Human colon carcinogenesis is associated with increased interleukin-17-driven inflammatory responses

Drug Design, Development and Therapy

Volumn 9, Issue , 2015, Pages 1679-1689

  Xie, Zhaohui ^a   Qu, Yine ^b   Leng, Yanli ^b   Sun, Wenxiu ^b   Ma, Siqi ^b   Wei, Jingbo ^b   Hu, Jiangong ^c   Zhang, Xiaolan ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

^b HEBEI UNITED UNIVERSITY   (China)

^c TIANJIN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Colitis; Colorectal cancer; IL 17; Inflammation

Indexed keywords

CYCLIN D1; GELATINASE A; GELATINASE B; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; MATRILYSIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BAX; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ADULT; AGED; ANGIOGENESIS; ARTICLE; CLINICAL ARTICLE; COLON ADENOCARCINOMA; COLON ADENOMA; COLON BIOPSY; COLON CARCINOGENESIS; COLON POLYP; COLON RESECTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG RESEARCH; DRUG TARGETING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS; VERY ELDERLY; WESTERN BLOTTING; ADENOCARCINOMA; ADOLESCENT; CARCINOGENESIS; COLON TUMOR; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; YOUNG ADULT;

ADENOCARCINOMA; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CARCINOGENESIS; COLONIC NEOPLASMS; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-17; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84929157473     PISSN: 11778881     EISSN: 11778881     Source Type: Journal    
DOI: 10.2147/DDDT.S79431     Document Type: Article

References (59)

1. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity. 2004;21(4):467–476.
2. Novatchkova M, Leibbrandt A, Werzowa J, Neubüser A, Eisenhaber F. The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem Sci. 2003;28(5):226–229.
3. Chang SH, Park H, Dong C. Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J Biol Chem. 2006;281(47):35603–35607.
4. Qian Y, Liu C, Hartupee J, et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol. 2007;8(3):247–256.
5. Maitra A, Shen F, Hanel W, et al. Distinct functional motifs within the IL-17 receptor regulate signal transduction and target gene expression. Proc Natl Acad Sci U S A. 2007;104(18):7506–7511.
6. Ho AW, Shen F, Conti HR, et al. IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail. J Immunol. 2010;185(2):1063–1070.
7. Liu C, Qian W, Qian Y, et al. Act1, a U-box E3 ubiquitin ligase for IL-17 signaling. Sci Signal. 2009;2(92):ra63.
8. Ge D, Dauchy RT, Liu S, et al. Insulin and IGF1 enhance IL-17-induced chemokine expression through a GSK3B-dependent mechanism: a new target for melatonin’s anti-inflammatory action. J Pineal Res. 2013;55(4):377–387.
9. Zhu S, Pan W, Song X, et al. The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-α. Nat Med. 2012;18(7):1077–1086.
10. Hwang SY, Kim JY, Kim KW, et al. IL-17 induces production of IL-6 and IL-8 in rheumatoid arthritis synovial fibroblasts via NF-kappaB-and PI3-kinase/Akt-dependent pathways. Arthritis Res Ther. 2004;6(2):R120–R128.
11. Bulek K, Liu C, Swaidani S, et al. The inducible kinase IKKi is required for IL-17-dependent signaling associated with neutrophilia and pulmonary inflammation. Nat Immunol. 2011;12(9):844–852.
12. Sun D, Novotny M, Bulek K, Liu C, Li X, Hamilton T. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat Immunol. 2011;12(9):853–860.
13. Faour WH, Mancini A, He QW, Di Battista JA. T-cell-derived interleukin-17 regulates the level and stability of cyclooxygenase-2 (COX-2) mRNA through restricted activation of the p38 mitogen-activated protein kinase cascade: role of distal sequences in the 3′-untranslated region of COX-2 mRNA. J Biol Chem. 2003;278(29):26897–26907.
14. Hata K, Andoh A, Shimada M, et al. IL-17 stimulates inflammatory responses via NF-kappaB and MAP kinase pathways in human colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol. 2002;282(6):G1035–G1044.
15. Ma X, Reynolds SL, Baker BJ, Li X, Benveniste EN, Qin H. IL-17 enhancement of the IL-6 signaling cascade in astrocytes. J Immunol. 2010;184(9):4898–4906.
16. Sylvester J, Liacini A, Li WQ, Zafarullah M. Interleukin-17 signal transduction pathways implicated in inducing matrix metalloproteinase-3,-13 and aggrecanase-1 genes in articular chondrocytes. Cell Signal. 2004;16(4):469–476.
17. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9–29.
18. Zeng S, Cai S. Colorectal cancer epidemiology and prevention study in China. Chin-Ger J Clin Oncol. 2003;2(2):72–75.
19. Xu AG, Yu ZJ, Jiang B, et al. Colorectal cancer in Guangdong Province of China: a demographic and anatomic survey. World J Gastroenterol. 2010;16(8):960–965.
20. Ahmed S, Johnson K, Ahmed O, Iqbal N. Advances in the management of colorectal cancer: from biology to treatment. Int J Colorectal Dis. 2014;29(9):1031–1042.
21. Lee J, Jeon JY, Meyerhardt JA. Diet and lifestyle in survivors of colorectal cancer. Hematol Oncol Clin North Am. 2015;29(1):1–27.
22. Tárraga López PJ, Albero JS, Rodríguez-Montes JA. Primary and secondary prevention of colorectal cancer. Clin Med Insights Gastroenterol. 2014;7:33–46.
23. Desai D, Desai N. Colorectal cancer surveillance in inflammatory bowel disease: A critical analysis. World J Gastrointest Endosc. 2014;6(11):541–548.
24. Liu S, Ren J, Li J. IL-17RA in intestinal inflammation: structure, signaling, function, and clinical application. Inflamm Bowel Dis. 2015;21(1):154–166.
25. Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–1022.
26. Chae WJ, Gibson TF, Zelterman D, Hao L, Henegariu O, Bothwell AL. Ablation of IL-17A abrogates progression of spontaneous intestinal tumorigenesis. Proc Natl Acad Sci U S A. 2010;107(12):5540–5544.
27. Chae WJ, Bothwell AL. IL-17F deficiency inhibits small intestinal tumorigenesis in ApcMin/+ mice. Biochem Biophys Res Commun. 2011;414(1):31–36.
28. Tong Z, Yang XO, Yan H, et al. A protective role by interleukin-17F in colon tumorigenesis. PLoS One. 2012;7(4):e34959.
29. Guo X, Jiang X, Xiao Y, et al. IL-17A signaling in colonic epithelial cells inhibits pro-inflammatory cytokine production by enhancing the activity of ERK and PI3K. PLoS One. 2014;9(2):e89714.
30. Wang YL, Fang M, Wang XM, et al. Proinflammatory effects and molecular mechanisms of interleukin-17 in intestinal epithelial cell line HT-29. World J Gastroenterol. 2014;20(47):17924–17931.
31. Hölttä V, Klemetti P, Salo HM, et al. Interleukin-17 immunity in pediatric Crohn disease and ulcerative colitis. J Pediatr Gastroenterol Nutr. 2013;57(3):287–292.
