Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2017, Article ID 5126048, 8 pages
https://doi.org/10.1155/2017/5126048
Review Article

The Role of Proinflammatory Pathways in the Pathogenesis of Colitis-Associated Colorectal Cancer

Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, China

Correspondence should be addressed to Hu Zhang; nc.ude.ucs@uhgnahz

Received 15 April 2017; Revised 30 June 2017; Accepted 17 July 2017; Published 9 August 2017

Academic Editor: Manoj K. Mishra

Copyright © 2017 Chengxin Luo and Hu Zhang. 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. T. Ullman, R. Odze, and F. A. Farraye, “Diagnosis and management of dysplasia in patients with ulcerative colitis and Crohn’s disease of the colon,” Inflammatory Bowel Diseases, vol. 15, pp. 630–638, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. A. Eaden, K. R. Abrams, and J. F. Mayberry, “The risk of colorectal cancer in ulcerative colitis: a meta-analysis,” Gut, vol. 48, pp. 526–535, 2001. View at Google Scholar
  3. C. Castano-Milla, M. Chaparro, and J. P. Gisbert, “Systematic review with meta-analysis: the declining risk of colorectal cancer in ulcerative colitis,” Alimentary Pharmacology & Therapeutics, vol. 39, pp. 645–659, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Canavan, K. R. Abrams, and J. Mayberry, “Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn’s disease,” Alimentary Pharmacology & Therapeutics, vol. 23, pp. 1097–1104, 2006. View at Google Scholar
  5. S. Sebastian, V. Hernandez, P. Myrelid et al., “Colorectal cancer in inflammatory bowel disease: results of the 3rd ECCO pathogenesis scientific workshop (I),” Journal of Crohn's & Colitis, vol. 8, pp. 5–18, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. C. D. Gillen, R. S. Walmsley, P. Prior, H. A. Andrews, and R. N. Allan, “Ulcerative colitis and Crohn's disease: a comparison of the colorectal cancer risk in extensive colitis,” Gut, vol. 35, no. 11, pp. 1590–1592, 1994. View at Google Scholar
  7. A. Ekbom, C. Helmick, M. Zack, and H. O. Adami, “Ulcerative colitis and colorectal cancer. A population-based study,” The New England Journal of Medicine, vol. 323, pp. 1228–1233, 1990. View at Publisher · View at Google Scholar
  8. M. Rutter, B. Saunders, K. Wilkinson et al., “Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis,” Gastroenterology, vol. 126, pp. 451–459, 2004. View at Google Scholar
  9. R. Wang and R. W. Leong, “Primary sclerosing cholangitis as an independent risk factor for colorectal cancer in the context of inflammatory bowel disease: a review of the literature,” World Journal of Gastroenterology, vol. 20, pp. 8783–8789, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. R. M. Soetikno, O. S. Lin, P. A. Heidenreich, H. S. Young, and M. O. Blackstone, “Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: a meta-analysis,” Gastrointestinal Endoscopy, vol. 56, pp. 48–54, 2002. View at Google Scholar
  11. S. H. Itzkowitz and X. Yio, “Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation,” American Journal of Physiology. Gastrointestinal and Liver Physiology, vol. 287, pp. G7–17, 2004. View at Google Scholar
  12. D. E. Aust, J. P. Terdiman, R. F. Willenbucher et al., “The APC/beta-catenin pathway in ulcerative colitis-related colorectal carcinomas: a mutational analysis,” Cancer, vol. 94, pp. 1421–1427, 2002. View at Google Scholar
  13. T. Watanabe, T. Konishi, J. Kishimoto et al., “Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study,” Inflammatory Bowel Diseases, vol. 17, pp. 802–808, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. S. H. Itzkowitz, “Molecular biology of dysplasia and cancer in inflammatory bowel disease,” Gastroenterology Clinics of North America, vol. 35, pp. 553–571, 2006. View at Google Scholar
  15. S. A. Azer, “Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development,” European Journal of Gastroenterology & Hepatology, vol. 25, pp. 271–281, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Karin and F. R. Greten, “NF-kappaB: linking inflammation and immunity to cancer development and progression,” Nature Reviews. Immunology, vol. 5, pp. 749–759, 2005. View at Google Scholar
  17. M. Karin, “Nuclear factor-kappaB in cancer development and progression,” Nature, vol. 441, pp. 431–436, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. P. M. O'Connor, T. K. Lapointe, P. L. Beck, and A. G. Buret, “Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 16, pp. 1411–1420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Atreya, R. Atreya, and M. F. Neurath, “NF-kappaB in inflammatory bowel disease,” Journal of Internal Medicine, vol. 263, pp. 591–596, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. N. N. Danial and S. J. Korsmeyer, “Cell death: critical control points,” Cell, vol. 116, pp. 205–219, 2004. View at Google Scholar
  21. S. Wang, Z. Liu, L. Wang, and X. Zhang, “NF-kappaB signaling pathway, inflammation and colorectal cancer,” Cellular & Molecular Immunology, vol. 6, pp. 327–334, 2009. View at Publisher · View at Google Scholar
