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Published in: BMC Cancer 1/2018

Open Access 01-12-2018 | Research article

Expression of estrogen receptor beta correlates with adverse prognosis in resected pancreatic adenocarcinoma

Authors: Hendrik Seeliger, Ioannis Pozios, Gerald Assmann, Yue Zhao, Mario H. Müller, Thomas Knösel, Martin E. Kreis, Christiane J. Bruns

Published in: BMC Cancer | Issue 1/2018

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Abstract

Background

The relevance of estrogen receptor (ER) expression in pancreatic ductal adenocarcinoma (PDAC) is largely unknown. Clinical trials targeting ER with selective estrogen receptor modulators in pancreatic cancer did not show any benefit. Here, we analyze the impact of recently characterized ER isoform beta on survival in a cohort of patients with resected PDAC.

Methods

Eighty-four patients having undergone pancreatic resection for PDAC at a single institution were identified. Tissue microarrays were constructed of archival tumor specimens. The expression of ER beta was determined by immunohistochemistry and quantified by a system established for estrogen receptor expression in breast cancer. ER beta expression was then correlated with clinicopathological parameters, and univariate and multivariate survival analyses were performed.

Results

Nuclear expression of ER beta was found in 31% of tumors. No significant correlation was found between ER beta expression and TNM status, tumor grade, age or sex. Univariate analysis revealed nodal metastasis and the expression of ER beta as factors correlating with a shorter overall survival and disease free survival. When comparing ER beta expression in patients surviving more than 24 months with those who died from the tumor within 12 or 24 months, respectively, a significantly lower ER beta expression was found in the long term survivors. In multivariate analysis, ER beta expression was demonstrated to be an independent predictor of shorter overall survival.

