Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development

European Journal of Gastroenterology and Hepatology

Volumn 25, Issue 3, 2013, Pages 271-281

  Azer, Samy A ^a  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

biomarkers; carcinogenesis; colorectal cancer in IBD; early detection; inflammatory bowel disease; molecular pathways; pathogenesis

Indexed keywords

BETA CATENIN; CALGRANULIN; CHEMOKINE; CONJUGATED LINOLEIC ACID; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; PATTERN RECOGNITION RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E2; PROTEIN MLH1; PROTEIN P53; RANTES; REACTIVE OXYGEN METABOLITE; SIALOGLYCOPROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VITAMIN D RECEPTOR; VSL3;

CANCER GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; CHROMOSOMAL INSTABILITY; COLITIS; COLON BIOPSY; COLON CARCINOGENESIS; COLON MUCOSA; COLORECTAL CANCER; CPG ISLAND; DISEASE ASSOCIATION; DISEASE DURATION; DNA METHYLATION; EARLY DIAGNOSIS; ENTERITIS; FAMILY HISTORY; GENE SILENCING; HIGH RISK PATIENT; HUMAN; IMMUNOREGULATION; INTESTINE ENDOSCOPY; INTESTINE EPITHELIUM; INTESTINE FLORA; META ANALYSIS (TOPIC); MICROSATELLITE INSTABILITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PLOIDY; PREDICTIVE VALIDITY; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; RISK FACTOR; SENSITIVITY AND SPECIFICITY; STOMACH MUCOSA; TH17 CELL; TUMOR SUPPRESSOR GENE; ULCERATIVE COLITIS; WNT SIGNALING PATHWAY;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; EARLY DETECTION OF CANCER; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATION MEDIATORS; INFLAMMATORY BOWEL DISEASES; RISK FACTORS; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR MARKERS, BIOLOGICAL;

EID: 84873412849     PISSN: 0954691X     EISSN: 14735687     Source Type: Journal    
DOI: 10.1097/MEG.0b013e32835b5803     Document Type: Review

References (93)

1. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 1990; 323:1228-1233
2. Gillen CD, Waimsley RS, Prior P, Andrews HA, Allan RN. Ulcerative colitis and Crohn's disease: A comparison of the colorectal cancer risk in extensive colitis. Gut 1994; 35:1590-1592
3. Choi PM, Zelig MP. Similarity of colorectal cancer in Crohn's disease and ulcerative colitis: Implications for carcinogenesis and prevention. Gut 1994; 35:950-954
4. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J Gastroenterol 2008; 14:378-389
5. Herszenvi L, Miheller P, Tulassay Z. Carcinogenesis in inflammatory bowel disease. Dig Dis 2007; 25:267-269
6. Cairns SR, Scholefield JH, Steele RJ, Dunlop MG, Thomas HJ, Evans GD, et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 2010; 59:666-689
7. Eaden JA, Mayberry JF. Guidelines for screening and surveillance of asymptomatic colorectal cancer in patients with inflammatory bowel disease. Gut 2002; 51:V10-V12
8. Farraye FA, Odze RD, Eaden J, Itzkowitz SH. AGA medical position statement on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology 2010; 138:738-745
9. Baars JE, Kuipers EJ, van Haastert M, Nicolai? JJ, Poen AC, van derWoude CJ. Age at diagnosis of inflammatory bowel disease influences early development of colorectal cancer in inflammatory bowel disease patients: A nationwide, long-Term survey. J Gastroenterol 2012 [Epub ahead of print
10. Collins PD, Mpofu C,Watson AJ, Rhodes JM. Strategies for detecting colon cancer and/or dysplasia in patients with inflammatory bowel disease. Cochrane Database Syst Rev 2006; Issue 2:CD000279
11. Itzkowitz S. Colon carcinogenesis in inflammatory bowel disease: Applying molecular genetics to clinical practice. J Clin Gastroenterol 2003; 36:S70-S74
12. Guagnozzi D, Lucendo AJ. Colorectal cancer surveillance in patients with inflammatory bowel disease: What is new? World J Gastrointest Endosc 2012; 4:108-116
13. Chan EP, Lichtenstein GR. Chemoprevention: Risk reduction with medical therapy of inflammatory bowel disease. Gastroenterol Clin North Am 2006; 35:675-712
14. Farhadi A, Banan A, Fields J, Keshavarzian A. Intestinal barrier: An interface between health and disease. J Gastroenterol Hepatol 2003; 18:479-497
15. Keshavarzian A, Morgan G, Sedghi S, Gordon JH, Doria M. Role of reactive oxygen metabolites in experimental colitis. Gut 1990; 31:786-790
16. Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A. Oxidantinduced intestinal barrier disruption and its prevention by growth factors in a human colonic cell line: Role of the microtubule cytoskeleton. Free Radic Biol Med 2000; 28:727-738
17. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 2003; 171:6164-6172
18. Itzkowitz SH. Molecular biology of dysplasia and cancer in inflammatory bowel disease. Gastroenterol Clin North Am 2006; 35:553-571
19. Klampfer L. Cytokines, inflammation and colon cancer. Curr Cancer Drug Targets 2011; 11:451-464
20. Gerrits MM, Chen M, Theeuwes M, van Dekken H, Sikkema M, Steyerberg EW, et al. Biomarker-based prediction of inflammatory bowel disease-related colorectal cancer: A case-control study. Cell Oncol (Dordr) 2011; 34:107-117
21. Issa J-P. The epigenrtics of colorectal cancer. Ann N Y Acad Sci 2006; 910:140-155
22. Toyota M, Ho C, Ahuja N, Jair KW, Li Q, Ohe-Toyota M, et al. Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res 1999; 59:2307-2312
23. Grady WM. Epigenetic events in the colorectum and in colon cancer. Biochem Soc Trans 2005; 33 (Pt 4):684-688
24. Reeves HL, Narla G, Ogunbiyi O, Haq AI, Katz A, Benzeno S, et al. Kruppellike factor 6 (KLF6) is a tumor-suppressor gene frequently inactivated in colorectal cancer. Gastroenterology 2004; 126:1090-1103
25. Fleisher AS, Esteller M, Harpaz N, Leytin A, Rashid A, Xu Y, et al. Microsatellite instability in inflammatory bowel disease-Associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH11. Cancer Res 2000; 60:4864-4868
26. Vietri MT, Riegler G, De Paola M, Simeone S, Boggia M, Improta A, et al. I219V polymorphism in hMLH1 gene in patients affected with ulcerative colitis. Genet Test Mol Biomarkers 2009; 13:193-197
