Estrogen receptor α in cancer associated fibroblasts suppresses prostate cancer invasion via reducing CCL5, IL6 and macrophage infiltration in the tumor microenvironment
参考文献:1.Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–30.PubMed CrossRef 2.Nunez C, Cansino JR, Bethencourt F, Perez-Utrilla M, Fraile B, Martinez-Onsurbe P, et al. TNF/IL-1/NIK/NF-kappa B transduction pathway: a comparative study in normal and pathological human prostate (benign hyperplasia and carcinoma). Histopathology. 2008;53:166–76.PubMed CrossRef 3.Nelson WG, De Marzo AM, DeWeese TL, Isaacs WB. The role of inflammation in the pathogenesis of prostate cancer. J Urol. 2004;172:S6–11. discussion S11-12.PubMed CrossRef 4.De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, Drake CG, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007;7:256–69.PubMed PubMedCentral CrossRef 5.Sciarra A, Di Silverio F, Salciccia S, Autran Gomez AM, Gentilucci A, Gentile V. Inflammation and chronic prostatic diseases: evidence for a link? Eur Urol. 2007;52:964–72.PubMed CrossRef 6.MacLennan GT, Eisenberg R, Fleshman RL, Taylor JM, Fu P, Resnick MI, et al. The influence of chronic inflammation in prostatic carcinogenesis: a 5-year followup study. J Urol. 2006;176:1012–6.PubMed CrossRef 7.Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002;196:254–65.PubMed CrossRef 8.Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605–12.PubMed CrossRef 9.Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003;3:422–33.PubMed CrossRef 10.Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I, et al. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc Natl Acad Sci U S A. 2010;107:20009–14.PubMed PubMedCentral CrossRef 11.Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell. 2011;19:257–72.PubMed PubMedCentral CrossRef 12.Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002;3:349–63.PubMed CrossRef 13.Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-kappaB-Dependent Manner. Cancer Cell. 2010;17:135–47.PubMed CrossRef 14.Ellem SJ, Schmitt JF, Pedersen JS, Frydenberg M, Risbridger GP. Local aromatase expression in human prostate is altered in malignancy. J Clin Endocrinol Metab. 2004;89:2434–41.PubMed CrossRef 15.Vermeulen A, Kaufman JM, Goemaere S, van Pottelberg I. Estradiol in elderly men. Aging Male. 2002;5:98–102.PubMed CrossRef 16.Bosland MC, Ford H, Horton L. Induction at high incidence of ductal prostate adenocarcinomas in NBL/Cr and Sprague–Dawley Hsd:SD rats treated with a combination of testosterone and estradiol-17 beta or diethylstilbestrol. Carcinogenesis. 1995;16:1311–7.PubMed CrossRef 17.Nilsson S, Gustafsson JA. Estrogen receptor transcription and transactivation: Basic aspects of estrogen action. Breast Cancer Res. 2000;2:360–6.PubMed PubMedCentral CrossRef 18.Greene GL, Gilna P, Waterfield M, Baker A, Hort Y, Shine J. Sequence and expression of human estrogen receptor complementary DNA. Science. 1986;231:1150–4.PubMed CrossRef 19.Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A. 1996;93:5925–30.PubMed PubMedCentral CrossRef 20.Leav I, Lau KM, Adams JY, McNeal JE, Taplin ME, Wang J, et al. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol. 2001;159:79–92.PubMed PubMedCentral CrossRef 21.Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.PubMed CrossRef 22.Solinas G, Germano G, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol. 2009;86:1065–73.PubMed CrossRef 23.Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549–55.PubMed CrossRef 24.Slavin S, Yeh CR, Da J, Yu S, Miyamoto H, Messing EM, et al. Estrogen receptor alpha in cancer-associated fibroblasts suppresses prostate cancer invasion via modulation of thrombospondin 2 and matrix metalloproteinase 3. Carcinogenesis. 2014;35:1301–9.PubMed PubMedCentral CrossRef 25.Chen M, Yeh CR, Shyr CR, Lin HH, Da J, Yeh S. Reduced prostate branching morphogenesis in stromal fibroblast, but not in epithelial, estrogen receptor alpha knockout mice. Asian J Androl. 