How does estrogen work on autophagy?

References

• Cheng Y, Ren X, Hait WN, et al. Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol Rev. 2013;65:1162–1197.
   PubMed Web of Science ®Google Scholar
• Levy JMM, Towers CG, Thorburn A. Targeting autophagy in cancer. Nat Rev Cancer. 2017;17:528–542.
   PubMed Web of Science ®Google Scholar
• Mei Y, Thompson MD, Cohen RA, et al. Autophagy and oxidative stress in cardiovascular diseases. Biochim Biophys Acta. 2015;1852:243–251.
   PubMed Web of Science ®Google Scholar
• Jia M, Dahlman-Wright K, Gustafsson J-Å. Estrogen receptor alpha and beta in health and disease. Best Pract Res Clin Endocrinol Metab. 2015;29:557–568.
   PubMed Web of Science ®Google Scholar
• Meyer MR, Barton M. Estrogens and coronary artery disease: new clinical perspectives. Adv Pharmacol. 2016;77:307–360.
   PubMedGoogle Scholar
• Schiebler TH, Danner KG. The effect of sex hormones on the proximal tubules in the rat kidney. Cell Tissue Res. 1978;192:527–549.
   PubMed Web of Science ®Google Scholar
• Park J, Shin H, Song H, et al. Autophagic regulation in steroid hormone-responsive systems. Steroids. 2016;115:177–181.
   PubMed Web of Science ®Google Scholar
• Totta P, Busonero C, Leone S, et al. Dynamin II is required for 17β-estradiol signaling and autophagy-based ERα degradation. Sci Res. 2016;6:23727.
   Google Scholar
• Lahm T, Petrache I. LC3 as a potential therapeutic target in hypoxia-induced pulmonary hypertension. Autophagy. 2012;8:1146–1147.
   PubMed Web of Science ®Google Scholar
• Lahm T, Albrecht M, Fisher AJ, et al. 17β-Estradiol attenuates hypoxic pulmonary hypertension via estrogen receptor-mediated effects. Am J Respir Crit Care Med. 2012;185:965–980.
   PubMed Web of Science ®Google Scholar
• Kimura A, Ishida Y, Nosaka M, et al. Exaggerated arsenic nephrotoxicity in female mice through estrogen-dependent impairments in the autophagic flux. Toxicology. 2016;339:9–18.
   PubMed Web of Science ®Google Scholar
• Yang YH, Chen K, Li B, et al. Estradiol inhibits osteoblast apoptosis via promotion of autophagy through the ER-ERK-mTOR pathway. Apoptosis. 2013;18:1363–1375.
   PubMed Web of Science ®Google Scholar
• Brasseur K, Leblanc V, Fabi F, et al. ERα-targeted therapy in ovarian cancer cells by a novel estradiol-platinum(II) hybrid. Endocrinology. 2013;154:2281–2295.
   PubMed Web of Science ®Google Scholar
• Li XZ, Sui C-Y, Chen Q, et al. The effects and mechanism of estrogen on rats with Parkinson’s disease in different age groups. Am J Transl Res. 2016;8:4134–4146.
   PubMed Web of Science ®Google Scholar
• Chen KC, Lin C-M, Huang C-J, et al. Dual roles of 17-β estradiol in estrogen receptor-dependent growth inhibition in renal cell carcinoma. Cancer Genomics Proteomics. 2016;13:219–230.
   PubMed Web of Science ®Google Scholar
• Guido C, Panza S, Santoro M, et al. 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. 2012;11:2911–2921.
   PubMed Web of Science ®Google Scholar
• Hsieh DJ, Kuo -W-W, Lai Y-P, et al. 17β-Estradiol and/or estrogen receptor β attenuate the autophagic and apoptotic effects induced by prolonged hypoxia through HIF-1α-Mediated BNIP3 and IGFBP-3 signaling blockage. Cell Physiol Biochem. 2015;36:274–284.
   PubMed Web of Science ®Google Scholar
• Wang F, Xiao J, Shen Y, et al. Estrogen protects cardiomyocytes against lipopolysaccharide by inhibiting autophagy. Mol Med Rep. 2014;10:1509–1512.