27. Dhir M, Montgomery EA, Glockner SC, Schuebel KE, Hooker CM, Herman JG, et al. Epigenetic regulation of WNT signaling pathway genes in inflammatory bowel disease (IBD) associated neoplasia. J Gastrointest Surg 2008; 12:1745-1753
28. Smalley WE, De Bois RN. Colorectal cancer and nonsteroidal anti-inflammatory drugs. Adv Pharmacol 1997; 39:1-20
29. Wang S, Liu Z, Wang L, Zhang X. NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 2009; 6:327-334
30. Loch T, Michalski B, Mazurek U, Graniczka M. Vascular endothelial growth factor (VEGF) and its role in neoplastic processes. Postepy Hig Med Dosw 2001; 55:257-274
31. Gupta RA, Du Bois RN. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer 2001; 1:11-21
32. Marnett IJ, De Bois RN. COX-2: Target for colon cancer prevention. Annu Rev Pharmacol Toxicol 2002; 42:55-80
33. Chan AT, Ogino S, Fuchs CS. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med 2007; 356:2131-2142
34. Agoff SN, Brentnall TA, Crispin DA, Taylor SL, Raaka S, Haggitt RC, et al. The role of cyclooxygenase 2 in ulcerative colitis-Associated neoplasia. Am J Pathol 2000; 157:737-745
35. Singer II, Kawka DW, Schloemann S, Tessner T, Riehl T, Stenson WF. Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 1998; 115:297-306
36. Shattuck-Brandt RL, Varilek GW, Radhika A, Yang F,Washington MK, DuBois RN. Cyclooxygenase 2 expression is increased in the stroma of colon carcinomas from IL-10(- / -) mice. Gastroenterology 2000; 118:337-345
37. Ungaro R, Fukata M, Hsu D, Hernandez Y, Breglio K, Chen A, et al. A novel Toll-Like receptor 4 antagonist antibody ameliorates inflammation but impairs mucosal healing in murine colitis. Am J Physiol Gastrointest Liver Physiol 2009; 296:G1167-G1179
38. Wang D,Wang H, Brown J, Daikoku T, NingW, Shi Q, et al. CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer. J Exp Med 2006; 203:941-951
39. Castellone MD, Teramoto H, Gutkind JS. Cyclooxygenase-2 and colorectal cancer chemoprevention: The beta-catenin connection. Cancer Res 2006; 66:11085-11088
40. Kishimoto T. Interleukin-6 from basic science to medicine-40 years in immunology. Annu Rev Immunol 2005; 23:1-21
41. Atreya R, Neurath MF. Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin Rev Allergy Immunol 2005; 28:187-196
42. Ishihara K, Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002; 13:357-368
43. Szkaradkiewicz A, Marciniak R, Chudzicka-Strugała I,Wasilewska A, Drews M, Majewski P, et al. Proinflammatory cytokines and IL-10 in inflammatory bowel disease and colorectal cancer patients. Arch Immunol Ther Exp (Warsz) 2009; 57:291-294
44. Li Y, de Haar C, Chen M, Deuring J, Gerrits MM, Smits R, et al. Diseaserelated expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut 2010; 59:227-235
45. Sarra M, Pallone F, Macdonald TT, Monteleone G. IL-23/IL-17 axis in IBD. Inflamm Bowel Dis 2010; 16:1808-1813
46. Ljujic B, Radosavljevic G, Jovanovic I, Pavlovic S, Zdravkovic N, Milovanovic M, et al. Elevated serum level of IL-23 correlates with expression of VEGF in human colorectal carcinoma. Arch Med Res 2010; 41:182-189
47. Adamo V, Franchina T, Minciullo P, Pace E, Colonese F, Ricciardi G, et al. Role of interleukin-23 circulating levels increase in resected colorectal cancer before and after chemotherapy: Preliminary data and future perspectives. J Cell Physiol 2011; 226:3032-3034
48. Fan W, Maoqing W, Wangyang C, Fulan H, Dandan L, Jiaojiao R, et al. Relationship between the polymorphism of tumor necrosis factor-A-308 G> A and susceptibility to inflammatory bowel diseases and colorectal cancer: A meta-Analysis. Eur J Hum Genet 2011; 19:432-437
49. Eckmann L. Animal models of inflammatory bowel disease: Lessons from enteric infections. Ann N Y Acad Sci 2006; 1072:28-38
50. Lee J, Mo JH, Katakura K, Alkalay I, Rucker AN, Liu YT, et al. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 2006; 8:1327-1336
51. Bene L, Falus A, Baffy N, Fulop AK. Cellular and molecular mechanisms in the two major forms of inflammatory bowel disease. Pathol Oncol Res 2011; 17:463-472
