About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 748160, 10 pages
http://dx.doi.org/10.1155/2013/748160
Research Article

Acetylsalicylic Acid Reduces the Severity of Dextran Sodium Sulfate-Induced Colitis and Increases the Formation of Anti-Inflammatory Lipid Mediators

1Department of Gastroenterology, Hepatology and Endocrinology, Virchow-Hospital, Charité Medical School, Free and Humboldt-University of Berlin, 13353 Berlin, Germany
2Laboratory for Lipid Medicine and Technology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
3Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
4Lurie Family Imaging Center, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115, USA
5Lipidomix GmbH, 13125 Berlin, Germany

Received 18 June 2013; Accepted 19 July 2013

Academic Editor: Gabriella Calviello

Copyright © 2013 Thomas Köhnke 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. D. C. Baumgart and S. R. Carding, “Inflammatory bowel disease: cause and immunobiology,” The Lancet, vol. 369, no. 9573, pp. 1627–1640, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. D. C. Baumgart and W. J. Sandborn, “Inflammatory bowel disease: clinical aspects and established and evolving therapies,” The Lancet, vol. 369, no. 9573, pp. 1641–1657, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. D. K. Podolsky, “Inflammatory bowel disease,” The New England Journal of Medicine, vol. 347, no. 6, pp. 417–429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. R. J. Xavier and D. K. Podolsky, “Unravelling the pathogenesis of inflammatory bowel disease,” Nature, vol. 448, no. 7152, pp. 427–434, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Takeuchi, S. Smale, P. Premchand et al., “Prevalence and mechanism of nonsteroidal anti-inflammatory drug-induced clinical relapse in patients with inflammatory bowel disease,” Clinical Gastroenterology and Hepatology, vol. 4, no. 2, pp. 196–202, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. R. S. Bloomfeld, “Are COX-2 inhibiotrs safe for anyone,” Inflammatory Bowel Diseases, vol. 12, no. 9, pp. 922–923, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. El Miedany, S. Youssef, I. Ahmed, and M. El Gaafary, “The gastrointestinal safety and effect on disease activity of etoricoxib, a selective Cox-2 inhibitor in inflammatory bowel diseases,” The American Journal of Gastroenterology, vol. 101, no. 2, pp. 311–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Matuk, J. Crawford, M. T. Abreu, S. R. Targan, E. A. Vasiliauskas, and K. A. Papadakis, “The spectrum of gastrointestinal toxicity and effect on disease activity of selective cyclooxygenase-2 inhibitors in patients with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 10, no. 4, pp. 352–356, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. L. A. Feagins and B. L. Cryer, “Do non-steroidal anti-inflammatory drugs cause exacerbations of inflammatory bowel disease?” Digestive Diseases and Sciences, vol. 55, no. 2, pp. 226–232, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Okayama, S. Hayashi, Y. Aoi, H. Nishio, S. Kato, and K. Takeuchi, “Aggravation by selective COX-1 and COX-2 inhibitors of dextran sulfate sodium (DSS)-induced colon lesions in rats,” Digestive Diseases and Sciences, vol. 52, no. 9, pp. 2095–2103, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Tsubouchi, S. Hayashi, Y. Aoi et al., “Healing impairment effect of cyclooxygenase inhibitors on dextran sulfate sodium-induced colitis in rats,” Digestion, vol. 74, no. 2, pp. 91–100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. O. Morteau, S. G. Morham, R. Sellon et al., “Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2,” Journal of Clinical Investigation, vol. 105, no. 4, pp. 469–478, 2000. View at Scopus
  13. J. L. Wallace, C. M. Keenan, D. Gale, and T. S. Shoupe, “Exacerbation of experimental colitis by nonsteroidal anti-inflammatory drugs is not related to elevated leukotriene B4 synthesis,” Gastroenterology, vol. 102, no. 1, pp. 18–27, 1992. View at Scopus
  14. A. R. Martín, I. Villegas, and C. Alarcón de la Lastra, “The COX-2 inhibitor, rofecoxib, ameliorates dextran sulphate sodium induced colitis in mice,” Inflammation Research, vol. 54, no. 4, pp. 145–151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Kankuri, K. Vaali, R. Korpela, I. Paakkari, H. Vapaatalo, and E. Moilanen, “Effects of a COX-2 preferential agent nimesulide on TNBS-induced acute inflammation in the gut,” Inflammation, vol. 25, no. 5, pp. 301–310, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. K. H. Weylandt, J. X. Kang, B. Wiedenmann, and D. C. Baumgart, “Lipoxins and resolvins in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 13, no. 6, pp. 797–799, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. C. N. Serhan, M. Hamberg, and B. Samuelsson, “Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 17 I, pp. 5335–5339, 1984. View at Scopus