   PubMed Web of Science ®Google Scholar
• Lin CW, Chen B, Huang K-L, et al. Inhibition of autophagy by estradiol promotes locomotor recovery after spinal cord injury in rats. Neurosci Bull. 2016;32:137–144.
   PubMed Web of Science ®Google Scholar
• Yang Y, Zheng X, Li B, et al. Increased activity of osteocyte autophagy in ovariectomized rats and its correlation with oxidative stress status and bone loss. Biochem Biophys Res Commun. 2014;451:86–92.
   PubMed Web of Science ®Google Scholar
• Yu, X., Luo A, Liu Y, et al. MiR-214 increases the sensitivity of breast cancer cells to tamoxifen and fulvestrant through inhibition of autophagy. Mol Cancer. 2015;14:208.
   PubMed Web of Science ®Google Scholar
• Yu X, Li R, Shi W, et al. Silencing of MicroRNA-21 confers the sensitivity to tamoxifen and fulvestrant by enhancing autophagic cell death through inhibition of the PI3K-AKT-mTOR pathway in breast cancer cells. Biomed Pharmacother. 2016;77:37–44.
   PubMed Web of Science ®Google Scholar
• Pawlik, A., Słomińska-Wojewódzka M, Herman-Antosiewicz A. Sensitization of estrogen receptor-positive breast cancer cell lines to 4-hydroxytamoxifen by isothiocyanates present in cruciferous plants. Eur J Nutr. 2016;55:1165–1180.
   PubMed Web of Science ®Google Scholar
• Duan L, Danzer B, Levenson VV, et al. Critical roles for nitric oxide and ERK in the completion of prosurvival autophagy in 4OHTAM-treated estrogen receptor-positive breast cancer cells. Cancer Lett. 2014;353:290–300.
   PubMed Web of Science ®Google Scholar
• Kim, H.S., Tian L, Jung M, et al. Downregulation of choline kinase-alpha enhances autophagy in tamoxifen-resistant breast cancer cells. PloS one. 2015;10:e0141110.
   PubMed Web of Science ®Google Scholar
• Wu ST, Sun G-H, Cha T-L, et al. CSC-3436 switched tamoxifen-induced autophagy to apoptosis through the inhibition of AMPK/mTOR pathway. J Biomed Sci. 2016;23:60.
   PubMed Web of Science ®Google Scholar
• Liu ZR, Song Y, Wan L-H, et al. Over-expression of miR-451a can enhance the sensitivity of breast cancer cells to tamoxifen by regulating 14-3-3ζ, estrogen receptor α, and autophagy. Life Sci. 2016;149:104–113.
   PubMed Web of Science ®Google Scholar
• Nagelkerke A, Sieuwerts AM, Bussink J, et al. LAMP3 is involved in tamoxifen resistance in breast cancer cells through the modulation of autophagy. Endocr Relat Cancer. 2014;21:101–112.
   PubMed Web of Science ®Google Scholar
• Kim DE, Kim Y, Cho D-H, et al. Raloxifene induces autophagy-dependent cell death in breast cancer cells via the activation of AMP-activated protein kinase. Mol Cells. 2015;38:138–144.
   PubMed Web of Science ®Google Scholar
• Ruddy SC, Lau R, Cabrita MA, et al. Preferential estrogen receptor β ligands reduce Bcl-2 expression in hormone-resistant breast cancer cells to increase autophagy. Mol Cancer Ther. 2014;13:1882–1893.
   PubMed Web of Science ®Google Scholar
• Prietsch RF, Monte LG, Da Silva FA, et al. Genistein induces apoptosis and autophagy in human breast MCF-7 cells by modulating the expression of proapoptotic factors and oxidative stress enzymes. Mol Cell Biochem. 2014;390:235–242.
   PubMed Web of Science ®Google Scholar
• Alayev A, Berger SM, Kramer MY, et al. The combination of rapamycin and resveratrol blocks autophagy and induces apoptosis in breast cancer cells. J Cell Biochem. 2015;116:450–457.
   PubMed Web of Science ®Google Scholar
• Turan B, Tuncay E, Vassort G. Resveratrol and diabetic cardiac function: focus on recent in vitro and in vivo studies. J Bioenerg Biomembr. 2012;44:281–296.