2012;14:546–55.PubMed PubMedCentral CrossRef 26.Vitkus S, Yeh CR, Lin HH, Hsu I, Yu J, Chen M, et al. Distinct function of estrogen receptor alpha in smooth muscle and fibroblast cells in prostate development. Mol Endocrinol. 2013;27:38–49.PubMed PubMedCentral CrossRef 27.Bosland MC. Sex steroids and prostate carcinogenesis: integrated, multifactorial working hypothesis. Ann N Y Acad Sci. 2006;1089:168–76.PubMed PubMedCentral CrossRef 28.Daniels G, Gellert LL, Melamed J, Hatcher D, Li Y, Wei J, et al. Decreased expression of stromal estrogen receptor alpha and beta in prostate cancer. Am J Transl Res. 2014;6:140–6.PubMed PubMedCentral 29.Xiang B, Muthuswamy SK: Using Three‐Dimensional Acinar Structures for Molecular and Cell Biological Assays. Methods in Enzymology. Volume 406. Edited by William E. Balch CJD, Alan H: Academic Press. 2006;406:692–701. 30.Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes. 2009;58:2574–82.PubMed PubMedCentral CrossRef 31.Lee G-S, Choi K-C, Han H-J, Jeung E-B. The classical and a non-classical pathways associated with NF-κB are involved in estrogen-medicated regulation of Calbindin-D9k gene in rat pituitary cells. Mol Cell Endocrinol. 2007;277:42–50.PubMed CrossRef 32.Jakacka M, Ito M, Weiss J, Chien P-Y, Gehm BD, Jameson JL. Estrogen receptor binding to DNA is not required for its activity through the nonclassical AP1 pathway. J Biol Chem. 2001;276:13615–21.PubMed 33.Kumar D, Hosse J, von Toerne C, Noessner E, Nelson PJ. JNK MAPK pathway regulates constitutive transcription of CCL5 by human NK cells through SP1. J Immunol. 2009;182:1011–20.PubMed CrossRef 34.Lucia MS, Torkko KC. Inflammation as a target for prostate cancer chemoprevention: pathological and laboratory rationale. J Urol. 2004;171:S30–34. discussion S35.PubMed CrossRef 35.Nelson WG, De Marzo AM, Isaacs WB. Prostate cancer. N Engl J Med. 2003;349:366–81.PubMed CrossRef 36.De Marzo AM, Marchi VL, Epstein JI, Nelson WG. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol. 1999;155:1985–92.PubMed PubMedCentral CrossRef 37.Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4:540–50.PubMed CrossRef 38.Ronnov-Jessen L, Petersen OW, Bissell MJ. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev. 1996;76:69–125.PubMed 39.Guo X, Oshima H, Kitmura T, Taketo MM, Oshima M. Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem. 2008;283:19864–71.PubMed CrossRef 40.Camp JT, Elloumi F, Roman-Perez E, Rein J, Stewart DA, Harrell JC, et al. Interactions with fibroblasts are distinct in Basal-like and luminal breast cancers. Mol Cancer Res. 2011;9:3–13.PubMed PubMedCentral CrossRef 41.Camps JL, Chang SM, Hsu TC, Freeman MR, Hong SJ, Zhau HE, et al. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci U S A. 1990;87:75–9.PubMed PubMedCentral CrossRef 42.Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol. 1993;9:541–73.PubMed CrossRef 43.Balkwill FR, Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol. 2012;22:33–40.PubMed CrossRef 44.Mueller L, von Seggern L, Schumacher J, Goumas F, Wilms C, Braun F, et al. TNF-alpha similarly induces IL-6 and MCP-1 in fibroblasts from colorectal liver metastases and normal liver fibroblasts. Biochem Biophys Res Commun. 2010;397:586–91.PubMed CrossRef 45.Silzle T, Kreutz M, Dobler MA, Brockhoff G, Knuechel R, Kunz-Schughart LA. Tumor-associated fibroblasts recruit blood monocytes into tumor tissue. Eur J Immunol. 2003;33:1311–20.PubMed CrossRef 46.Robinson SC, Scott KA, Wilson JL, Thompson RG, Proudfoot AE, Balkwill FR. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res. 2003;63:8360–5.PubMed 47.Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122:787–95.PubMed PubMedCentral CrossRef 48.Comito G, Giannoni E, Segura CP, Barcellos-de-Souza P, Raspollini MR, Baroni G, et al. