Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease

Inflammatory Bowel Diseases

Volumn 16, Issue 8, 2010, Pages 1411-1420

  O'Connor, Pamela M ^a   Lapointe, Tamia K ^a   Beck, Paul L ^b   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Colorectal cancer; Crohn's disease; Inflammation; Nuclear factor B; Ulcerative colitis

Indexed keywords

CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; NITROGEN; PROSTAGLANDIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; APOPTOSIS; BASIC RESEARCH; CANCER INVASION; CANCER RISK; CARCINOGENESIS; CELL MIGRATION; CHRONIC DISEASE; CHRONIC INFLAMMATION; CLINICAL ASSESSMENT; CLINICAL FEATURE; CYTOKINE PRODUCTION; ENTERITIS; ENVIRONMENT; EPITHELIUM CELL; HUMAN; IMMUNITY; INFLAMMATORY DISEASE; INTESTINE CANCER; MEDIATOR; METASTASIS; MIGRATION; MUTAGENESIS; OXIDATIVE STRESS; PRIORITY JOURNAL; RELAPSE; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL; TUMOR CELL; TUMOR GROWTH; TUMOR NECROSIS; TUMOR PROMOTION; ULCERATIVE COLITIS;

ANIMALS; HUMANS; INFLAMMATION MEDIATORS; INFLAMMATORY BOWEL DISEASES; INTESTINAL NEOPLASMS; MICE; MUTATION; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; RISK;

EID: 77955279767     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21217     Document Type: Review

References (101)

1. Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer. 2001;91:854-862. (Pubitemid 32173312)
2. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48:526-535. (Pubitemid 32234798)
3. Jess T, Loftus EV Jr, Velayos FS, et al. Risk of intestinal cancer in inflammatory bowel disease: a population-based study from Olmsted County, Minnesota. Gastroenterology. 2006;130:1039-1046.
4. Rutter MD, Saunders BP, Wilkinson KH, et al. Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterology. 2006;130:1030-1038.
5. Sachar DB. Cancer in Crohn's disease: dispelling the myths. Gut. 1994;35:1507-1508. (Pubitemid 24339242)
6. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004;126:451-459. (Pubitemid 38182302)
7. Ekbom A, Helmick C, Zack M, et al. The epidemiology of inflammatory bowel disease: a large, population-based study in Sweden. Gastroenterology. 1991;100:350-358.
8. Cheng Y, Desreumaux P. 5-Aminosalicylic acid is an attractive candidate agent for chemoprevention of colon cancer in patients with inflammatory bowel disease. World J Gastroenterol. 2005;11:309-314. (Pubitemid 40125228)
9. Guadagni F, Ferroni P, Palmirotta R, et al. Non-steroidal anti-inflammatory drugs in cancer prevention and therapy. Anticancer Res. 2007;27:3147-3162. (Pubitemid 47607538)
10. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357:539-545.
11. Eslick GD, Lim LL, Byles JE, et al. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol. 1999;94:2373-2379. (Pubitemid 29420659)
12. Huang JQ, Sridhar S, Chen Y, et al. Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology. 1998;114:1169-1179. (Pubitemid 28243902)
13. Perz JF, Armstrong GL, Farrington LA, et al. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol. 2006;45:529-538.
14. Fireman Z, Grossman A, Lilos P, et al. Intestinal cancer in patients with Crohn's disease. A population study in central Israel. Scand J Gastroenterol. 1989;24:346-350. (Pubitemid 19110894)
15. Kvist N, Jacobsen O, Norgaard P, et al. Malignancy in Crohn's disease. Scand J Gastroenterol. 1986;21:82-86.
16. Gollop JH, Phillips SF, Melton LJ 3rd, et al. Epidemiologic aspects of Crohn's disease: a population based study in Olmsted County, Minnesota, 1943-1982. Gut. 1988;29:49-56.
17. Gyde SN, Prior P, Macartney JC, et al. Malignancy in Crohn's disease. Gut. 1980;21:1024-1029.
18. Freeman HJ. Colorectal cancer complicating Crohn's disease. Can J Gastroenterol. 2001;15:231-236. (Pubitemid 32496345)
19. Canavan C, Abrams KR, Mayberry J. Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn's disease. Aliment Pharmacol Ther. 2006;23:1097-1104. (Pubitemid 43779348)
20. Nuako KW, Ahlquist DA, Mahoney DW, et al. Familial predisposition for colorectal cancer in chronic ulcerative colitis: a case-control study. Gastroenterology. 1998;115:1079-1083. (Pubitemid 28485597)
21. Askling J, Dickman PW, Karlen P, et al. Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology. 2001;120:1356-1362. (Pubitemid 32322309)
22. Fuchs CS, Giovannucci EL, Colditz GA, et al. A prospective study of family history and the risk of colorectal cancer. N Engl J Med. 1994;331:1669-1674. (Pubitemid 24373618)
23. Shetty K, Rybicki L, Brzezinski A, et al. The risk for cancer or dysplasia in ulcerative colitis patients with primary sclerosing cholangitis. Am J Gastroenterol. 1999;94:1643-1649. (Pubitemid 29260459)
24. van Staa TP, Card T, Logan RF, et al. 5-Aminosalicylate use and colorectal cancer risk in inflammatory bowel disease: a large epidemiological study. Gut. 2005;54:1573-1578. (Pubitemid 41531774)
25. Velayos FS, Terdiman JP, Walsh JM. Effect of 5-aminosalicylate use on colorectal cancer and dysplasia risk: a systematic review and metaanalysis of observational studies. Am J Gastroenterol. 2005;100:1345-1353.
26. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 2005;5:749-759. (Pubitemid 41400849)
27. Cooper HS, Murthy S, Kido K, et al. Dysplasia and cancer in the dextran sulfate sodium mouse colitis model. Relevance to colitis-associated neoplasia in the human: a study of histopathology, B-catenin and p53 expression and the role of inflammation. Carcinogenesis. 2000;21:757-768.