Conclusions

In resected PDAC, expression of ER beta seems to correlate with poor prognosis. These data may help to identify patients who may benefit from additional systemic therapy including selective estrogen receptor modulators.
Literature
1.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.CrossRef Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.CrossRef
2.
go back to reference Kamisawa T, Wood LD, Itoi T, Takaori K. Pancreatic cancer. Lancet. 2016;388(10039):73–85.CrossRef Kamisawa T, Wood LD, Itoi T, Takaori K. Pancreatic cancer. Lancet. 2016;388(10039):73–85.CrossRef
3.
go back to reference Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. New Engl J Med. 2014;371(11):1039–49.CrossRef Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. New Engl J Med. 2014;371(11):1039–49.CrossRef
4.
go back to reference Chiaravalli M, Reni M, O'Reilly EM. Pancreatic ductal adenocarcinoma: state-of-the-art 2017 and new therapeutic strategies. Cancer Treat Rev. 2017;60:32–43.CrossRef Chiaravalli M, Reni M, O'Reilly EM. Pancreatic ductal adenocarcinoma: state-of-the-art 2017 and new therapeutic strategies. Cancer Treat Rev. 2017;60:32–43.CrossRef
5.
go back to reference Ottaiano A, Capozzi M, De Divitiis C, De Stefano A, Botti G, Avallone A, Tafuto S. Gemcitabine mono-therapy versus gemcitabine plus targeted therapy in advanced pancreatic cancer: a meta-analysis of randomized phase III trials. Acta Oncol. 2017;56(3):377–83.CrossRef Ottaiano A, Capozzi M, De Divitiis C, De Stefano A, Botti G, Avallone A, Tafuto S. Gemcitabine mono-therapy versus gemcitabine plus targeted therapy in advanced pancreatic cancer: a meta-analysis of randomized phase III trials. Acta Oncol. 2017;56(3):377–83.CrossRef
6.
go back to reference Campbell-Thompson M, Lynch IJ, Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res. 2001;61(2):632–40.PubMed Campbell-Thompson M, Lynch IJ, Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res. 2001;61(2):632–40.PubMed
7.
go back to reference Martineti V, Picariello L, Tognarini I, Carbonell Sala S, Gozzini A, Azzari C, Mavilia C, Tanini A, Falchetti A, Fiorelli G, et al. ERbeta is a potent inhibitor of cell proliferation in the HCT8 human colon cancer cell line through regulation of cell cycle components. Endocr Relat Cancer. 2005;12(2):455–69.CrossRef Martineti V, Picariello L, Tognarini I, Carbonell Sala S, Gozzini A, Azzari C, Mavilia C, Tanini A, Falchetti A, Fiorelli G, et al. ERbeta is a potent inhibitor of cell proliferation in the HCT8 human colon cancer cell line through regulation of cell cycle components. Endocr Relat Cancer. 2005;12(2):455–69.CrossRef
8.
go back to reference Satake M, Sawai H, Go VL, Satake K, Reber HA, Hines OJ, Eibl G. Estrogen receptors in pancreatic tumors. Pancreas. 2006;33(2):119–27.CrossRef Satake M, Sawai H, Go VL, Satake K, Reber HA, Hines OJ, Eibl G. Estrogen receptors in pancreatic tumors. Pancreas. 2006;33(2):119–27.CrossRef
9.
go back to reference Skliris GP, Leygue E, Curtis-Snell L, Watson PH, Murphy LC. Expression of oestrogen receptor-beta in oestrogen receptor-alpha negative human breast tumours. Br J Cancer. 2006;95(5):616–26.CrossRef Skliris GP, Leygue E, Curtis-Snell L, Watson PH, Murphy LC. Expression of oestrogen receptor-beta in oestrogen receptor-alpha negative human breast tumours. Br J Cancer. 2006;95(5):616–26.CrossRef
10.
go back to reference Marquez-Garban DC, Chen HW, Fishbein MC, Goodglick L, Pietras RJ. Estrogen receptor signaling pathways in human non-small cell lung cancer. Steroids. 2007;72(2):135–43.CrossRef Marquez-Garban DC, Chen HW, Fishbein MC, Goodglick L, Pietras RJ. Estrogen receptor signaling pathways in human non-small cell lung cancer. Steroids. 2007;72(2):135–43.CrossRef
