IL-6 and Stat3 Are Required for Survival of Intestinal Epithelial Cells and Development of Colitis-Associated Cancer

Cancer Cell - Tập 15 - Trang 103-113 - 2009
Sergei Grivennikov1, Eliad Karin1, Janos Terzic1,2, Daniel Mucida3, Guann-Yi Yu1, Sivakumar Vallabhapurapu1, Jürgen Scheller4, Stefan Rose-John4, Hilde Cheroutre3, Lars Eckmann5, Michael Karin1
1Laboratory of Gene Regulation and Signal Transduction, Department of Pharmacology, UCSD School of Medicine, University of California, San Diego, La Jolla, CA 92093-0723, USA
2School of Medicine, University of Split, Soltanska 2, Split, HR-21000, Croatia
3La Jolla Institute for Allergy and Immunology, La Jolla, CA 92093, USA
4Department of Biochemistry, Christian-Albrechts-Universität zu Kiel, Medical Faculty, Olshausenstraße 40, D-24098 Kiel, Germany
5Department of Medicine, UCSD School of Medicine, University of California, San Diego, La Jolla, CA 92093-0723, USA

Tài liệu tham khảo

Ancrile, 2007, Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis, Genes Dev., 21, 1714, 10.1101/gad.1549407 Atreya, 2000, Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo, Nat. Med., 6, 583, 10.1038/75068 Atreya, 2005, Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer, Clin. Rev. Allergy Immunol., 28, 187, 10.1385/CRIAI:28:3:187 Balkwill, 2005, Smoldering and polarized inflammation in the initiation and promotion of malignant disease, Cancer Cell, 7, 211, 10.1016/j.ccr.2005.02.013 Becker, 2004, TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling, Immunity, 21, 491, 10.1016/j.immuni.2004.07.020 Becker, 2005, IL-6 signaling promotes tumor growth in colorectal cancer, Cell Cycle, 4, 217, 10.4161/cc.4.2.1413 Bettelli, 2006, Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells, Nature, 441, 235, 10.1038/nature04753 Bollrath, 2009, gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis, Cancer Cell, 15, 91, 10.1016/j.ccr.2009.01.002 Bromberg, 1999, Stat3 as an oncogene, Cell, 98, 295, 10.1016/S0092-8674(00)81959-5 Chan, 2004, Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis, J. Clin. Invest., 114, 720, 10.1172/JCI200421032 Coussens, 2002, Inflammation and cancer, Nature, 420, 860, 10.1038/nature01322 Dann, 2008, IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens, J. Immunol., 180, 6816, 10.4049/jimmunol.180.10.6816 Denning, 2007, Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses, Nat. Immunol., 8, 1086, 10.1038/ni1511 Dinarello, 1994, The interleukin-1 family: 10 years of discovery, FASEB J., 8, 1314, 10.1096/fasebj.8.15.8001745 Eaden, 2001, The risk of colorectal cancer in ulcerative colitis: a meta-analysis, Gut, 48, 526, 10.1136/gut.48.4.526 Ernst, 2008, STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice, J. Clin. Invest., 118, 1727 Fischer, 1997, I. A bioactive designer cytokine for human hematopoietic progenitor cell expansion, Nat. Biotechnol., 15, 142, 10.1038/nbt0297-142 Fu, 2006, STAT3 in immune responses and inflammatory bowel diseases, Cell Res., 16, 214, 10.1038/sj.cr.7310029 Gao, 2007, Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas, J. Clin. Invest., 117, 3846, 10.1172/JCI31871 Garlanda, 2007, Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory member of the interleukin-1 receptor family, Cancer Res., 67, 6017, 10.1158/0008-5472.CAN-07-0560 Greten, 2005, NF-kB: linking inflammation and immunity to cancer development and progression, Nat. Rev. Immunol., 5, 749, 10.1038/nri1703 Greten, 2004, IKKb links inflammation and tumorigenesis in a mouse model of colitis-associated cancer, Cell, 118, 285, 10.1016/j.cell.2004.07.013 Grivennikov, 2008, Autocrine IL-6 signaling: a key event in tumorigenesis?, Cancer Cell, 13, 7, 10.1016/j.ccr.2007.12.020 Heikkila, 2008, Systematic review of the association between circulating interleukin-6 (IL-6) and cancer, Eur. J. Cancer, 44, 937, 10.1016/j.ejca.2008.02.047 Hodge, 2005, The role of IL-6 and STAT3 in inflammation and cancer, Eur. J. Cancer, 41, 2502, 10.1016/j.ejca.2005.08.016 Hussain, 2003, Radical causes of cancer, Nat. Rev. Cancer, 3, 276, 10.1038/nrc1046 Jenkins, 2005, Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-beta signaling, Nat. Med., 11, 845, 10.1038/nm1282 Judd, 2004, Gastric cancer development in mice lacking the SHP2 binding site on the IL-6 family co-receptor gp130, Gastroenterology, 126, 196, 10.1053/j.gastro.2003.10.066 Karin, 2006, Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer, Cell, 124, 823, 10.1016/j.cell.2006.02.016 Kataoka, 2008, Stage-specific disruption of Stat3 demonstrates a direct requirement during both the initiation and promotion stages of mouse skin tumorigenesis, Carcinogenesis, 29, 1108, 10.1093/carcin/bgn061 Kishimoto, 2005, Interleukin-6: from basic science to medicine--40 years in immunology, Annu. Rev. Immunol., 23, 1, 10.1146/annurev.immunol.23.021704.115806 Klampfer, 2008, The role of signal transducers and activators of transcription