28. Shattuck-Brandt RL, Varilek GW, Radhika A, et al. Cyclooxygenase 2 expression is increased in the stroma of colon carcinomas from IL-10(-/-) mice. Gastroenterology. 2000;118:337-345. (Pubitemid 30067507)
29. Erdman SE, Poutahidis T, Tomczak M, et al. CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol. 2003;162:691-702. (Pubitemid 36267876)
30. Ikeda I, Tomimoto A, Wada K, et al. 5-Aminosalicylic acid given in the remission stage of colitis suppresses colitis-associated cancer in a mouse colitis model. Clin Cancer Res. 2007;13:6527-6531. (Pubitemid 350075044)
31. Fuss IJ, Neurath M, Boirivant M, et al. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol. 1996;157:1261-1270. (Pubitemid 126449643)
32. Fuss IJ, Heller F, Boirivant M, et al. Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest. 2004;113:1490-1497. (Pubitemid 39071705)
33. Heller F, Florian P, Bojarski C, et al. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology. 2005;129:550-564. (Pubitemid 41096643)
34. Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet. 2007;369:1627-1640. (Pubitemid 46722636)
35. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221-227.
36. Rogler G, Brand K, Vogl D, et al. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology. 1998;115:357-369. (Pubitemid 28363428)
37. Lind DS, Hochwald SN, Malaty J, et al. Nuclear factor-kappa B is upregulated in colorectal cancer. Surgery. 2001;130:363-369. (Pubitemid 32721692)
38. Yu HG, Yu LL, Yang Y, et al. Increased expression of RelA/nuclear factor-kappa B protein correlates with colorectal tumorigenesis. Oncology. 2003;65:37-45. (Pubitemid 36829089)
39. Greten FR, Eckmann L, Greten TF, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118:285-296. (Pubitemid 39061110)
40. Itzkowitz SH. Molecular biology of dysplasia and cancer in inflammatory bowel disease. Gastroenterol Clin North Am. 2006;35:553-571. (Pubitemid 44307575)
41. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4:71-78.
42. Hussain SP, Amstad P, Raja K, et al. Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease. Cancer Res. 2000;60:3333-3337. (Pubitemid 30482141)
43. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer. 2003;3:276-285.
44. Singer, II, Kawka DW, Scott S, et al. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology. 1996;111:871-885. (Pubitemid 26327590)
45. Souici AC, Mirkovitch J, Hausel P, et al. Transition mutation in codon 248 of the p53 tumor suppressor gene induced by reactive oxygen species and a nitric oxide-releasing compound. Carcinogenesis. 2000;21:281-287. (Pubitemid 30098714)
46. Ambs S, Bennett WP, Merriam W, et al. Relationship between p53 mutations and inducible nitric oxide synthase expression in human colorectal cancer. J Natl Cancer Inst. 1999;91:86-88. (Pubitemid 29042448)
47. Rao CV, Indranie C, Simi B, et al. Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase-2 inhibitor. Cancer Res. 2002;62:165-170. (Pubitemid 34074001)
48. Zhang R, Ma A, Urbanski SJ, et al. Induction of inducible nitric oxide synthase: a protective mechanism in colitis-induced adenocarcinoma. Carcinogenesis. 2007;28:1122-1130. (Pubitemid 47072200)
49. Seidelin JB, Nielsen OH. Continuous cytokine exposure of colonic epithelial cells induces DNA damage. Eur J Gastroenterol Hepatol. 2005;17:363-369. (Pubitemid 40411225)
50. Yan B, Wang H, Rabbani ZN, et al. Tumor necrosis factor-alpha is a potent endogenous mutagen that promotes cellular transformation. Cancer Res. 2006;66:11565-11570. (Pubitemid 46094163)
51. Popivanova BK, Kitamura K, Wu Y, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest. 2008;118:560-570. (Pubitemid 351206546)
52. Hudson JD, Shoaibi MA, Maestro R, et al. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med. 1999;190:1375-1382.
53. Ohkawara T, Nishihira J, Takeda H, et al. Amelioration of dextran sulfate sodium-induced colitis by anti-macrophage migration inhibitory factor antibody in mice. Gastroenterology. 2002;123:256-270. (Pubitemid 34747546)