11.
go back to reference Greenberg JA, Somme S, Russnes HE, Durbin AD, Malkin D. The estrogen receptor pathway in rhabdomyosarcoma: a role for estrogen receptor-beta in proliferation and response to the antiestrogen 4’OH-tamoxifen. Cancer Res. 2008;68(9):3476–85.CrossRef Greenberg JA, Somme S, Russnes HE, Durbin AD, Malkin D. The estrogen receptor pathway in rhabdomyosarcoma: a role for estrogen receptor-beta in proliferation and response to the antiestrogen 4’OH-tamoxifen. Cancer Res. 2008;68(9):3476–85.CrossRef
12.
go back to reference Taylor OM, Benson EA, McMahon MJ. Clinical trial of tamoxifen in patients with irresectable pancreatic adenocarcinoma. The Yorkshire Gastrointestinal Tumour Group. Br J Surg. 1993;80(3):384–6.CrossRef Taylor OM, Benson EA, McMahon MJ. Clinical trial of tamoxifen in patients with irresectable pancreatic adenocarcinoma. The Yorkshire Gastrointestinal Tumour Group. Br J Surg. 1993;80(3):384–6.CrossRef
13.
go back to reference Tomao S, Romiti A, Massidda B, Ionta MT, Farris A, Zullo A, Brescia A, Santuari L, Frati L. A phase II study of gemcitabine and tamoxifen in advanced pancreatic cancer. Anticancer Res. 2002;22(4):2361–4.PubMed Tomao S, Romiti A, Massidda B, Ionta MT, Farris A, Zullo A, Brescia A, Santuari L, Frati L. A phase II study of gemcitabine and tamoxifen in advanced pancreatic cancer. Anticancer Res. 2002;22(4):2361–4.PubMed
14.
go back to reference Wong A, Chan A. Survival benefit of tamoxifen therapy in adenocarcinoma of pancreas. A case-control study. Cancer. 1993;71(7):2200–3.CrossRef Wong A, Chan A. Survival benefit of tamoxifen therapy in adenocarcinoma of pancreas. A case-control study. Cancer. 1993;71(7):2200–3.CrossRef
15.
go back to reference Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 1996;392(1):49–53.CrossRef Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 1996;392(1):49–53.CrossRef
16.
go back to reference Kuiper GG, Gustafsson JA. The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett. 1997;410(1):87–90.CrossRef Kuiper GG, Gustafsson JA. The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett. 1997;410(1):87–90.CrossRef
17.
go back to reference Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, Scanlan TS. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 1997;277(5331):1508–10.CrossRef Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, Scanlan TS. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 1997;277(5331):1508–10.CrossRef
18.
go back to reference Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997;138(3):863–70.CrossRef Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997;138(3):863–70.CrossRef
19.
go back to reference Gruvberger-Saal SK, Bendahl PO, Saal LH, Laakso M, Hegardt C, Eden P, Peterson C, Malmstrom P, Isola J, Borg A, et al. Estrogen receptor beta expression is associated with tamoxifen response in ERalpha-negative breast carcinoma. Clin Cancer Res. 2007;13(7):1987–94.CrossRef Gruvberger-Saal SK, Bendahl PO, Saal LH, Laakso M, Hegardt C, Eden P, Peterson C, Malmstrom P, Isola J, Borg A, et al. Estrogen receptor beta expression is associated with tamoxifen response in ERalpha-negative breast carcinoma. Clin Cancer Res. 2007;13(7):1987–94.CrossRef
20.
go back to reference Hopp TA, Weiss HL, Parra IS, Cui Y, Osborne CK, Fuqua SA. Low levels of estrogen receptor beta protein predict resistance to tamoxifen therapy in breast cancer. Clin Cancer Res. 2004;10(22):7490–9.CrossRef Hopp TA, Weiss HL, Parra IS, Cui Y, Osborne CK, Fuqua SA. Low levels of estrogen receptor beta protein predict resistance to tamoxifen therapy in breast cancer. Clin Cancer Res. 2004;10(22):7490–9.CrossRef
21.