  22. F. R. Greten, L. Eckmann, T. F. Greten et al., “IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer,” Cell, vol. 118, pp. 285–296, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. B. K. Popivanova, K. Kitamura, Y. Wu et al., “Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis,” The Journal of Clinical Investigation, vol. 118, pp. 560–570, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Mehrad, M. P. Keane, and R. M. Strieter, “Chemokines as mediators of angiogenesis,” Thrombosis and Haemostasis, vol. 97, no. 5, pp. 755–762, 2007. View at Google Scholar
  25. Y. J. Kim, K. S. Hong, J. W. Chung, J. H. Kim, and K. B. Hahm, “Prevention of colitis-associated carcinogenesis with infliximab,” Cancer Prevention Research (Philadelphia, Pa.), vol. 3, pp. 1314–1333, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Atreya and M. F. Neurath, “Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer,” Clinical Reviews in Allergy & Immunology, vol. 28, pp. 187–196, 2005. View at Google Scholar
  27. A. Chalaris, D. Schmidt-Arras, K. Yamamoto, and S. Rose-John, “Interleukin-6 trans-signaling and colonic cancer associated with inflammatory bowel disease,” Digestive Diseases, vol. 30, pp. 492–499, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. G. W. Jones, R. M. McLoughlin, V. J. Hammond et al., “Loss of CD4+ T cell IL-6R expression during inflammation underlines a role for IL-6 trans signaling in the local maintenance of Th17 cells,” Journal of Immunology, vol. 184, pp. 2130–2139, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Rabe, A. Chalaris, U. May et al., “Transgenic blockade of interleukin 6 transsignaling abrogates inflammation,” Blood, vol. 111, pp. 1021–1028, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Romano, M. Sironi, C. Toniatti et al., “Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment,” Immunity, vol. 6, pp. 315–325, 1997. View at Google Scholar
  31. Y. C. Chung and Y. F. Chang, “Serum interleukin-6 levels reflect the disease status of colorectal cancer,” Journal of Surgical Oncology, vol. 83, pp. 222–226, 2003. View at Google Scholar
  32. S. Grivennikov, E. Karin, J. Terzic et al., “IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer,” Cancer Cell, vol. 15, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Becker, M. C. Fantini, C. Schramm et al., “TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling,” Immunity, vol. 21, pp. 491–501, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Bollrath, T. J. Phesse, V. A. von Burstin et al., “gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis,” Cancer Cell, vol. 15, pp. 91–102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Y. Fu, “STAT3 in immune responses and inflammatory bowel diseases,” Cell Research, vol. 16, pp. 214–219, 2006. View at Google Scholar
  36. L. Klampfer, “The role of signal transducers and activators of transcription in colon cancer,” Frontiers in Bioscience, vol. 13, pp. 2888–2899, 2008. View at Google Scholar
  37. A. Suzuki, T. Hanada, K. Mitsuyama et al., “CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation,” The Journal of Experimental Medicine, vol. 193, pp. 471–481, 2001. View at Google Scholar
  38. Y. Li, C. de Haar, M. Chen et al., “Disease-related expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis,” Gut, vol. 59, pp. 227–235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. R. J. Rigby, J. G. Simmons, C. J. Greenhalgh, W. S. Alexander, and P. K. Lund, “Suppressor of cytokine signaling 3 (SOCS3) limits damage-induced crypt hyper-proliferation and inflammation-associated tumorigenesis in the colon,” Oncogene, vol. 26, pp. 4833–4841, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Becker, M. C. Fantini, and M. F. Neurath, “TGF-beta as a T cell regulator in colitis and colon cancer,” Cytokine & Growth Factor Reviews, vol. 17, pp. 97–106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. R. F. Souza, J. Lei, J. Yin et al., “A transforming growth factor beta 1 receptor type II mutation in ulcerative colitis-associated neoplasms,” Gastroenterology, vol. 112, pp. 40–45, 1997. View at Google Scholar
  42. S. Sangha, M. Yao, and M. M. Wolfe, “Non-steroidal anti-inflammatory drugs and colorectal cancer prevention,” Postgraduate Medical Journal, vol. 81, pp. 223–227, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Lanas and A. Ferrandez, “NSAIDs and the colon,” Current Opinion in Gastroenterology, vol. 25, pp. 44–49, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. R. A. Gupta and R. N. Dubois, “Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2,” Nature Reviews. Cancer, vol. 1, pp. 11–21, 2001. View at Publisher · View at Google Scholar
  45. S. N. Agoff, T. A. Brentnall, D. A. Crispin et al., “The role of cyclooxygenase 2 in ulcerative colitis-associated neoplasia,” The American Journal of Pathology, vol. 157, pp. 737–745, 2000. View at Google Scholar
  46. M. Oshima, J. E. Dinchuk, S. L. Kargman et al., “Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2),” Cell, vol. 87, pp. 803–809, 1996. View at Google Scholar
  47. S. K. Boolbol, A. J. Dannenberg, A. Chadburn et al., “Cyclooxygenase-2 overexpression and tumor formation are blocked by sulindac in a murine model of familial adenomatous polyposis,” Cancer Research, vol. 56, pp. 2556–2560, 1996. View at Google Scholar