54. Fei BY, Lv HX, Yang JM, et al. Association of MIF-173 gene polymorphism with inflammatory bowel disease in Chinese Han population. Cytokine. 2008;41:44-47.
55. Griga T, Wilkens C, Wirkus N, et al. A polymorphism in the macrophage migration inhibitory factor gene is involved in the genetic predisposition of Crohn's disease and associated with cumulative steroid doses. Hepatogastroenterology. 2007;54:784-786. (Pubitemid 46903723)
56. Murch SH, Braegger CP, Walker-Smith JA, et al. Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut. 1993;34:1705-1709.
57. Murch SH, Lamkin VA, Savage MO, et al. Serum concentrations of tumour necrosis factor alpha in childhood chronic inflammatory bowel disease. Gut. 1991;32:913-917.
58. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353:2462-2476. (Pubitemid 41770166)
59. Scott KA, Moore RJ, Arnott CH, et al. An anti-tumor necrosis factor-alpha antibody inhibits the development of experimental skin tumors. Mol Cancer Ther. 2003;2:445-451.
60. Moore RJ, Owens DM, Stamp G, et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med. 1999;5:828-831. (Pubitemid 29318619)
61. Poutahidis T, Haigis KM, Rao VP, et al. Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis. 2007;28:2614-2623. (Pubitemid 350238965)
62. Mehrad B, Keane MP, Strieter RM. Chemokines as mediators of angiogenesis. Thromb Haemost. 2007;97:755-762.
63. Rustgi AK. The genetics of hereditary colon cancer. Genes Dev. 2007;21:2525-2538.
64. Bongartz T, Sutton AJ, Sweeting MJ, et al. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295:2275-2285. (Pubitemid 43736578)
65. Rutgeerts P, Van Assche G, Vermeire S. Optimizing anti-TNF treatment in inflammatory bowel disease. Gastroenterology. 2004;126:1593-1610. (Pubitemid 38649876)
66. Mitsuyama K, Sata M, Rose-John S. Interleukin-6 trans-signaling in inflammatory bowel disease. Cytokine Growth Factor Rev. 2006;17:451-461. (Pubitemid 44793118)
67. Schneider MR, Hoeflich A, Fischer JR, et al. Interleukin-6 stimulates clonogenic growth of primary and metastatic human colon carcinoma cells. Cancer Lett. 2000;151:31-38. (Pubitemid 30155582)
68. Chung YC, Chang YF. Serum interleukin-6 levels reflect the disease status of colorectal cancer. J Surg Oncol. 2003;83:222-226. (Pubitemid 36936007)
69. Becker C, Fantini MC, Schramm C, et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity. 2004;21:491-501. (Pubitemid 39370505)
70. Grivennikov S, Karin E, Terzic J, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell. 2009;15:103-113.
71. Blanchot-Jossic F, Jarry A, Masson D, et al. Up-regulated expression of ADAM17 in human colon carcinoma: co-expression with EGFR in neoplastic and endothelial cells. J Pathol. 2005;207:156-163. (Pubitemid 41404146)
72. Landi S, Moreno V, Gioia-Patricola L, et al. Association of common polymorphisms in inflammatory genes interleukin (IL)6, IL8, tumor necrosis factor alpha, NFKB1, and peroxisome proliferator-activated receptor gamma with colorectal cancer. Cancer Res. 2003;63:3560-3566.
73. Heinrich P, Behrmann I, Haan S, et al. Principles of interleukin (IL)-6 type cytokine signalling and its regulation. Biochem J. 2003;374:1-20. (Pubitemid 37046923)
74. Starr R, Willson TA, Viney EM, et al. A family of cytokine-inducible inhibitors of signalling. Nature. 1997;387:917-921.
75. Rigby R, Simmons J, Greenhalgh C, et al. Suppressor of cytokine signalign 3 (SOCS3) limits damage-induced crypt hyper-proliferation and inflammation-associated tumorigenesis in the colon. Oncogene. 2007;26:4833-4841. (Pubitemid 47093177)
76. He B, You L, Uematsu K, et al. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci U S A. 2003;100:14133-14138. (Pubitemid 37499203)
77. Oshimo Y, Kuraoka K, Nakayama H, et al. Epigenetic inactivation of SOCS-1 by CpG island hypermethylation in human gastric carcinoma. Int J Cancer. 2004;112:1003-1009. (Pubitemid 39507006)
78. Babyatsky MW, Rossiter G, Podolsky DK. Expression of transforming growth factors alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology. 1996;110:975-984. (Pubitemid 26113734)
