Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-κB-Dependent Manner

Cancer Cell - Tập 17 - Trang 135-147 - 2010
Neta Erez1,2,3, Morgan Truitt1,2,3, Peter Olson1,2,3, Douglas Hanahan1,2,3
1Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA 94143, USA
2Diabetes Center, University of California, San Francisco, San Francisco, CA 94143, USA
3Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA 94143, USA

Tài liệu tham khảo

Adegboyega, 2004, Subepithelial myofibroblasts express cyclooxygenase-2 in colorectal tubular adenomas, Clin. Cancer Res., 10, 5870, 10.1158/1078-0432.CCR-0431-03 Allinen, 2004, Molecular characterization of the tumor microenvironment in breast cancer, Cancer Cell, 6, 17, 10.1016/j.ccr.2004.06.010 Anderberg, 2009, Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts, Cancer Res., 69, 369, 10.1158/0008-5472.CAN-08-2724 Anderson, 2000, The angiogenic factor interleukin 8 is induced in non-small cell lung cancer/pulmonary fibroblast cocultures, Cancer Res., 60, 269 Andreu, 2010, FcRγ activation regulates inflammation-associated squamous carcinogenesis, Cancer Cell, 17, 121, 10.1016/j.ccr.2009.12.019 Arbeit, 1996, Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice, Proc. Natl. Acad. Sci. USA, 93, 2930, 10.1073/pnas.93.7.2930 Arbeit, 1994, Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice, J. Virol., 68, 4358, 10.1128/jvi.68.7.4358-4368.1994 Augsten, 2009, CXCL14 is an autocrine growth factor for fibroblasts and acts as a multi-modal stimulator of prostate tumor growth, Proc. Natl. Acad. Sci. USA, 106, 3414, 10.1073/pnas.0813144106 Baglole, 2008, The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-kappaB family member RelB, J. Biol. Chem., 283, 28944, 10.1074/jbc.M800685200 Bardeesy, 2006, Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse, Proc. Natl. Acad. Sci. USA, 103, 5947, 10.1073/pnas.0601273103 Begley, 2008, The inflammatory microenvironment of the aging prostate facilitates cellular proliferation and hypertrophy, Cytokine, 43, 194, 10.1016/j.cyto.2008.05.012 Bhowmick, 2004, TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia, Science, 303, 848, 10.1126/science.1090922 Bhowmick, 2004, Stromal fibroblasts in cancer initiation and progression, Nature, 432, 332, 10.1038/nature03096 Bissell, 2001, Putting tumours in context, Nat. Rev. Cancer, 1, 46, 10.1038/35094059 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 Brigstock, 2002, Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61), Angiogenesis, 5, 153, 10.1023/A:1023823803510 Buckley, 2001, Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation, Trends Immunol., 22, 199, 10.1016/S1471-4906(01)01863-4 Cahill, 2008, Interleukin (IL) 1beta induction of IL-6 is mediated by a novel phosphatidylinositol 3-kinase-dependent AKT/IkappaB kinase alpha pathway targeting activator protein-1, J. Biol. Chem., 283, 25900, 10.1074/jbc.M707692200 Chen, 2003, The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion, Nat. Med., 9, 575, 10.1038/nm849 Condeelis, 2006, Macrophages: obligate partners for tumor cell migration, invasion, and metastasis, Cell, 124, 263, 10.1016/j.cell.2006.01.007 Cook, 2005, Osteopontin induces multiple changes in gene expression that reflect the six “hallmarks of cancer” in a model of breast cancer progression, Mol. Carcinog., 43, 225, 10.1002/mc.20105 Coussens, 1996, Genetic predisposition and parameters of malignant progression in K14-HPV16 transgenic mice, Am. J. Pathol., 149, 1899 Coussens, 1999, Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis, Genes Dev., 13, 1382, 10.1101/gad.13.11.1382 Coussens, 2000, MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis, Cell, 