Activation of estrogen receptor ESR1 and ESR2 induces proliferation of the human testicular embryonal carcinoma NT2/D1 cells

Molecular and Cellular Endocrinology - Tập 554 - Trang 111708 - 2022
Carla Macheroni1, Thaís Fabiana Gameiro Lucas1, Deborah Simão Souza1, Carolina Meloni Vicente1, Gustavo José da Silva Pereira1, Itabajara da Silva Vaz Junior2, Maria Aparecida Juliano3, Catarina Segreti Porto1
1Laboratory of Experimental Endocrinology, Department of Pharmacology, Escola Paulista de Medicina, Universidade Federal de São Paulo, Rua Pedro de Toledo 669, Vila Clementino, São Paulo, SP, 04039-032, Brazil
2Centro de Biotecnologia e Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, Av. Bento Goncalves 9500, Porto Alegre, RS, 91501-970, Brazil
3Department of Biophysics, Escola Paulista de Medicina, Universidade Federal de São Paulo, Rua Três de Maio, 100, Vila Clementino, São Paulo, SP, 04044-020, Brazil

Tài liệu tham khảo

Ajj, 2013, An alkylphenol mix promotes seminoma derived cell proliferation through an ERalpha36-mediated mechanism, PLoS One, 8, 10.1371/journal.pone.0061758 Albers, 2015, Guidelines on testicular cancer: 2015 update, Eur. Urol., 68, 1054, 10.1016/j.eururo.2015.07.044 Andersson, 2017, Insufficient antibody validation challenges oestrogen receptor beta research, Nat. Commun., 8 Bachs, 2018, Role of p27Kip1 as a transcriptional regulator, Oncotarget, 9, 26259, 10.18632/oncotarget.25447 Bartkova, 1999, D-type cyclins in adult human testis and testicular cancer: relation to cell type, proliferation, differentiation, and malignancy, J. Pathol., 187, 573, 10.1002/(SICI)1096-9896(199904)187:5<573::AID-PATH289>3.0.CO;2-H Besson, 2008, CDK inhibitors: cell cycle regulators and beyond, Dev. Cell, 14, 159, 10.1016/j.devcel.2008.01.013 Boscia, 2015, High levels of GPR30 protein in human testicular carcinoma in situ and seminomas correlate with low levels of estrogen receptor-beta and indicate a switch in estrogen responsiveness, J. Cell. Physiol., 230, 1290, 10.1002/jcp.24864 Bosl, 1997, Testicular germ-cell cancer, N. Engl. J. Med., 337, 242, 10.1056/NEJM199707243370406 Bouchard, 1999, Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27, EMBO J., 18, 5321, 10.1093/emboj/18.19.5321 Bouskine, 2009, Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor, Environ. Health Perspect., 11, 1053, 10.1289/ehp.0800367 Bouskine, 2008, Estrogens promote human testicular germ cell cancer through a membrane-mediated activation of extracellular regulated kinase and protein kinase A, Endocrinology, 149, 565, 10.1210/en.2007-1318 Bray, 2006, Trends in testicular cancer incidence and mortality in 22 European countries: continuing increases in incidence and declines in mortality, Int. J. Cancer, 118, 3099, 10.1002/ijc.21747 Caldon, 2009, Estrogen regulation of cyclin E2 requires cyclin D1 but not c-Myc, Mol. Cell Biol., 29, 4623, 10.1128/MCB.00269-09 Carreau, 2010, Oestrogens and spermatogenesis, Philos. Trans. R. Soc. Lond. B Biol. Sci., 365, 1517, 10.1098/rstb.2009.0235 Carreau, 2002, Reproductive system: aromatase and estrogens, Mol. Cell. Endocrinol., 193, 137, 10.1016/S0303-7207(02)00107-7 Chen, 2003, Roles of estrogen receptor alpha (ER alpha) in the regulation of the human Müllerian inhibitory substance (MIS) promoter, J. Med. Invest., 50, 192 Chevalier, 2021, GPER and testicular germ cell cancer, Front. Endocrinol., 11, 10.3389/fendo.2020.600404 Chevalier, 2014, Genetic variants of GPER/GPR30, a novel estrogen-related G protein receptor, are associated with human seminoma, Int. J. Mol. Sci., 15, 1574, 10.3390/ijms15011574 Chevalier, 2012, GPR30, the non-classical membrane G protein related estrogen receptor, is overexpressed in human seminoma and promotes seminoma cell proliferation, PLoS One, 7, 10.1371/journal.pone.0034672 Chieffi, 2013, Molecular biomarkers as potential targets for therapeutic strategies in human testicular germ cell tumors: an overview, J. Cell. Physiol., 228, 1641, 10.1002/jcp.24328 Chimento, 2020, Role of GPER-mediated signaling in testicular