79. Becker C, Fantini MC, Neurath MF. TGF-beta as a T cell regulator in colitis and colon cancer. Cytokine Growth Factor Rev. 2006;17:97-106. (Pubitemid 43117519)
80. Sodir NM, Chen X, Park R, et al. Smad3 deficiency promotes tumorigenesis in the distal colon of ApcMin/+ mice. Cancer Res. 2006;66:8430-8438. (Pubitemid 44449154)
81. Jobin C, Morteau O, Han DS, et al. Specific NF-kappaB blockade selectively inhibits tumour necrosis factor-alpha-induced COX-2 but not constitutive COX-1 gene expression in HT-29 cells. Immunology. 1998;95:537-543. (Pubitemid 28559144)
82. Trifan OC, Hla T. Cyclooxygenase-2 modulates cellular growth and promotes tumorigenesis. J Cell Mol Med. 2003;7:207-222. (Pubitemid 37372041)
83. Shao J, Lee SB, Guo H, et al. Prostaglandin E2 stimulates the growth of colon cancer cells via induction of amphiregulin. Cancer Res. 2003;63:5218-5223. (Pubitemid 37139831)
84. Fukata M, Chen A, Vamadevan AS, et al. Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology. 2007;133:1869-1881.
85. Fukata M, Chen A, Klepper A, et al. Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: role in proliferation and apoptosis in the intestine. Gastroenterology. 2006;131:862-877. (Pubitemid 44316821)
86. Agoff SN, Brentnall TA, Crispin DA, et al. The role of cyclooxygenase 2 in ulcerative colitis-associated neoplasia. Am J Pathol. 2000;157:737-745.
87. Sangha S, Yao M, Wolfe MM. Non-steroidal anti-inflammatory drugs and colorectal cancer prevention. Postgrad Med J. 2005;81:223-227. (Pubitemid 40546616)
88. Inoue T, Hirata I, Murano M. Effects of nimesulide, a cyclooxygenase-2 selective inhibitor, on colitis induced tumors. Inflammopharmacology. 2008;16:36-39. (Pubitemid 351225997)
89. Mukawa K, Fujii S, Tominaga K, et al. Inhibitory effects of the cyclooxygenase-2 inhibitor, etodolac, on colitis-associated tumorigenesis in p53-deficient mice treated with dextran sulfate sodium. Oncol Rep. 2008;19:393-399. (Pubitemid 351176099)
90. Alters SE, Gadea JR, Holm B, et al. IL-13 can substitute for IL-4 in the generation of dendritic cells for the induction of cytotoxic T lymphocytes and gene therapy. J Immunother. 1999;22:229-236. (Pubitemid 29226983)
91. Terabe M, Matsui S, Noben-Trauth N, et al. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway. Nat Immunol. 2000;1:515-520.
92. Menetrier-Caux C, Montmain G, Dieu MC, et al. Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood. 1998;92:4778-4791. (Pubitemid 29005881)
93. Sun WH, Kreisle RA, Phillips AW, et al. In vivo and in vitro characteristics of interleukin 6-transfected B16 melanoma cells. Cancer Res. 1992;52:5412-5415.
94. Salazar-Onfray F, Lopez MN, Mendoza-Naranjo A. Paradoxical effects of cytokines in tumor immune surveillance and tumor immune escape. Cytokine Growth Factor Rev. 2007;18:171-182. (Pubitemid 46401435)
95. Bosch FX, Manos MM, Munoz N, et al. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International Biological Study on Cervical Cancer (IBSCC) Study Group. J Natl Cancer Inst. 1995;87:796-802.
96. Ness RB, Cottreau C. Possible role of ovarian epithelial inflammation in ovarian cancer. J Natl Cancer Inst. 1999;91:1459-1467. (Pubitemid 29424550)
97. Parazzini F, La Vecchia C, Negri E, et al. Pelvic inflammatory disease and risk of ovarian cancer. Cancer Epidemiol Biomarkers Prev. 1996;5:667-669. (Pubitemid 26294976)
98. Hamilton SR, Smith RR, Cameron JL. Prevalence and characteristics of Barrett esophagus in patients with adenocarcinoma of the esophagus or esophagogastric junction. Hum Pathol. 1988;19:942-948.
99. Winters C Jr, Spurling TJ, Chobanian SJ, et al. Barrett's esophagus. A prevalent, occult complication of gastroesophageal reflux disease. Gastroenterology. 1987;92:118-124.
100. Mossman BT, Kamp DW, Weitzman SA. Mechanisms of carcinogenesis and clinical features of asbestos-associated cancers. Cancer Invest. 1996;14:466-480. (Pubitemid 26338211)
101. Vainio H, Boffetta P. Mechanisms of the combined effect of asbestos and smoking in the etiology of lung cancer. Scand J Work Environ Health. 1994;20:235-242. (Pubitemid 24291305)