52. Bazan JF, Bacon KB, Hardiman G, Wang W, Soo K, Rossi D, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997; 385:640-644
53. Ottaiano A, Franco R, Aiello Talamanca A, Liguori G, Tatangelo F, Delrio P, et al. Overexpression of both CXC chemokine receptor 4 and vascular endothelial growth factor proteins predicts early distant relapse in stage II-III colorectal cancer patients. Clin Cancer Res 2006; 12:2795-2803
54. Kim J, Takeuchi H, Lam ST, Turner RR, Wang HJ, Kuo C, et al. Chemokine receptor CXCR4 expression in colorectal cancer patients increases the risk for recurrence and for poor survival. J Clin Oncol 2005; 23:2744-2753
55. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-Associated cancer. Cell 2004; 118:285-296
56. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006; 441:431-436
57. Dijkstra G, Moshage H, Jansen PL. Blockade of NF-kappaB activation and donation of nitric oxide: New treatment options in inflammatory bowel diseasëScand J Gastroenterol SUPPL2002; 37:37-41
58. Schottelius AJ, Cytokines Dinter H. NF-kappaB, microenvironment, intestinal inflammation and cancer. Cancer Treat Res 2006; 130:67-87
59. Souza RF, Lei J, Yin J, Appel R, Zou TT, Zhou X, et al. A transforming growth factor beta 1 receptor type II mutation in ulcerative colitis-Associated neoplasms. Gastroenterology 1997; 112:40-45
60. Hahm KB, Lee KM, Kim YB, Hong WS, Lee WH, Han SU, et al. Conditional loss of TGF-beta signalling leads to increased susceptibility to gastrointestinal carcinogenesis in mice. Aliment Pharmacol Ther 2002; 16 (SUPPL2):115-127
61. Afrem G, Mogoanta SS, Secureanu FA, Olaru A, Neamţu C, Totolici BD, et al. Study of molecular prognostic factors Bcl-2 and EGFR in rectal mucinous carcinomas. Rom J Morphol Embryol 2012; 53:277-285
62. Sethi K, Sarkar S, Das S, Rajput S, Mazumder A, Roy B, et al. Expressions of CK-19, NF-kappaB, E-cadherin, beta-catenin and EGFR as diagnostic and prognostic markers by immunohistochemical analysis in thyroid carcinoma. J Exp Ther Oncol 2011; 9:187-199
63. Noske A, Schwabe M, Weichert W, Darb-Esfahani S, Buckendahl AC, Sehouli J, et al. An intracellular targeted antibody detects EGFR as an independent prognostic factor in ovarian carcinomas. BMC Cancer 2011; 11:294
64. Wickbom G, Cha SO, O'Leary P. Experimentally induced ileal ulcers in rats. Scand J Gastroenterol 1988; 23:808
65. Trzcinski R, Bry M, Krajewska W, Kulig M, Dzyiki A. ErbB-1 expression in experimental model of inflammatory bowel disease in rats. Acta Chir Iugosl 2004; 51:85-89
66. Alexander RJ, Panja A, Kaplan-Liss E, Mayer L, Raicht RF. Expression of growth factor receptor-Encoded mRNA by colonic epithelial cells is altered in inflammatory bowel disease. Dig Dis Sci 1995; 40:485-494
67. Yan F, John SK, Wilson G, Jones DS, Washington MK, Polk DB. Kinase suppressor of Ras-1 protects intestinal epithelium from cytokine-mediated apoptosis during inflammation. J Clin Invest 2004; 114:1272-1280
68. Kolesnick R, Xing HR. Inflammatory bowel disease reveals the kinase activity of KSR1. J Clin Invest 2004; 114:1233-1237
69. Goettel JA, Scott Algood HM, Olivares-Villago'mez D, Washington MK, Chaturvedi R, Wilson KT, et al. KSR1 protects from interleukin-10 deficiency-induced colitis in mice by suppressing T-Lymphocyte interferon-g production. Gastroenterology 2011; 140:265-274
70. Campbell MJ, Adorini L. The vitamin D receptor as a therapeutic target. Expert Opin Ther Targets 2006; 10:735-748
71. Jahnsen J, Falch JA, Mowinckel P, Aadland E. Vitamin D status, parathyroid hormone and bone mineral density in patients with inflammatory bowel disease. Scand J Gastroenterol 2002; 37:192-199
72. Cross HS, Nittke T, Kallay E. Colonic vitamin D metabolism: Implications for the pathogenesis of inflammatory bowel disease and colorectal cancer. Mol Cell Endocrinol 2011; 347:70-79
73. Cantorna MT, Munsick C, Bemiss C, Mahon BD. 1,25-Dihydroxycholecalciferol prevents an ameliorates symptoms of experimental murine inflammatory bowel disease. J Nutr 2000; 130:2648-2652