go back to reference Skjefstad K, Grindstad T, Khanehkenari MR, Richardsen E, Donnem T, Kilvaer T, Andersen S, Bremnes RM, Busund LT, Al-Saad S. Prognostic relevance of estrogen receptor alpha, beta and aromatase expression in non-small cell lung cancer. Steroids. 2016;113:5–13.CrossRef Skjefstad K, Grindstad T, Khanehkenari MR, Richardsen E, Donnem T, Kilvaer T, Andersen S, Bremnes RM, Busund LT, Al-Saad S. Prognostic relevance of estrogen receptor alpha, beta and aromatase expression in non-small cell lung cancer. Steroids. 2016;113:5–13.CrossRef
22.
go back to reference Ma L, Zhan P, Liu Y, Zhou Z, Zhu Q, Miu Y, Wang X, Jin J, Li Q, Lv T, et al. Prognostic value of the expression of estrogen receptor beta in patients with non-small cell lung cancer: a meta-analysis. Transl Lung Cancer Res. 2016;5(2):202–7.CrossRef Ma L, Zhan P, Liu Y, Zhou Z, Zhu Q, Miu Y, Wang X, Jin J, Li Q, Lv T, et al. Prognostic value of the expression of estrogen receptor beta in patients with non-small cell lung cancer: a meta-analysis. Transl Lung Cancer Res. 2016;5(2):202–7.CrossRef
23.
go back to reference Song RX, Zhang Z, Chen Y, Bao Y, Santen RJ. Estrogen signaling via a linear pathway involving insulin-like growth factor I receptor, matrix metalloproteinases, and epidermal growth factor receptor to activate mitogen-activated protein kinase in MCF-7 breast cancer cells. Endocrinology. 2007;148(8):4091–101.CrossRef Song RX, Zhang Z, Chen Y, Bao Y, Santen RJ. Estrogen signaling via a linear pathway involving insulin-like growth factor I receptor, matrix metalloproteinases, and epidermal growth factor receptor to activate mitogen-activated protein kinase in MCF-7 breast cancer cells. Endocrinology. 2007;148(8):4091–101.CrossRef
24.
go back to reference Konduri S, Schwarz RE. Estrogen receptor beta/alpha ratio predicts response of pancreatic cancer cells to estrogens and phytoestrogens. J Surg Res. 2007;140(1):55–66.CrossRef Konduri S, Schwarz RE. Estrogen receptor beta/alpha ratio predicts response of pancreatic cancer cells to estrogens and phytoestrogens. J Surg Res. 2007;140(1):55–66.CrossRef
25.
go back to reference Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998;4(7):844–7.CrossRef Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998;4(7):844–7.CrossRef
26.
go back to reference Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe. 1987;8(3):138–40.PubMed Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe. 1987;8(3):138–40.PubMed
27.
go back to reference Ollayos CW, Riordan GP, Rushin JM. Estrogen receptor detection in paraffin sections of adenocarcinoma of the colon, pancreas, and lung. Arch Pathol Lab Med. 1994;118(6):630–2.PubMed Ollayos CW, Riordan GP, Rushin JM. Estrogen receptor detection in paraffin sections of adenocarcinoma of the colon, pancreas, and lung. Arch Pathol Lab Med. 1994;118(6):630–2.PubMed
28.
go back to reference Yeh TS, Jan YY, Chiu CT, Ho YB, Chen TC, Lee KF, Chan KM, Hsu JC, Hwang TL, Chen MF. Characterisation of oestrogen receptor, progesterone receptor, trefoil factor 1, and epidermal growth factor and its receptor in pancreatic cystic neoplasms and pancreatic ductal adenocarcinoma. Gut. 2002;51(5):712–6.CrossRef Yeh TS, Jan YY, Chiu CT, Ho YB, Chen TC, Lee KF, Chan KM, Hsu JC, Hwang TL, Chen MF. Characterisation of oestrogen receptor, progesterone receptor, trefoil factor 1, and epidermal growth factor and its receptor in pancreatic cystic neoplasms and pancreatic ductal adenocarcinoma. Gut. 2002;51(5):712–6.CrossRef
29.