in colon cancer, Front. Biosci., 13, 2888, 10.2741/2893 Kollias, 1999, On the role of tumor necrosis factor and receptors in models of multiorgan failure, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease, Immunol. Rev., 169, 175, 10.1111/j.1600-065X.1999.tb01315.x Kusaba, 2005, Expression of p-STAT3 in human colorectal adenocarcinoma and adenoma; correlation with clinicopathological factors, J. Clin. Pathol., 58, 833, 10.1136/jcp.2004.023416 Langholz, 1992, Colorectal cancer risk and mortality in patients with ulcerative colitis, Gastroenterology, 103, 1444, 10.1016/0016-5085(92)91163-X Legrand-Poels, 2000, Regulation of interleukin-6 gene expression by pro-inflammatory cytokines in a colon cancer cell line, Biochem. J., 349, 765, 10.1042/bj3490765 Lin, 2007, A cytokine-mediated link between innate immunity, inflammation, and cancer, J. Clin. Invest., 117, 1175, 10.1172/JCI31537 Madamanchi, 2001, Reactive oxygen species regulate heat-shock protein 70 via the JAK/STAT pathway, Arterioscler. Thromb. Vasc. Biol., 21, 321, 10.1161/01.ATV.21.3.321 Madison, 2002, Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine, J. Biol. Chem., 277, 33275, 10.1074/jbc.M204935200 Meira, 2008, DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice, J. Clin. Invest., 118, 2516 Mitsuyama, 2006, Interleukin-6 trans-signaling in inflammatory bowel disease, Cytokine Growth Factor Rev., 17, 451, 10.1016/j.cytogfr.2006.09.003 Neufert, 2007, An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression, Nat. Protoc., 2, 1998, 10.1038/nprot.2007.279 Parikh, 1997, IL-6 production in human intestinal epithelial cells following stimulation with IL-1 beta is associated with activation of the transcription factor NF-kappa B, J. Surg. Res., 69, 139, 10.1006/jsre.1997.5061 Peters, 1998, In vivo and in vitro activities of the gp130-stimulating designer cytokine Hyper-IL-6, J. Immunol., 161, 3575, 10.4049/jimmunol.161.7.3575 Pikarsky, 2004, NF-kB functions as a tumour promoter in inflammation-associated cancer, Nature, 431, 461, 10.1038/nature02924 Popivanova, 2008, Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis, J. Clin. Invest., 118, 560 Poutahidis, 2007, Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma, Carcinogenesis, 28, 2614, 10.1093/carcin/bgm180 Radisky, 2004, Cancer. Respect thy neighbor!, Science, 303, 775, 10.1126/science.1094412 Rakoff-Nahoum, 2004, Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis, Cell, 118, 229, 10.1016/j.cell.2004.07.002 Rigby, 2007, Suppressor of cytokine signaling 3 (SOCS3) limits damage-induced crypt hyper-proliferation and inflammation-associated tumorigenesis in the colon, Oncogene, 26, 4833, 10.1038/sj.onc.1210286 Rivat, 2004, Disruption of STAT3 signaling leads to tumor cell invasion through alterations of homotypic cell-cell adhesion complexes, Oncogene, 23, 3317, 10.1038/sj.onc.1207437 Romano, 1997, Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment, Immunity, 6, 315, 10.1016/S1074-7613(00)80334-9 Sakurai, 2008, Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis, Cancer Cell, 14, 156, 10.1016/j.ccr.2008.06.016 Sander, 2008, Gp130 signaling promotes development of acute experimental colitis by facilitating early neutrophil/macrophage recruitment and activation, J. Immunol., 181, 3586, 10.4049/jimmunol.181.5.3586 Sansone, 2007, IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland, J. Clin. Invest., 117, 3988, 10.1172/JCI32533 Sriuranpong, 2003, Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system, Cancer Res., 63, 2948 Strober, 2007, The fundamental basis of inflammatory bowel disease, J. Clin. Invest., 117, 514, 10.1172/JCI30587 Sugimoto, 2008, IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis, J. Clin. Invest., 118, 534 Suzuki, 2001, CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation, J. Exp. Med., 193, 471, 10.1084/jem.193.4.471 Takeda, 1999, Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils, Immunity, 10, 39, 10.1016/S1074-7613(00)80005-9 Tebbutt, 2002, Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice, Nat. Med., 8, 1089, 10.1038/nm763 Veldhoen, 2006, TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells, Immunity, 24, 179, 10.1016/j.immuni.2006.01.001 Wang, 2004, Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells, Nat. Med., 10, 48, 10.1038/nm976 Weir, 2003, Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control, J. Natl. Cancer Inst., 95, 1276, 10.1093/jnci/djg040 Xiao, 2007, The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis, Immunity, 26, 461, 10.1016/j.immuni.2007.02.012 Yamaoka, 2008, Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis, Proc. Natl. Acad. Sci. USA, 105, 11772, 10.1073/pnas.0801463105 Yu, 2007, Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment, Nat. Rev. Immunol., 7, 41, 10.1038/nri1995 Zheng, 2008, Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens, Nat. Med., 14, 282, 10.1038/nm1720