  18. J. F. Parkinson, “Lipoxin and synthetic lipoxin analogs: an overview of anti-inflammatory functions and new concepts in immunomodulation,” Inflammation and Allergy, vol. 5, no. 2, pp. 91–106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. A. T. Gewirtz, L. S. Collier-Hyams, A. N. Young et al., “Lipoxin A4 analogs attenuate induction of intestinal epithelial proinflammatory gene expression and reduce the severity of dextran sodium sulfate-induced colitis,” Journal of Immunology, vol. 168, no. 10, pp. 5260–5267, 2002. View at Scopus
  20. S. Fiorucci, J. L. Wallace, A. Mencarelli et al., “A β-oxidation-resistant lipoxin A4 analog treats hapten-induced colitis by attenuating inflammation and immune dysfunction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15736–15741, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. C. A. Hudert, K. H. Weylandt, Y. Lu et al., “Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 30, pp. 11276–11281, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Arita, M. Yoshida, S. Hong et al., “Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 21, pp. 7671–7676, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. A. F. Bento, R. F. Claudino, R. C. Dutra, R. Marcon, and J. B. Calixto, “Omega-3 fatty acid-derived mediators 17(R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice,” Journal of Immunology, vol. 187, no. 4, pp. 1957–1969, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Ishida, M. Yoshida, M. Arita et al., “Resolvin E1, an endogenous lipid mediator derived from eicosapentaenoic acid, prevents dextran sulfate sodium-induced colitis,” Inflammatory Bowel Diseases, vol. 16, no. 1, pp. 87–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Melgar, L. Karlsson, E. Rehnström et al., “Validation of murine dextran sulfate sodium-induced colitis using four therapeutic agents for human inflammatory bowel disease,” International Immunopharmacology, vol. 8, no. 6, pp. 836–844, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Wirtz, C. Neufert, B. Weigmann, and M. F. Neurath, “Chemically induced mouse models of intestinal inflammation,” Nature Protocols, vol. 2, no. 3, pp. 541–546, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. M. F. Fredin, L. Hultin, G. Hyberg et al., “Predicting and monitoring colitis development in mice by micro-computed tomography,” Inflammatory Bowel Diseases, vol. 14, no. 4, pp. 491–499, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. A. E. Larsson, S. Melgar, E. Rehnstrom et al., “Magnetic resonance imaging of experimental mouse colitis and association with inflammatory activity,” Inflammatory Bowel Diseases, vol. 12, no. 6, pp. 478–485, 2006.
  29. S. Melgar, P. G. Gillberg, P. D. Hockings, and L. E. Olsson, “High-throughput magnetic resonance imaging in murine colonic inflammation,” Biochemical and Biophysical Research Communications, vol. 355, no. 4, pp. 1102–1107, 2007.
  30. L. A. Dieleman, M. J. Palmen, H. Akol et al., “Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines,” Clinical and Experimental Immunology, vol. 114, no. 3, pp. 385–391, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Gomolka, E. Siegert, K. Blossey, W.-H. Schunck, M. Rothe, and K. H. Weylandt, “Analysis of omega-3 and omega-6 fatty acid-derived lipid metabolite formation in human and mouse blood samples,” Prostaglandins and other Lipid Mediators, vol. 94, no. 3-4, pp. 81–87, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Spite and C. N. Serhan, “Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins,” Circulation Research, vol. 107, no. 10, pp. 1170–1184, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Li, A. Scherl, F. Medina et al., “Impaired phagocytosis in caveolin-1 deficient macrophages,” Cell Cycle, vol. 4, no. 11, pp. 1599–1607, 2005. View at Scopus
  34. C. P. Wan, C. S. Park, and B. H. S. Lau, “A rapid and simple microfluorometric phagocytosis assay,” Journal of Immunological Methods, vol. 162, no. 1, pp. 1–7, 1993. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Munkholm, “Review article: the incidence and prevalence of colorectal cancer in inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, Supplement, vol. 18, supplement 2, pp. 1–5, 2003. View at Scopus
  36. M. W. Lutgens, B. Oldenburg, P. D. Siersema et al., “Colonoscopic surveillance improves survival after colorectal cancer diagnosis in inflammatory bowel disease,” British Journal of Cancer, vol. 101, no. 10, pp. 1671–1675, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. T. Chan, E. L. Giovannucci, J. A. Meyerhardt, E. S. Schernhammer, G. C. Curhan, and C. S. Fuchs, “Long-term use of aspirin and nonsteroidal anti-inflammatory drugs and risk of colorectal cancer,” Journal of the American Medical Association, vol. 294, no. 8, pp. 914–923, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Rosenberg, C. Louik, and S. Shapiro, “Nonsteroidal antiinflammatory drug use and reduced risk of large bowel carcinoma,” Cancer, vol. 82, no. 12, pp. 2326–2333, 1998.