32. Wedebye Schmidt EG, Larsen HL, Kristensen NN, et al. TH17 cell induction and effects of IL-17A and IL-17F blockade in experimental colitis. Inflamm Bowel Dis. 2013;19(8):1567–1576.
33. Hyun YS, Han DS, Lee AR, Eun CS, Youn J, Kim HY. Role of IL-17A in the development of colitis-associated cancer. Carcinogenesis. 2012;33(4):931–936.
34. Qi H, Yang H, Xu G, et al. Therapeutic efficacy of IL-17A antibody injection in preventing the development of colitis associated carcinogenesis in mice. Immunobiology. 2015;220(1):54–59.
35. De Simone V, Pallone F, Monteleone G, Stolfi C. Role of TH17 cytokines in the control of colorectal cancer. Oncoimmunology. 2013;2(12):e26617.
36. Le Gouvello S, Bastuji-Garin S, Aloulou N, et al. High prevalence of Foxp3 and IL17 in MMR-proficient colorectal carcinomas. Gut. 2008;57(6):772–779.
37. Laan M, Lötvall J, Chung KF, Lindén A. IL-17-induced cytokine release in human bronchial epithelial cells in vitro: role of mitogen-activated protein (MAP) kinases. Br J Pharmacol. 2001;133(1):200–206.
38. Andoh A, Shimada M, Bamba S, et al. Extracellular signal-regulated kinases 1 and 2 participate in interleukin-17 plus tumor necrosis factor-alpha-induced stabilization of interleukin-6 mRNA in human pancreatic myofibroblasts. Biochim Biophys Acta. 2002;1591(1–3):69–74.
39. Li Q, Liu L, Zhang Q, Liu S, Ge D, You Z. Interleukin-17 Indirectly Promotes M2 Macrophage Differentiation through Stimulation of COX-2/PGE2 Pathway in the Cancer Cells. Cancer Res Treat. 2014;46(3):297–306.
40. Shalom-Barak T, Quach J, Lotz M. Interleukin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-kappaB. J Biol Chem. 1998;273(42):27467–27473.
41. Martel-Pelletier J, Mineau F, Jovanovic D, Di Battista JA, Pelletier JP. Mitogen-activated protein kinase and nuclear factor kappaB together regulate interleukin-17-induced nitric oxide production in human osteoarthritic chondrocytes: possible role of transactivating factor mitogen-activated protein kinase-activated proten kinase (MAPKAPK). Arthritis Rheum. 1999;42(11):2399–2409.
42. Li J, Lau GK, Chen L, et al. Interleukin 17A promotes hepatocellular carcinoma metastasis via NF-kB induced matrix metalloproteinases 2 and 9 expression. PLoS One. 2011;6(7):e21816.
43. Xu B, Guenther JF, Pociask DA, et al. Promotion of lung tumor growth by interleukin-17. Am J Physiol Lung Cell Mol Physiol. 2014;307(6):L497–L508.
44. Zhang Q, Liu S, Ge D, et al. Interleukin-17 promotes formation and growth of prostate adenocarcinoma in mouse models. Cancer Res. 2012;72(10):2589–2599.
45. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med. 2009;206(7):1457–1464.
46. Mudter J, Neurath MF. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm Bowel Dis. 2007;13(8):1016–1023.
47. Masuelli L, Di Stefano E, Fantini M, et al. Resveratrol potentiates the in vitro and in vivo anti-tumoral effects of curcumin in head and neck carcinomas. Oncotarget. 2014;5(21):10745–10762.
48. Wang L, Yi T, Zhang W, Pardoll DM, Yu H. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 2010;70(24):10112–10120.
49. Numasaki M, Lotze MT, Sasaki H. Interleukin-17 augments tumor necrosis factor-alpha-induced elaboration of proangiogenic factors from fibroblasts. Immunol Lett. 2004;93(1):39–43.
50. Honorati MC, Cattini L, Facchini A. IL-17, IL-1beta and TNF-alpha stimulate VEGF production by dedifferentiated chondrocytes. Osteoarthritis Cartilage. 2004;12(9):683–691.
51. Takahashi H, Numasaki M, Lotze MT, Sasaki H. Interleukin-17 enhances bFGF-, HGF-and VEGF-induced growth of vascular endothelial cells. Immunol Lett. 2005;98(2):189–193.
52. Zhang Q, Liu S, Zhang Q, et al. Interleukin-17 promotes development of castration-resistant prostate cancer potentially through creating an immunotolerant and pro-angiogenic tumor microenvironment. Prostate. 2014;74(8):869–879.
53. Mittal K, Ebos J, Rini B. Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond. Semin Oncol. 2014;41(2):235–251.
54. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
55. Xiao M, Wang C, Zhang J, Li Z, Zhao X, Qin Z. IFNgamma promotes papilloma development by up-regulating Th17-associated inflammation. Cancer Res. 2009;69(5):2010–2017.
56. Solt LA, Kumar N, Nuhant P, et al. Suppression of TH17 differentiation and autoimmunity by a synthetic ROR ligand. Nature. 2011;472(7344):491–494.
57. Hueber W, Patel DD, Dryja T, et al; Psoriasis Study Group; Rheumatoid Arthritis Study Group; Uveitis Study Group. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med. 2010;2(52):52ra72.
58. Leonardi C, Matheson R, Zachariae C, et al. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med. 2012;366(13):1190–1199.
59. Papp KA, Leonardi C, Menter A, et al. Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N Engl J Med. 2012;366(13):1181–1189.