go back to reference Iwao K, Miyoshi Y, Ooka M, Ishikawa O, Ohigashi H, Kasugai T, Egawa C, Noguchi S. Quantitative analysis of estrogen receptor-alpha and -beta messenger RNA expression in human pancreatic cancers by real-time polymerase chain reaction. Cancer Lett. 2001;170(1):91–7.CrossRef Iwao K, Miyoshi Y, Ooka M, Ishikawa O, Ohigashi H, Kasugai T, Egawa C, Noguchi S. Quantitative analysis of estrogen receptor-alpha and -beta messenger RNA expression in human pancreatic cancers by real-time polymerase chain reaction. Cancer Lett. 2001;170(1):91–7.CrossRef
30.
go back to reference Singh S, Baker PR, Poulsom R, Wright NA, Sheppard MC, Langman MJ, Neoptolemos JP. Expression of oestrogen receptor and oestrogen-inducible genes in pancreatic cancer. Br J Surg. 1997;84(8):1085–9.CrossRef Singh S, Baker PR, Poulsom R, Wright NA, Sheppard MC, Langman MJ, Neoptolemos JP. Expression of oestrogen receptor and oestrogen-inducible genes in pancreatic cancer. Br J Surg. 1997;84(8):1085–9.CrossRef
31.
go back to reference Izumo A, Yamaguchi K, Eguchi T, Nishiyama K, Yamamoto H, Yonemasu H, Yao T, Tanaka M, Tsuneyoshi M. Mucinous cystic tumor of the pancreas: immunohistochemical assessment of “ovarian-type stroma”. Oncol Rep. 2003;10(3):515–25.PubMed Izumo A, Yamaguchi K, Eguchi T, Nishiyama K, Yamamoto H, Yonemasu H, Yao T, Tanaka M, Tsuneyoshi M. Mucinous cystic tumor of the pancreas: immunohistochemical assessment of “ovarian-type stroma”. Oncol Rep. 2003;10(3):515–25.PubMed
32.
go back to reference Thompson LD, Becker RC, Przygodzki RM, Adair CF, Heffess CS. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low-grade malignant potential) of the pancreas: a clinicopathologic study of 130 cases. Am J Surg Pathol. 1999;23(1):1–16.CrossRef Thompson LD, Becker RC, Przygodzki RM, Adair CF, Heffess CS. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low-grade malignant potential) of the pancreas: a clinicopathologic study of 130 cases. Am J Surg Pathol. 1999;23(1):1–16.CrossRef
33.
go back to reference Arpino G, Wiechmann L, Osborne CK, Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev. 2008;29(2):217–33.CrossRef Arpino G, Wiechmann L, Osborne CK, Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev. 2008;29(2):217–33.CrossRef
34.
go back to reference Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem. 2001;276(13):9817–24.CrossRef Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem. 2001;276(13):9817–24.CrossRef
35.
go back to reference Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007;87(3):905–31.CrossRef Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007;87(3):905–31.CrossRef
36.
go back to reference Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene. 2004;23(48):7979–89.CrossRef Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene. 2004;23(48):7979–89.CrossRef
37.
go back to reference Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I, Sotiropoulou-Bonikou G, Papavassiliou AG. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour’s dedifferentiation. Eur J Cancer. 2003;39(9):1251–8.CrossRef Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I, Sotiropoulou-Bonikou G, Papavassiliou AG. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour’s dedifferentiation. Eur J Cancer. 2003;39(9):1251–8.CrossRef
38.
go back to reference Nozoe T, Oyama T, Takenoyama M, Hanagiri T, Sugio K, Yasumoto K. Significance of immunohistochemical expression of estrogen receptors alpha and beta in squamous cell carcinoma of the esophagus. Clin Cancer Res. 2007;13(14):4046–50.CrossRef Nozoe T, Oyama T, Takenoyama M, Hanagiri T, Sugio K, Yasumoto K. Significance of immunohistochemical expression of estrogen receptors alpha and beta in squamous cell carcinoma of the esophagus. Clin Cancer Res. 2007;13(14):4046–50.CrossRef
39.