functions and tumorigenesis, Cells, 9, 2115, 10.3390/cells9092115 Chu, 2008, The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy, Nat. Rev. Cancer, 8, 253, 10.1038/nrc2347 Cooke, 2017, Estrogens in male physiology, Physiol. Rev., 97, 995, 10.1152/physrev.00018.2016 Daniel, 2014, Selective CREB-dependent cyclin expression mediated by the PI3K and MAPK pathways supports glioma cell proliferation, Oncogenesis, 3, e108, 10.1038/oncsis.2014.21 Datta, 2000, Evaluation of cyclin expression in testicular germ cell tumors: cyclin E correlates with tumor type, advanced clinical stage, and pulmonary metastasis, Mod. Pathol., 13, 667, 10.1038/modpathol.3880117 Diehl, 1998, Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization, Genes Dev., 12, 3499, 10.1101/gad.12.22.3499 Ding, 2019, Prognostic role of cyclin D2/D3 in multiple human malignant neoplasms: a systematic review and meta-analysis, Cancer Med., 8, 2717, 10.1002/cam4.2152 Esposito, 2011, Down-regulation of oestrogen receptor-beta associates with transcriptional co-regulator PATZ1 delocalization in human testicular seminomas, J. Pathol., 224, 110, 10.1002/path.2846 Facchini, 2019, Prognostic and predictive factors in testicular cancer, Eur. Rev. Med. Pharmacol. Sci., 23, 3885 Fénichel, 2019, Is testicular germ cell cancer estrogen dependent? The role of endocrine disrupting chemicals, Endocrinology, 160, 2981, 10.1210/en.2019-00486 Franco, 2011, GPR30 is overexpressed in post-puberal testicular germ cell tumors, Cancer Biol. Ther., 11, 609, 10.4161/cbt.11.6.14672 Grimmler, 2007, Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases, Cell, 128, 269, 10.1016/j.cell.2006.11.047 Guido, 2012, Estrogen receptor beta (ERβ) produces autophagy and necroptosis in human seminoma cell line through the binding of the Sp1 on the phosphatase and tensin homolog deleted from chromosome 10 (PTEN) promoter gene, Cell Cycle, 11, 2911, 10.4161/cc.21336 Heldring, 2007, Estrogen receptors: how do they signal and what are their targets, Physiol. Rev., 87, 905, 10.1152/physrev.00026.2006 Hnit, 2015, p27(Kip1) signaling: transcriptional and post-translational regulation, Int. J. Biochem. Cell Biol., 68, 9, 10.1016/j.biocel.2015.08.005 James, 2008, Differential modification of p27Kip1 controls its cyclin D-cdk4 inhibitory activity, Mol. Cell Biol., 28, 498, 10.1128/MCB.02171-06 Kukoski, 2003, p27 and cyclin E/D2 associations in testicular germ cell tumors: implications for tumorigenesis, Appl. Immunohistochem. Mol. Morphol., 11, 138, 10.1097/00129039-200306000-00008 Kumar, 2018, Analysis of cell viability by the MTT assay, Cold Spring Harb, 469 Le Cornet, 2014, Testicular cancer incidence to rise by 25% by 2025 in Europe? Model-based predictions in 40 countries using population-based registry data, Eur. J. Cancer, 50, 831, 10.1016/j.ejca.2013.11.035 Lee, 2000, Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway, Mol. Cell Biol., 20, 672, 10.1128/MCB.20.2.672-683.2000 Lombardi, 2021, Estrogen receptor signaling pathways involved in invasion and colony formation of androgen-independent prostate cancer cells PC-3, Int. J. Mol. Sci., 22, 1153, 10.3390/ijms22031153 Lucas, 2010, Expression and signaling of G protein-coupled estrogen receptor 1 (GPER) in rat sertoli cells, Biol. Reprod., 83, 307, 10.1095/biolreprod.110.084160 Lucas, 2008, 17beta-estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane, MAPK3/1 phosphorylation, and proliferation of cultured immature rat Sertoli cells, Biol. Reprod., 78, 101, 10.1095/biolreprod.107.063909 Martinez-Soria, 2018, The oncogenic transcription factor RUNX1/ETO corrupts cell cycle regulation to drive Leukemic transformation, Cancer Cell, 34, 626, 10.1016/j.ccell.2018.08.015 McIver, 2013, 2, 55 Meyers, 2001, Estrogen receptor β potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues, J. Med. Chem., 44, 4230, 10.1021/jm010254a Morishita, 2008, Pim kinases promote cell cycle progression by phosphorylating and down-regulating p27Kip1 at the transcriptional and posttranscriptional levels, Cancer