   PubMed Web of Science ®Google Scholar
• Zhang X, Xu W, Su J, et al. The prosurvival role of autophagy in resveratrol-induced cytotoxicity in GH3 cells. Int J Mol Med. 2014;33:987–993.
   PubMed Web of Science ®Google Scholar
• Graham CD, Kaza N, Klocke BJ, et al. Tamoxifen induces cytotoxic autophagy in glioblastoma. J Neuropathol Exp Neurol. 2016;75:946–954.
   PubMed Web of Science ®Google Scholar
• Bai LY, Weng J-R, Hu J-L, et al. G15, a GPR30 antagonist, induces apoptosis and autophagy in human oral squamous carcinoma cells. Chem Biol Interact. 2013;206:375–384.
   PubMed Web of Science ®Google Scholar
• Bravo D, Shogren KL, Zuo D, et al. 2-Methoxyestradiol-Mediated Induction of Frzb contributes to cell death and autophagy in MG63 osteosarcoma cells. J Cell Biochem. 2017;118:1497–1504.
   PubMed Web of Science ®Google Scholar
• Li L, Li X, Han X, et al. An ovarian cancer model with positive ER: reversion of ER antagonist resistance by Src blockade. Oncol Rep. 2014;32:943–950.
   PubMed Web of Science ®Google Scholar
• Simpkins F, Hevia-Paez P, Sun J, et al. Src Inhibition with saracatinib reverses fulvestrant resistance in ER-positive ovarian cancer models in vitro and in vivo. Clin Cancer Res. 2012;18:5911–5923.
   PubMed Web of Science ®Google Scholar
• Dittmar, A.J., Drozda AA, Blader IJ. Drug repurposing screening identifies novel compounds that effectively inhibit toxoplasma gondii growth. mSphere. 2016;1:e00042–15.
   PubMed Web of Science ®Google Scholar
• Klionsky, D.J., Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
   PubMed Web of Science ®Google Scholar
• Luo H, Liu M, Luo S, et al. Dynamic monitoring of GPER-mediated estrogenic effects in breast cancer associated fibroblasts: an alternative role of estrogen in mammary carcinoma development. Steroids. 2016;112:1–11.
   PubMed Web of Science ®Google Scholar
• Carmeci C, Thompson DA, Ring HZ, et al. Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics. 1997;45:607–617.
   PubMed Web of Science ®Google Scholar
• Nilsson S, Gustafsson JA. Estrogen receptors: therapies targeted to receptor subtypes. Clin Pharmacol Ther. 2011;89:44–55.
   PubMed Web of Science ®Google Scholar
• Matsuyama S, Ohkura Y, Eguchi H, et al. Estrogen receptor beta is expressed in human stomach adenocarcinoma. J Cancer Res Clin Oncol. 2002;128:319–324.
   PubMed Web of Science ®Google Scholar
• Filardo E, Quinn J, Pang Y, et al. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology. 2007;148:3236–3245.
   PubMed Web of Science ®Google Scholar
• Thomas P, Pang Y, Filardo EJ, et al. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology. 2005;146:624–632.
   PubMed Web of Science ®Google Scholar
• Razandi M, Alton G, Pedram A, et al. Identification of a structural determinant necessary for the localization and function of estrogen receptor alpha at the plasma membrane. Mol Cell Biol. 2003;23:1633–1646.
   PubMed Web of Science ®Google Scholar
• Otto C, Rohde-Schulz B, Schwarz G, et al. G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology. 2008;149:4846–4856.
   PubMed Web of Science ®Google Scholar
• Orshal JM, Khalil RA. Gender, sex hormones, and vascular tone. Am J Physiol Regul Integr Comp Physiol. 2004;286:R233–249.
   PubMed Web of Science ®Google Scholar
• He H, Feng Y-S, Zang L-H, et al. Nitric oxide induces apoptosis and autophagy; autophagy down-regulates NO synthesis in physalin A-treated A375-S2 human melanoma cells. Food and Chem Toxicol. 2014;71:128–135.
   PubMed Web of Science ®Google Scholar
• Solakidi S, Psarra A-MG, Sekeris CE. Differential subcellular distribution of estrogen receptor isoforms: localization of ERalpha in the nucleoli and ERbeta in the mitochondria of human osteosarcoma SaOS-2 and hepatocarcinoma HepG2 cell lines. Biochim Biophys Acta. 2005;1745:382–392.