  39. E. Flossmann and P. M. Rothwell, “Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies,” The Lancet, vol. 369, no. 9573, pp. 1603–1613, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. P. M. Rothwell, M. Wilson, C.-E. Elwin et al., “Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials,” The Lancet, vol. 376, no. 9754, pp. 1741–1750, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. F. S. Velayos, E. V. Loftus Jr., T. Jess et al., “Predictive and protective factors associated with colorectal cancer in ulcerative colitis: a case-control study,” Gastroenterology, vol. 130, no. 7, pp. 1941–1949, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. L. A. Stark, K. Reid, O. J. Sansom et al., “Aspirin activates the NF-κB signalling pathway and induces apoptosis in intestinal neoplasia in two in vivo models of human colorectal cancer,” Carcinogenesis, vol. 28, no. 5, pp. 968–976, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. X. Zhang, Z. Wang, Y. Zhang, Q. Jia, L. Wu, and W. Zhang, “Impact of acetylsalicylic acid on tumor angiogenesis and lymphangiogenesis through inhibition of VEGF signaling in a murine sarcoma model,” Oncology Reports, vol. 29, no. 5, pp. 1907–1913, 2013. View at Publisher · View at Google Scholar
  44. M. A. Mcilhatton, J. Tyler, L. A. Kerepesi et al., “Aspirin and low-dose nitric oxide-donating aspirin increase life span in a Lynch syndrome mouse model,” Cancer Prevention Research, vol. 4, no. 5, pp. 684–693, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. N. N. Mahmoud, A. J. Dannenberg, J. Mestre et al., “Aspirin prevents tumors in a murine model of familial adenomatous polyposis,” Surgery, vol. 124, no. 2, pp. 225–231, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Tian, Y. Ye, W. Gao et al., “Aspirin promotes apoptosis in a murine model of colorectal cancer by mechanisms involving downregulation of IL-6-STAT3 signaling pathway,” International Journal of Colorectal Disease, vol. 26, no. 1, pp. 13–22, 2011.
  47. H. L. Newmark, “Nutrient density: an important and useful tool for laboratory animal studies,” Carcinogenesis, vol. 8, no. 7, pp. 871–873, 1987. View at Scopus
  48. A. González-Périz, A. Planagumà, K. Gronert et al., “Docosahexaenoic acid (DHA) blunts liver injury by conversion to protective lipid mediators: protectin D1 and 17S-hydroxy-DHA,” The FASEB Journal, vol. 20, no. 14, pp. 2537–2539, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Spite, L. V. Norling, L. Summers et al., “Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis,” Nature, vol. 461, no. 7268, pp. 1287–1291, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Spite, L. Summers, T. F. Porter, S. Srivastava, A. Bhatnagar, and C. N. Serhan, “Resolvin D1 controls inflammation initiated by glutathione-lipid conjugates formed during oxidative stress,” British Journal of Pharmacology, vol. 158, no. 4, pp. 1062–1073, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. Y.-P. Sun, S. F. Oh, J. Uddin et al., “Resolvin D1 and its aspirin-triggered 17R epimer: stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation,” Journal of Biological Chemistry, vol. 282, no. 13, pp. 9323–9334, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. J. F. Lima-Garcia, R. C. Dutra, K. A. B. S. Da Silva, E. M. Motta, M. M. Campos, and J. B. Calixto, “The precursor of resolvin D series and aspirin-triggered resolvin D1 display anti-hyperalgesic properties in adjuvant-induced arthritis in rats,” British Journal of Pharmacology, vol. 164, no. 2, pp. 278–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. K. H. Weylandt, L. F. Krause, B. Gomolka et al., “Suppressed liver tumorigenesis in fat-1 mice with elevated omega-3 fatty acids is associated with increased omega-3 derived lipid mediators and reduced TNF-α,” Carcinogenesis, vol. 32, no. 6, pp. 897–903, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Godson, S. Mitchell, K. Harvey, N. A. Petasis, N. Hogg, and H. R. Brady, “Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages,” Journal of Immunology, vol. 164, no. 4, pp. 1663–1667, 2000. View at Scopus
  55. D. Prescott and D. M. McKay, “Aspirin-triggered lipoxin enhances macrophage phagocytosis of bacteria while inhibiting inflammatory cytokine production,” International Journal of Colorectal Disease, vol. 2301, no. 3, pp. G487–G497, 2011. View at Publisher · View at Google Scholar
  56. S. Krishnamoorthy, A. Recchiuti, N. Chiang et al., “Resolvin D1 binds human phagocytes with evidence for proresolving receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 4, pp. 1660–1665, 2010. View at Publisher · View at Google Scholar · View at Scopus