go back to reference Slattery ML, Sweeney C, Murtaugh M, Ma KN, Wolff RK, Potter JD, Caan BJ, Samowitz W. Associations between ERalpha, ERbeta, and AR genotypes and colon and rectal cancer. Cancer Epidemiol Biomark Prev. 2005;14(12):2936–42.CrossRef Slattery ML, Sweeney C, Murtaugh M, Ma KN, Wolff RK, Potter JD, Caan BJ, Samowitz W. Associations between ERalpha, ERbeta, and AR genotypes and colon and rectal cancer. Cancer Epidemiol Biomark Prev. 2005;14(12):2936–42.CrossRef
40.
go back to reference Caiazza F, Galluzzo P, Lorenzetti S, Marino M. 17Beta-estradiol induces ERbeta up-regulation via p38/MAPK activation in colon cancer cells. Biochem Biophys Res Commun. 2007;359(1):102–7.CrossRef Caiazza F, Galluzzo P, Lorenzetti S, Marino M. 17Beta-estradiol induces ERbeta up-regulation via p38/MAPK activation in colon cancer cells. Biochem Biophys Res Commun. 2007;359(1):102–7.CrossRef
41.
go back to reference Kalayarasan R, Ananthakrishnan N, Kate V, Basu D. Estrogen and progesterone receptors in esophageal carcinoma. Dis Esophagus. 2008;21(4):298–303.CrossRef Kalayarasan R, Ananthakrishnan N, Kate V, Basu D. Estrogen and progesterone receptors in esophageal carcinoma. Dis Esophagus. 2008;21(4):298–303.CrossRef
42.
go back to reference Verbeke CS, Menon KV. Variability in reporting resection margin status in pancreatic cancer. Ann Surg. 2008;247(4):716–7.CrossRef Verbeke CS, Menon KV. Variability in reporting resection margin status in pancreatic cancer. Ann Surg. 2008;247(4):716–7.CrossRef
43.
go back to reference Xu CY, Guo JL, Jiang ZN, Xie SD, Shen JG, Shen JY, Wang LB. Prognostic role of estrogen receptor alpha and estrogen receptor beta in gastric cancer. Ann Surg Oncol. 2010;17(9):2503–9.CrossRef Xu CY, Guo JL, Jiang ZN, Xie SD, Shen JG, Shen JY, Wang LB. Prognostic role of estrogen receptor alpha and estrogen receptor beta in gastric cancer. Ann Surg Oncol. 2010;17(9):2503–9.CrossRef
44.
go back to reference Rudolph A, Toth C, Hoffmeister M, Roth W, Herpel E, Jansen L, Marx A, Brenner H, Chang-Claude J. Expression of oestrogen receptor beta and prognosis of colorectal cancer. Br J Cancer. 2012;107(5):831–9.CrossRef Rudolph A, Toth C, Hoffmeister M, Roth W, Herpel E, Jansen L, Marx A, Brenner H, Chang-Claude J. Expression of oestrogen receptor beta and prognosis of colorectal cancer. Br J Cancer. 2012;107(5):831–9.CrossRef
45.
go back to reference Iavarone M, Lampertico P, Seletti C, Francesca Donato M, Ronchi G, del Ninno E, Colombo M. The clinical and pathogenetic significance of estrogen receptor-beta expression in chronic liver diseases and liver carcinoma. Cancer. 2003;98(3):529–34.CrossRef Iavarone M, Lampertico P, Seletti C, Francesca Donato M, Ronchi G, del Ninno E, Colombo M. The clinical and pathogenetic significance of estrogen receptor-beta expression in chronic liver diseases and liver carcinoma. Cancer. 2003;98(3):529–34.CrossRef
46.
go back to reference Villa E, Colantoni A, Camma C, Grottola A, Buttafoco P, Gelmini R, Ferretti I, Manenti F. Estrogen receptor classification for hepatocellular carcinoma: comparison with clinical staging systems. J Clin Oncol. 2003;21(3):441–6.CrossRef Villa E, Colantoni A, Camma C, Grottola A, Buttafoco P, Gelmini R, Ferretti I, Manenti F. Estrogen receptor classification for hepatocellular carcinoma: comparison with clinical staging systems. J Clin Oncol. 2003;21(3):441–6.CrossRef
47.
go back to reference Giroux V, Lemay F, Bernatchez G, Robitaille Y, Carrier JC. Estrogen receptor beta deficiency enhances small intestinal tumorigenesis in ApcMin/+ mice. Int J Cancer. 2008;123(2):303–11.CrossRef Giroux V, Lemay F, Bernatchez G, Robitaille Y, Carrier JC. Estrogen receptor beta deficiency enhances small intestinal tumorigenesis in ApcMin/+ mice. Int J Cancer. 2008;123(2):303–11.CrossRef
48.
