, “Engulfment of gram-positive bacteria by pancreatic stellate cells in pancreatic fibrosis,” Pancreas, vol. 39, no. 7, pp. 1002–1007, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Bedossa, J. Bacci, G. Lemaigre, and E. Martin, “Lymphocyte subsets and HLA-DR expression in normal pancreas in chronic pancreatitis,” Pancreas, vol. 5, no. 4, pp. 415–420, 1990. View at Google Scholar · View at Scopus
  38. R. P. Jalleh, J. A. Gilbertson, R. C. N. Williamson, S. D. Slater, and C. S. Foster, “Expression of major histocompatibility antigens in human chronic pancreatitis,” Gut, vol. 34, no. 10, pp. 1452–1457, 1993. View at Google Scholar · View at Scopus
  39. L. S. Wicker, M. C. Appel, F. Dotta et al., “Autoimmune syndromes in major histocompatibility complex (MHC) congenic strains of nonobese diabetic (NOD) mice. The NOD MHC is dominant for insulitis and cyclophosphamide-induced diabetes,” Journal of Experimental Medicine, vol. 176, no. 1, pp. 67–77, 1992. View at Publisher · View at Google Scholar · View at Scopus
  40. 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
  41. T. Watanabe, A. Masamune, K. Kikuta et al., “Bone marrow contributes to the population of pancreatic stellate cells in mice,” American Journal of Physiology, vol. 297, no. 6, pp. G1138–G1146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Sparmann, M. L. Kruse, N. Hofmeister-Mielke et al., “Bone marrow-derived pancreatic stellate cells in rats,” Cell Research, vol. 20, no. 3, pp. 288–298, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Y. Feng and Y. Y. Li, “Alteration and role of heat shock proteins in acute pancreatitis,” Journal of Digestive Diseases, vol. 11, no. 5, pp. 277–283, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. P. A. Banks, M. Hughes, M. Ferrante, E. C. Noordhoek, V. Ramagopal, and A. Slivka, “Does allopurinol reduce pain of chronic pancreatitis?” International Journal of Pancreatology, vol. 22, no. 3, pp. 171–176, 1997. View at Google Scholar · View at Scopus