Novel evidence for an oncogenic role of microRNA-21 in colitis-associated colorectal cancer

Gut

Volumn 65, Issue 9, 2016, Pages 1470-1481

  Shi, Chenzhang ^a   Yang, Yongzhi ^a   Xia, Yang ^b   Okugawa, Yoshinaga ^c   Yang, Jun ^b   Liang, Yong ^b   Chen, Hongqi ^b   Zhang, Peng ^a   Wang, Feng ^a   Han, Huazhong ^b   Wu, Wen ^a   Gao, Renyuan ^a   Gasche, Christoph ^d   Qin, Huanlong ^a   Ma, Yanlei ^a   Goel, Ajay ^c  

^a TENTH PEOPLE S HOSPITAL OF TONGJI UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^c BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Cancer; colorectal cancer

Indexed keywords

BETA CATENIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; KI 67 ANTIGEN; MICRORNA 21; PROTEIN BCL 2; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX9; UVOMORULIN; APOPTOSIS REGULATORY PROTEIN; CADHERIN; MICRORNA; MIRN21 MICRORNA, HUMAN; PDCD4 PROTEIN, MOUSE; RNA BINDING PROTEIN; SOX9 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; COLITIS; COLORECTAL CANCER; CONTROLLED STUDY; FEMALE; GENE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PDCD4 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; ANIMAL; CANCER STAGING; COLON; COLON TUMOR; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BETA CATENIN; CADHERINS; CARCINOGENESIS; CELL PROLIFERATION; COLITIS; COLON; COLONIC NEOPLASMS; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; MIDDLE AGED; NEOPLASM STAGING; RNA-BINDING PROTEINS; SOX9 TRANSCRIPTION FACTOR;

EID: 84931313475     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2014-308455     Document Type: Article

References (49)