74. Froicu M, Weaver V, Wynn TA, McDowell MA, Welsh JE, Cantorna MT. A crucial role for the vitamin D receptor in experimental inflammatory bowel diseases. Mol Endocrinol 2003; 17:2386-2392
75. Pá lmer HG, González-Sancho JM, Espada J, Berciano MT, Puig I, Baulida J, et al. Vitamin D(3) promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. J Cell Biol 2001; 154:369-387
76. Larriba MJ, Ordó ñ ez-Mora'n P, Chicote I, Marti'n-Ferna'ndez G, Puig I, Muñ oz A, Pa'lmer HG. Vitamin D receptor deficiency enhancesWnt/b-catenin signaling and tumor burden in colon cancer. PLoS One 2011; 6:e23524
77. Murillo G, Nagpal V, Tiwari N, Benya RV, Mehta RG. Actions of vitamin D are mediated by the TLR4 pathway in inflammation-induced colon cancer. J Steroid Biochem Mol Biol 2010; 121:403-407
78. Banan A, Zhang LJ, Shaikh M, Fields JZ, Farhadi A, Keshavarzian A. Novel effect of NF-kappaB activation: Carbonylation and nitration injury to cytoskeleton and disruption of monolayer barrier in intestinal epithelium. Am J Physiol Cell Physiol 2004; 287:C1139-C1151
79. Banan A, Fields JZ, Zhang Y, Keshavarzian A. Key role of PKC and Ca2+ in EGF protection of microtubules and intestinal barrier against oxidants. Am J Physiol Gastrointest Liver Physiol 2001; 280:G828-G843
80. Haller D, Jobin C. Interaction between resident luminal bacteria and the host: Can a healthy relationship turn sour? J Pediatr Gastroenterol Nutr 2004; 38:123-136
81. Berg DJ, Davidson N, Kühn R, Müller W, Menon S, Holland G, et al. Enterocolitis and colon cancer in interleukin-10-Deficient mice are associated with aberrant cytokine production and CD4(+) TH1-Like responses. J Clin Invest 1996; 98:1010-1020
82. Kanneganti TD, Lamkanfi M, Nunez G. Intracellular NOD-Like receptors in host defense and disease. Immunity 2007; 27:549-559
83. Uronis JM, Mü hlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. Modulation of the intestinal microbiota alters colitis-Associated colorectal cancer susceptibility. PLoS One 2009; 4:e6026
84. Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Hontecillas R. Immunoregulatory mechanisms underlying prevention of colitis-Associated colorectal cancer by probiotic bacteria. PLoS One 2012; 7:e34676
85. von Roon AC, Karamountzos L, Purkayastha S, Reese GE, Darzi AW, Teare JP, et al. Diagnostic precision of fecal calprotectin for inflammatory bowel disease and colorectal malignancy. Am J Gastroenterol 2007; 102:803-813
86. Osborn NK, Ahlquist DA. Stool screening for colorectal cancer: Molecular approaches. Gastroenterology 2005; 128:192-206
87. Azuara D, Rodriguez-Moranta F, de Oca J, Sanjuan X, Guardiola J, Lobaton T, et al. Novel methylation panel for the early detection of neoplasia in highrisk ulcerative colitis and Crohn's colitis patients. Inflamm Bowel Dis 2012 . doi: 10.1002/ibd.22994
88. Laurent C, Svrcek M, Flejou JF, Chenard MP, Duclos B, Freund JN, Reimund JM. Immunohistochemical expression of CDX2, b-catenin, and TP53 in inflammatory bowel disease-Associated colorectal cancer. Inflamm Bowel Dis 2011; 17:232-240
89. Claessen MM, Schipper ME, Oldenburg B, Siersema PD, Offerhaus GJ, Vleggaar FP. WNT-pathway activation in IBD-Associated colorectal carcinogenesis: Potential biomarkers for colonic surveillance. Cell Oncol 2010; 32:303-310
90. Itzkowitz SH, Marshall A, Kornbluth A, Harpaz N, McHugh JB, Ahnen D, Sachar DB. Sialosyl-Tn antigen: Initial report of a new marker of malignant progression in long-standing ulcerative colitis. Gastroenterology 1995; 109:490-497
91. Buda A, Lamboglia F, Hatem G, D'Incà R, Sturniolo GC. Evolving endoscopic technologies for the detection of dysplasia in inflammatory bowel diseases. Ann Ital Chir 2011; 82:29-35
92. Va'zquez-Marti'n C, Cuevas E, Gil-Marti'n E, Fernández-Briera A. Correlation analysis between tumor-Associated antigen sialyl-Tn expression and ST6GalNAc I activity in human colon adenocarcinoma. Oncology 2004; 67:159-165
93. Repici A, Laterra MA, Cisaro F, Pellicano R, Fini L, Ishaq S. Unveiling cancer in IBD: Screening colonoscopy or chromoendoscopy. Curr Drug Targets 2012 [Epub ahead of print