Res., 68, 5076, 10.1158/0008-5472.CAN-08-0634 Nelson, 2017, Comprehensive assessment of estrogen receptor beta antibodies in cancer cell line models and tissue reveals critical limitations in reagent specificity, Mol. Cell. Endocrinol., 440, 138, 10.1016/j.mce.2016.11.016 Ou, 2011, Incomplete folding upon binding mediates Cdk4/cyclin D complex activation by tyrosine phosphorylation of inhibitor p27 protein, J. Biol. Chem., 286, 30142, 10.1074/jbc.M111.244095 Pais, 2003, Estrogen receptor-beta expression in human testicular germ cell tumors, Clin. Cancer Res., 9, 4475 Perry, 1998, Epidermal growth factor induces cyclin D1 in a human prostate cancer cell line, Prostate, 35, 117, 10.1002/(SICI)1097-0045(19980501)35:2<117::AID-PROS5>3.0.CO;2-G Pisolato, 2016, Expression and regulation of the estrogen receptors in PC-3 human prostate cancer cells, Steroids, 107, 74, 10.1016/j.steroids.2015.12.021 Rago, 2009, Identification of ERbeta1 and ERbeta2 in human seminoma, in embryonal carcinoma and in their adjacent intratubular germ cell neoplasia, Reprod. Biol. Endocrinol., 7, 56, 10.1186/1477-7827-7-56 Rago, 2011, Identification of the estrogen receptor GPER in neoplastic and non-neoplastic human testes, Reprod. Biol. Endocrinol., 9, 135, 10.1186/1477-7827-9-135 Roger, 2005, Estrogen-induced growth inhibition of human seminoma cells expressing estrogen receptor beta and aromatase, J. Mol. Endocrinol., 35, 191, 10.1677/jme.1.01704 Razavipour, 2020, p27 as a transcriptional regulator: new roles in development and cancer, Cancer Res., 80, 3451, 10.1158/0008-5472.CAN-19-3663 Saltzman, 2018, Adolescent and young adult testicular germ cell tumors: Special considerations, Adv. Urol., 31 Sarkar, 2010, Expression of cyclin D2 is an independent predictor of the development of hepatic metastasis in colorectal cancer, Colorectal Dis., 12, 316, 10.1111/j.1463-1318.2009.01829.x Schmidt, 2001, Up-regulation of cyclin-dependent kinase 4/cyclin D2 expression but down-regulation of cyclin-dependent kinase 2/cyclin E in testicular germ cell tumors, Cancer Res., 61, 4214 Sherr, 1994, G1 phase progression: cycling on cue, Cell, 79, 551, 10.1016/0092-8674(94)90540-1 Sherr, 1996, Cancer cell cycles, Science, 274, 1672, 10.1126/science.274.5293.1672 Skakkebaek, 1972, Possible carcinoma-in-situ of the testis, Lancet, 2, 516, 10.1016/S0140-6736(72)91909-5 Skakkebaek, 2016, A brief review of the link between environment and male reproductive health: Lessons from studies of testicular germ cell cancer, Horm. Res. Paediatr., 86, 240, 10.1159/000443400 Snow, 2009, Wnt pathway reprogramming during human embryonal carcinoma differentiation and potential for therapeutic targeting, BMC Cancer, 9, 383, 10.1186/1471-2407-9-383 Sonne, 2009, Analysis of gene expression profiles of microdissected cell populations indicates that testicular carcinoma in situ is an arrested gonocyte, Cancer Res., 69, 5241, 10.1158/0008-5472.CAN-08-4554 Souza, 2019, Estrogen receptors localization and signaling pathways in DU-145 human prostate cancer cells, Mol. Cell. Endocrinol., 483, 11, 10.1016/j.mce.2018.12.015 Stauffer, 2000, Pyrazole ligands: structureaffinity/activity relationships and estrogen receptor-alpha-selective agonists, J. Med. Chem., 43, 4934, 10.1021/jm000170m Takano, 1999, Cyclin D2, but not cyclin D1, overexpression closely correlates with gastric cancer progression and prognosis, J. Pathol., 189, 194, 10.1002/(SICI)1096-9896(199910)189:2<194::AID-PATH426>3.0.CO;2-P Varricchio, 2007, Inhibition of estradiol receptor/Src association and cell growth by an estradiol receptor alpha tyrosine-phosphorylated peptide, Mol. Cancer Res., 5, 1213, 10.1158/1541-7786.MCR-07-0150 Wallacides, 2012, Estrogens promote proliferation of the seminoma-like TCam-2 cell line through a GPER-dependent ERα36 induction, Mol. Cell. Endocrinol., 350, 61, 10.1016/j.mce.2011.11.021 Wu, 2012, Development, characterization, and applications of a novel estrogen receptor beta monoclonal antibody, J. Cell. Biochem., 113, 711, 10.1002/jcb.23443