  48. D. Wang and R. N. Dubois, “The role of COX-2 in intestinal inflammation and colorectal cancer,” Oncogene, vol. 29, pp. 781–788, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. A. F. Sheibanie, J. H. Yen, T. Khayrullina et al., “The proinflammatory effect of prostaglandin E2 in experimental inflammatory bowel disease is mediated through the IL-23-->IL-17 axis,” Journal of Immunology, vol. 178, pp. 8138–8147, 2007. View at Google Scholar
  50. G. L. Jiang, A. Nieves, W. B. Im, D. W. Old, D. T. Dinh, and L. Wheeler, “The prevention of colitis by E prostanoid receptor 4 agonist through enhancement of epithelium survival and regeneration,” The Journal of Pharmacology and Experimental Therapeutics, vol. 320, pp. 22–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Sheng, J. Shao, J. D. Morrow, R. D. Beauchamp, and R. N. DuBois, “Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells,” Cancer Research, vol. 58, pp. 362–366, 1998. View at Google Scholar
  52. M. Mutoh, K. Watanabe, T. Kitamura et al., “Involvement of prostaglandin E receptor subtype EP(4) in colon carcinogenesis,” Cancer Research, vol. 62, pp. 28–32, 2002. View at Google Scholar
  53. K. Watanabe, T. Kawamori, S. Nakatsugi et al., “Role of the prostaglandin E receptor subtype EP1 in colon carcinogenesis,” Cancer Research, vol. 59, pp. 5093–5096, 1999. View at Google Scholar
  54. D. Wang, H. Wang, J. Brown et al., “CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer,” The Journal of Experimental Medicine, vol. 203, pp. 941–951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Wang, H. Wang, Q. Shi et al., “Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta,” Cancer Cell, vol. 6, pp. 285–295, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Wang and R. N. DuBois, “PPARdelta and PGE2 signaling pathways communicate and connect inflammation to colorectal cancer,” Inflammation and Cell Signaling, vol. 1, 2014. View at Publisher · View at Google Scholar
  57. M. Sarra, F. Pallone, T. T. Macdonald, and G. Monteleone, “IL-23/IL-17 axis in IBD,” Inflammatory Bowel Diseases, vol. 16, pp. 1808–1813, 2010. View at Google Scholar
  58. G. Hundorfean, M. F. Neurath, and J. Mudter, “Functional relevance of T helper 17 (Th17) cells and the IL-17 cytokine family in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 18, pp. 180–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Fujino, A. Andoh, S. Bamba et al., “Increased expression of interleukin 17 in inflammatory bowel disease,” Gut, vol. 52, pp. 65–70, 2003. View at Google Scholar
  60. D. McGovern and F. Powrie, “The IL23 axis plays a key role in the pathogenesis of IBD,” Gut, vol. 56, pp. 1333–1336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. C. O. Elson, Y. Cong, C. T. Weaver et al., “Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice,” Gastroenterology, vol. 132, pp. 2359–2370, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. R. H. Duerr, K. D. Taylor, S. R. Brant et al., “A genome-wide association study identifies IL23R as an inflammatory bowel disease gene,” Science, vol. 314, pp. 1461–1463, 2006. View at Google Scholar
  63. S. I. Grivennikov, K. Wang, D. Mucida et al., “Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth,” Nature, vol. 491, pp. 254–258, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Liu, Y. Duan, X. Cheng et al., “IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma,” Biochemical and Biophysical Research Communications, vol. 407, pp. 348–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. B. Ljujic, G. Radosavljevic, I. Jovanovic et al., “Elevated serum level of IL-23 correlates with expression of VEGF in human colorectal carcinoma,” Archives of Medical Research, vol. 41, pp. 182–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. S. Hyun, D. S. Han, A. R. Lee, C. S. Eun, J. Youn, and H. Y. Kim, “Role of IL-17A in the development of colitis-associated cancer,” Carcinogenesis, vol. 33, pp. 931–936, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. V. De Simone, F. Pallone, G. Monteleone, and C. Stolfi, “Role of TH17 cytokines in the control of colorectal cancer,” Oncoimmunology, vol. 2, article e26617, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Stolfi, A. Rizzo, E. Franze et al., “Involvement of interleukin-21 in the regulation of colitis-associated colon cancer,” The Journal of Experimental Medicine, vol. 208, pp. 2279–2290, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Jiang, H. Wang, L. Deng et al., “IL-22 is related to development of human colon cancer by activation of STAT3,” BMC Cancer, vol. 13, p. 59, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Huber, N. Gagliani, L. A. Zenewicz et al., “IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine,” Nature, vol. 491, pp. 259–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. Z. Tong, X. O. Yang, H. Yan et al., “A protective role by interleukin-17F in colon tumorigenesis,” PLoS One, vol. 7, article e34959, 2012. View at Publisher · View at Google Scholar · View at Scopus