1. Mantovani A, Allavena P, Sica A, et al. Cancer-related inflammation. Nature 2008;454:436-44.
2. Stolfi C, Rizzo A, Franze E, et al. Involvement of interleukin-21 in the regulation of colitis-associated colon cancer. J Exp Med 2011;208:2279-90.
3. Gupta RB, Harpaz N, Itzkowitz S, et al. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology 2007;133:1099-105; quiz 340-1.
4. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004;126:451-9.
5. Francescone R, Hou V, Grivennikov SI. Cytokines, IBD, and colitis-associated cancer. Inflamm Bowel Dis 2015;21:409-18.
6. Craven B, Zaric V, Martin A, et al. Effect of genetic deletion or pharmacological antagonism of tumor necrosis factor alpha on colitis-associated carcinogenesis in mice. Inflamm Bowel Dis 2015;21:485-95.
7. Bai J, Li Y, Shao T, et al. Integrating analysis reveals microRNA-mediated pathway crosstalk among Crohn's disease, ulcerative colitis and colorectal cancer. Mol Biosyst 2014;10:2317-28.
8. Josse C, Bouznad N, Geurts P, et al. Identification of a microRNA landscape targeting the PI3K/Akt signaling pathway in inflammation-induced colorectal carcinogenesis. Am J Physiol Gastrointest Liver Physiol 2014;306:G229-43.
9. Ueda Y, Ando T, Nanjo S, et al. DNA methylation of microRNA-124a is a potential risk marker of colitis-associated cancer in patients with ulcerative colitis. Dig Dis Sci 2014;59:2444-51.
10. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 2005;65:6029-33.
11. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006;103:2257-61.
12. Schetter AJ, Leung SY, Sohn JJ, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008;299:425-36.
13. Wang P, Zou F, Zhang X, et al. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res 2009;69:8157-65.
14. Asangani IA, Rasheed SA, Nikolova DA, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008;27:2128-36.
15. Meng F, Henson R, Wehbe-Janek H, et al. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007;133:647-58.
16. Zhu S, Si ML, Wu H, et al. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 2007;282:14328-36.
17. Sayed D, Rane S, Lypowy J, et al. MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol Biol Cell 2008;19:3272-82.
18. Wu H, Neilson JR, Kumar P, et al. miRNA profiling of naive, effector and memory CD8T cells. PLoS ONE 2007;2:e1020.
19. Shi C, Liang Y, Yang J, et al. MicroRNA-21 knockout improve the survival rate in DSS induced fatal colitis through protecting against inflammation and tissue injury. PLoS ONE 2013;8:e66814.
20. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990;98:694-702.
21. Popivanova BK, Kitamura K, Wu Y, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-70.
22. Greten FR, Eckmann L, Greten TF, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
23. 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;15:103-13.
24. Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17T cell responses. Nat Med 2009;15:1016-22.
25. Terzic J, Grivennikov S, Karin E, et al. Inflammation and colon cancer. Gastroenterology 2010;138:2101-14.e5.
26. Zhang XY, Shen BR, Zhang YC, et al. Induction of thoracic aortic remodeling by endothelial-specific deletion of microRNA-21 in mice. PLoS ONE 2013;8:e59002.
27. Holzenberger M, Lenzner C, Leneuve P, et al. Cre-mediated germline mosaicism: a method allowing rapid generation of several alleles of a target gene. Nucleic Acids Res 2000;28:E92.
28. Koliaraki V, Roulis M, Kollias G. Tpl2 regulates intestinal myofibroblast HGF release to suppress colitis-associated tumorigenesis. J Clin Invest 2012;122:4231-42.
29. Vetrano S, Rescigno M, Cera MR, et al. Unique role of junctional adhesion molecule-a in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 2008;135:173-84.
30. Scaldaferri F, Sans M, Vetrano S, et al. Crucial role of the protein C pathway in governing microvascular inflammation in inflammatory bowel disease. J Clin Invest 2007;117:1951-60.
31. Campa MJ, Wang MZ, Howard B, et al. Protein expression profiling identifies macrophage migration inhibitory factor and cyclophilin a as potential molecular targets in non-small cell lung cancer. Cancer Res 2003;63:1652-6.
32. Xiao F, Zuo Z, Cai G, et al. miRecords: an integrated resource for microRNA-target interactions. Nucleic acids research 2009;37:D105-10.
33. Hwang SK, Baker AR, Young MR, et al. Tumor suppressor PDCD4 inhibits NF-kappaB-dependent transcription in human glioblastoma cells by direct interaction with p65. Carcinogenesis 2014;35:1469-80.
34. Caprioli F, Sarra M, Caruso R, et al. Autocrine regulation of IL-21 production in human T lymphocytes. J Immunol 2008;180:1800-7.
35. Hirahara K, Ghoreschi K, Laurence A, et al. Signal transduction pathways and transcriptional regulation in Th17 cell differentiation. Cytokine Growth Factor Rev 2010;21:425-34.
36. Atreya R, Neurath MF. Signaling molecules: the pathogenic role of the IL-6/STAT-3 trans signaling pathway in intestinal inflammation and in colonic cancer. Curr Drug Targets 2008;9:369-74.
37. Bhattacharya S, Ray RM, Johnson LR. STAT3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyamine-depleted cells. Biochem J 2005;392:335-44.
38. Yang Y, Ma Y, Shi C, et al. Overexpression of miR-21 in patients with ulcerative colitis impairs intestinal epithelial barrier function through targeting the Rho GTPase RhoB. Biochem Biophys Res Commun 2013;434:746-52.
39. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998;396:643-9.
40. Karin M, Lawrence T, Nizet V. Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell 2006;124:823-35.
41. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.
42. Lin WW, Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007;117:1175-83.
43. Pikarsky E, Porat RM, Stein I, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004;431:461-6.
44. Ling M, Li Y, Xu Y, et al. Regulation of miRNA-21 by reactive oxygen speciesactivated ERK/NF-kappaB in arsenite-induced cell transformation. Free Radic Biol Med 2012;52:1508-18.
45. Iliopoulos D, Jaeger SA, Hirsch HA, et al. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010;39:493-506.
46. Luo F, Xu Y, Ling M, et al. Arsenite evokes IL-6 secretion, autocrine regulation of STAT3 signaling, and miR-21 expression, processes involved in the EMT and malignant transformation of human bronchial epithelial cells. Toxicol Appl Pharmacol 2013;273:27-34.
47. Maniati E, Soper R, Hagemann T. Up for Mischief? IL-17/Th17 in the tumour microenvironment. Oncogene 2010;29:5653-62.
48. Ancrile B, Lim KH, Counter CM. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev 2007;21:1714-19.
49. Gao SP, Mark KG, Leslie K, et al. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 2007;117:3846-56.