103, 481, 10.1016/S0092-8674(00)00139-2 Crawford, 2009, PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment, Cancer Cell, 15, 21, 10.1016/j.ccr.2008.12.004 De Marzo, 1999, Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis, Am. J. Pathol., 155, 1985, 10.1016/S0002-9440(10)65517-4 de Visser, 2006, Paradoxical roles of the immune system during cancer development, Nat. Rev. Cancer, 6, 24, 10.1038/nrc1782 de Visser, 2005, De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent, Cancer Cell, 7, 411, 10.1016/j.ccr.2005.04.014 Desmouliere, 2004, The stroma reaction myofibroblast: a key player in the control of tumor cell behavior, Int. J. Dev. Biol., 48, 509, 10.1387/ijdb.041802ad Elson, 2000, Sensitivity of the cervical transformation zone to estrogen-induced squamous carcinogenesis, Cancer Res., 60, 1267 Finak, 2008, Stromal gene expression predicts clinical outcome in breast cancer, Nat Med, 14, 518, 10.1038/nm1764 Flavell, 2008, Fibroblasts as novel therapeutic targets in chronic inflammation, Br. J. Pharmacol., 153, S241, 10.1038/sj.bjp.0707487 Gallagher, 2005, Gene expression profiling reveals cross-talk between melanoma and fibroblasts: implications for host-tumor interactions in metastasis, Cancer Res., 65, 4134, 10.1158/0008-5472.CAN-04-0415 Ghosh, 2002, Missing pieces in the NF-kappaB puzzle, Cell, 109, S81, 10.1016/S0092-8674(02)00703-1 Giraudo, 2004, An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis, J. Clin. Invest., 114, 623, 10.1172/JCI200422087 Greten, 2004, IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer, Cell, 118, 285, 10.1016/j.cell.2004.07.013 Grivennikov, 2009, IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer, Cancer Cell, 15, 103, 10.1016/j.ccr.2009.01.001 Guy, 1992, Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease, Mol. Cell. Biol., 12, 954 Hanahan, 2000, The hallmarks of cancer, Cell, 100, 57, 10.1016/S0092-8674(00)81683-9 Harris, 2009, Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung, Inflammopharmacology, 17, 55, 10.1007/s10787-009-8049-8 Hinz, 2007, The myofibroblast: one function, multiple origins, Am. J. Pathol., 170, 1807, 10.2353/ajpath.2007.070112 Hu, 2005, Distinct epigenetic changes in the stromal cells of breast cancers, Nat. Genet., 37, 899, 10.1038/ng1596 Kalluri, 2009, The basics of epithelial-mesenchymal transition, J. Clin. Invest., 119, 1420, 10.1172/JCI39104 Kalluri, 2006, Fibroblasts in cancer, Nat. Rev. Cancer, 6, 392, 10.1038/nrc1877 Karin, 2000, Phosphorylation meets ubiquitination: the control of NF-κB activity, Annu. Rev. Immunol., 18, 621, 10.1146/annurev.immunol.18.1.621 Karin, 2005, NF-kappaB: linking inflammation and immunity to cancer development and progression, Nat. Rev. Immunol., 5, 749, 10.1038/nri1703 Kisseleva, 2008, Mechanisms of fibrogenesis, Exp. Biol. Med. (Maywood), 233, 109, 10.3181/0707-MR-190 Korc, 2007, Pancreatic cancer-associated stroma production, Am. J. Surg., 194, S84, 10.1016/j.amjsurg.2007.05.004 Kuper, 2000, Infections as a major preventable cause of human cancer, J. Intern. Med., 248, 171, 10.1046/j.1365-2796.2000.00742.x Lin, 2003, Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases, Am. J. Pathol., 163, 2113, 10.1016/S0002-9440(10)63568-7 Mahadevan, 2007, Tumor-stroma interactions in pancreatic ductal adenocarcinoma, Mol. Cancer Ther., 6, 1186, 10.1158/1535-7163.MCT-06-0686 Mantovani, 2008, Cancer-related inflammation, Nature, 454, 436, 10.1038/nature07205 Martey, 2004, Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer, Am. J. Physiol. Lung Cell. Mol. Physiol., 287, L981, 10.1152/ajplung.00239.2003 Meylan, 