go back to reference Fan S, Liao Y, Liu C, Huang Q, Liang H, Ai B, Fu S, Zhou S. Estrogen promotes tumor metastasis via estrogen receptor beta-mediated regulation of matrix-metalloproteinase-2 in non-small cell lung cancer. Oncotarget. 2017;8(34):56443–59.CrossRef Fan S, Liao Y, Liu C, Huang Q, Liang H, Ai B, Fu S, Zhou S. Estrogen promotes tumor metastasis via estrogen receptor beta-mediated regulation of matrix-metalloproteinase-2 in non-small cell lung cancer. Oncotarget. 2017;8(34):56443–59.CrossRef
49.
go back to reference Niv Y. Estrogen receptor beta expression and colorectal cancer: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2015;27(12):1438–42.CrossRef Niv Y. Estrogen receptor beta expression and colorectal cancer: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2015;27(12):1438–42.CrossRef
50.
go back to reference Stevanato Filho PR, Aguiar Junior S, Begnami MD, Ferreira FO, Nakagawa WT, Spencer R, Bezerra TS, Boggiss PE, Lopes A. Estrogen receptor beta as a prognostic marker of tumor progression in colorectal Cancer with familial adenomatous polyposis and sporadic polyps. Pathol Oncol Res. 2017;24(3):533–40.CrossRef Stevanato Filho PR, Aguiar Junior S, Begnami MD, Ferreira FO, Nakagawa WT, Spencer R, Bezerra TS, Boggiss PE, Lopes A. Estrogen receptor beta as a prognostic marker of tumor progression in colorectal Cancer with familial adenomatous polyposis and sporadic polyps. Pathol Oncol Res. 2017;24(3):533–40.CrossRef
51.
go back to reference Topi G, Ehrnstrom R, Jirstrom K, Palmquist I, Lydrup ML, Sjolander A. Association of the oestrogen receptor beta with hormone status and prognosis in a cohort of female patients with colorectal cancer. Eur J Cancer. 2017;83:279–89.CrossRef Topi G, Ehrnstrom R, Jirstrom K, Palmquist I, Lydrup ML, Sjolander A. Association of the oestrogen receptor beta with hormone status and prognosis in a cohort of female patients with colorectal cancer. Eur J Cancer. 2017;83:279–89.CrossRef
52.
go back to reference Miller MM, McMullen PD, Andersen ME, Clewell RA. Multiple receptors shape the estrogen response pathway and are critical considerations for the future of in vitro-based risk assessment efforts. Crit Rev Toxicol. 2017;47(7):564–80.CrossRef Miller MM, McMullen PD, Andersen ME, Clewell RA. Multiple receptors shape the estrogen response pathway and are critical considerations for the future of in vitro-based risk assessment efforts. Crit Rev Toxicol. 2017;47(7):564–80.CrossRef
53.
go back to reference Assifi MM, Lu X, Eibl G, Reber HA, Li G, Hines OJ. Neoadjuvant therapy in pancreatic adenocarcinoma: a meta-analysis of phase II trials. Surgery. 2011;150(3):476–3.CrossRef Assifi MM, Lu X, Eibl G, Reber HA, Li G, Hines OJ. Neoadjuvant therapy in pancreatic adenocarcinoma: a meta-analysis of phase II trials. Surgery. 2011;150(3):476–3.CrossRef
54.
go back to reference Torlakovic E, Lilleby W, Berner A, Torlakovic G, Chibbar R, Furre T, Fossa SD. Differential expression of steroid receptors in prostate tissues before and after radiation therapy for prostatic adenocarcinoma. Int J Cancer. 2005;117(3):381–6.CrossRef Torlakovic E, Lilleby W, Berner A, Torlakovic G, Chibbar R, Furre T, Fossa SD. Differential expression of steroid receptors in prostate tissues before and after radiation therapy for prostatic adenocarcinoma. Int J Cancer. 2005;117(3):381–6.CrossRef
Metadata
Title
Expression of estrogen receptor beta correlates with adverse prognosis in resected pancreatic adenocarcinoma
Authors
Hendrik Seeliger
Ioannis Pozios
Gerald Assmann
Yue Zhao
Mario H. Müller
Thomas Knösel
Martin E. Kreis
Christiane J. Bruns
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2018
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-018-4973-6

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