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene. 2014;33:2423–31.PubMed CrossRef 49.Chen M, Yeh CR, Chang HC, Vitkus S, Wen XQ, Bhowmick NA, et al. Loss of epithelial oestrogen receptor α inhibits oestrogen-stimulated prostate proliferation and squamous metaplasia via in vivo tissue selective knockout models. J of Pathology. 2012;226:17–27.CrossRef 50.Ricke WA, McPherson SJ, Bianco JJ, Cunha GR, Wang Y, Risbridger GP. Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor alpha signaling. FASEB J. 2008;22:1512–20.PubMed CrossRef 51.Attia DM, Ederveen AG. Opposing roles of ERalpha and ERbeta in the genesis and progression of adenocarcinoma in the rat ventral prostate. Prostate. 2012;72:1013–22.PubMed CrossRef 52.Royuela M, de Miguel MP, Bethencourt FR, Sanchez-Chapado M, Fraile B, Arenas MI, et al. Estrogen receptors alpha and beta in the normal, hyperplastic and carcinomatous human prostate. J Endocrinol. 2001;168:447–54.PubMed CrossRef 53.Celhay O, Yacoub M, Irani J, Dore B, Cussenot O, Fromont G. Expression of estrogen related proteins in hormone refractory prostate cancer: association with tumor progression. J Urol. 2010;184:2172–8.PubMed CrossRef 54.Platz EA, De Marzo AM. Epidemiology of inflammation and prostate cancer. J Urol. 2004;171:S36–40.PubMed CrossRef 55.Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alphaERKO and betaERKO mice. Cancer Res. 2001;61:6089–97.PubMed 56.Van Laere SJ, Van der Auwera I, Van den Eynden GG, van Dam P, Van Marck EA, Vermeulen PB, et al. NF-kappaB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br J Cancer. 2007;97:659–69.PubMed PubMedCentral CrossRef 57.Spence RD, Wisdom AJ, Cao Y, Hill HM, Mongerson CR, Stapornkul B, et al. Estrogen mediates neuroprotection and anti-inflammatory effects during EAE through ERalpha signaling on astrocytes but not through ERbeta signaling on astrocytes or neurons. J Neurosci. 2013;33:10924–33.PubMed PubMedCentral CrossRef 58.Zhang GJ, Adachi I. Serum interleukin-6 levels correlate to tumor progression and prognosis in metastatic breast carcinoma. Anticancer Res. 1999;19:1427–32.PubMed 59.Yadav A, Kumar B, Datta J, Teknos TN, Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res. 2011;9:1658–67.PubMed PubMedCentral CrossRef 60.Michalaki V, Syrigos K, Charles P, Waxman J. Serum levels of IL-6 and TNF-alpha correlate with clinicopathological features and patient survival in patients with prostate cancer. Br J Cancer. 2004;90:2312–6.PubMed PubMedCentral 61.Lou W, Ni Z, Dyer K, Tweardy DJ, Gao AC. Interleukin-6 induces prostate cancer cell growth accompanied by activation of stat3 signaling pathway. Prostate. 2000;42:239–42.PubMed CrossRef 62.Hsu CP, Chen YL, Huang CC, Chou CC, Liu CL, Hung CH, et al. Anti-interleukin-6 receptor antibody inhibits the progression in human colon carcinoma cells. Eur J Clin Invest. 2011;41:277–84.PubMed CrossRef 63.Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 2007;317:121–4.PubMed CrossRef 64.Chen M, Hsu I, Wolfe A, Radovick S, Huang K, Yu S, et al. Defects of prostate development and reproductive system in the estrogen receptor-alpha null male mice. Endocrinology. 2009;150:251–9.PubMed CrossRef
作者单位:Chiuan-Ren Yeh (1) Spencer Slavin (1) Jun Da (1) Iawen Hsu (1) Jie Luo (1) Guang-Qian Xiao (2) Jie Ding (1) Fu-Ju Chou (1) Shuyuan Yeh (1)
1. George Whipple Lab for Cancer Research, Departments of Urology and Pathology, University of Rochester Medical Center, Rochester, NY, 14642, USA 2. Department of Pathology, University of Rochester Medical Center, Rochester, NY, 14642, USA
刊物主题:Cancer Research; Oncology;
出版者:BioMed Central
ISSN:1476-4598
文摘
Background Cancer associated fibroblasts (CAF) play important roles in tumor growth that involves inflammation and epithelial cell differentiation. Early studies suggested that estrogen receptor alpha (ERα) was expressed in stromal cells in normal prostates and prostate cancer (PCa), but the detailed functions of stromal ERα in the PCa remain to be further elucidated.