2009, Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma, Nature, 462, 104, 10.1038/nature08462 Micke, 2007, In situ identification of genes regulated specifically in fibroblasts of human basal cell carcinoma, J. Invest. Dermatol., 127, 1516, 10.1038/sj.jid.5700714 Micke, 2004, Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy?, Lung Cancer, 45, S163, 10.1016/j.lungcan.2004.07.977 Monnier, 2008, CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma, Cancer Res., 68, 7323, 10.1158/0008-5472.CAN-08-0841 Mueller, 2007, Stromal fibroblasts in colorectal liver metastases originate from resident fibroblasts and generate an inflammatory microenvironment, Am. J. Pathol., 171, 1608, 10.2353/ajpath.2007.060661 Nyberg, 2008, Tumor microenvironment and angiogenesis, Front. Biosci., 13, 6537, 10.2741/3173 Olumi, 1999, Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium, Cancer Res., 59, 5002 Orimo, 2005, Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion, Cell, 121, 335, 10.1016/j.cell.2005.02.034 Orimo, 2006, Stromal fibroblasts in cancer: a novel tumor-promoting cell type, Cell Cycle, 5, 1597, 10.4161/cc.5.15.3112 Pazolli, 2009, Senescent stromal-derived osteopontin promotes preneoplastic cell growth, Cancer Res., 69, 1230, 10.1158/0008-5472.CAN-08-2970 Pereira, 2008, Nuclear factor-kappaB1: regulation and function, Int. J. Biochem. Cell Biol., 40, 1425, 10.1016/j.biocel.2007.05.004 Pietras, 2008, Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting, PLoS Med., 5, e19, 10.1371/journal.pmed.0050019 Pikarsky, 2004, NF-kappaB functions as a tumour promoter in inflammation-associated cancer, Nature, 431, 461, 10.1038/nature02924 Pollard, 2004, Tumour-educated macrophages promote tumour progression and metastasis, Nat. Rev. Cancer, 4, 71, 10.1038/nrc1256 Rhodes, 2004, ONCOMINE: a cancer microarray database and integrated data-mining platform, Neoplasia, 6, 1, 10.1016/S1476-5586(04)80047-2 Rinn, 2006, Anatomic demarcation by positional variation in fibroblast gene expression programs, PLoS Genet., 2, e119, 10.1371/journal.pgen.0020119 Sahin, 2009, Cyclooxygenase-2 in cancer and angiogenesis, Angiology, 60, 242, 10.1177/0003319708318378 Sato, 2004, Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts, Cancer Res., 64, 6950, 10.1158/0008-5472.CAN-04-0677 Silzle, 2003, Tumor-associated fibroblasts recruit blood monocytes into tumor tissue, Eur. J. Immunol., 33, 1311, 10.1002/eji.200323057 Smith, 1997, Fibroblasts as sentinel cells: synthesis of chemokines and regulation of inflammation, Am. J. Pathol., 151, 317 Sugimoto, 2006, Identification of fibroblast heterogeneity in the tumor microenvironment, Cancer Biol. Ther., 5, 1640, 10.4161/cbt.5.12.3354 Tlsty, 2006, Tumor stroma and regulation of cancer development, Annu. Rev. Pathol., 1, 119, 10.1146/annurev.pathol.1.110304.100224 Trimboli, 2009, Pten in stromal fibroblasts suppresses mammary epithelial tumours, Nature, 461, 1084, 10.1038/nature08486 van Kempen, 2006, Inflammation, proteases and cancer, Eur. J. Cancer, 42, 728, 10.1016/j.ejca.2006.01.004 Vandoros, 2006, PPAR-gamma is expressed and NF-kB pathway is activated and correlates positively with COX-2 expression in stromal myofibroblasts surrounding colon adenocarcinomas, J. Cancer Res. Clin. Oncol., 132, 76, 10.1007/s00432-005-0042-z Walker, 2001, The complexities of breast cancer desmoplasia, Breast Cancer Res., 3, 143, 10.1186/bcr287 Whiteside, 2008, The tumor microenvironment and its role in promoting tumor growth, Oncogene, 27, 5904, 10.1038/onc.2008.271 Wu, 2009, Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion, Cancer Cell, 15, 416, 10.1016/j.ccr.2009.03.016