   PubMed Web of Science ®Google Scholar
• Solakidi S, Psarra A-MG, Sekeris CE. Differential distribution of glucocorticoid and estrogen receptor isoforms: localization of GRbeta and ERalpha in nucleoli and GRalpha and ERbeta in the mitochondria of human osteosarcoma SaOS-2 and hepatocarcinoma HepG2 cell lines. J Musculoskelet Neuronal Interact. 2007;7:240–245.
   PubMedGoogle Scholar
• Yang SH, Liu R, Perez EJ, et al. Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U S A. 2004;101:4130–4135.
   PubMed Web of Science ®Google Scholar
• Chen JQ, Delannoy M, Cooke C, et al. Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am J Physiol Endocrinol Metab. 2004;286:E1011–1022.
   PubMed Web of Science ®Google Scholar
• Chen JQ, Eshete M, Alworth WL, et al. Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors alpha and beta to human mitochondrial DNA estrogen response elements. J Cell Biochem. 2004;93:358–373.
   PubMed Web of Science ®Google Scholar
• Chen JQ, Russo PA, Cooke C, et al. ERbeta shifts from mitochondria to nucleus during estrogen-induced neoplastic transformation of human breast epithelial cells and is involved in estrogen-induced synthesis of mitochondrial respiratory chain proteins. Biochim Biophys Acta. 2007;1773:1732–1746.
   PubMed Web of Science ®Google Scholar
• Samartzis EP, Noske A, Meisel A, et al. The G protein-coupled estrogen receptor (GPER) is expressed in two different subcellular localizations reflecting distinct tumor properties in breast cancer. PloS one. 2014;9:e83296.
   PubMed Web of Science ®Google Scholar
• Totta P, Pesiri V, Marino M, et al. Lysosomal function is involved in 17β-estradiol-induced estrogen receptor α degradation and cell proliferation. PloS one. 2014;9:e94880.
   PubMed Web of Science ®Google Scholar
• Cheng SB, Quinn JA, Graeber CT, et al. Down-modulation of the G-protein-coupled estrogen receptor, GPER, from the cell surface occurs via a trans-Golgi-proteasome pathway. J Biol Chem. 2011;286:22441–22455.
   PubMed Web of Science ®Google Scholar
• Ma D, Panda S, Lin JD. Temporal orchestration of circadian autophagy rhythm by C/EBPβ. Embo J. 2011;30:4642–4651.
   PubMed Web of Science ®Google Scholar
• Torres-Aviles, N.A., Albores-García D, Luna A, et al. Exposure to p,p’-DDE induces morphological changes and activation of the PKCalpha-p38-C/EBPbeta pathway in human promyelocytic HL-60 cells. Biomed Res Int. 2016;2016:1375606.
   PubMedGoogle Scholar
• Lahn M, Köhler G, Sundell K, et al. Protein kinase C alpha expression in breast and ovarian cancer. Oncology. 2004;67:1–10.
   PubMed Web of Science ®Google Scholar
• Ramji DP, Foka P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J. 2002;365:561–575.
   PubMed Web of Science ®Google Scholar
• Yu T, Yang G, Hou Y, et al. Cytoplasmic GPER translocation in cancer-associated fibroblasts mediates cAMP/PKA/CREB/glycolytic axis to confer tumor cells with multidrug resistance. Oncogene. 2017;36:2131–2145.
   PubMed Web of Science ®Google Scholar
• Xiong X, Tao R, DePinho RA, et al. The autophagy-related gene 14 (Atg14) is regulated by forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism. J Biol Chem. 2012;287:39107–39114.
   PubMed Web of Science ®Google Scholar
• Mammucari C, Milan G, Romanello V, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007;6:458–471.
   PubMed Web of Science ®Google Scholar
• Sanchez AMJ, Csibi A, Raibon A, et al. AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem. 2012;113:695–710.
   PubMed Web of Science ®Google Scholar
• Schips TG, Wietelmann A, Höhn K, et al. FoxO3 induces reversible cardiac atrophy and autophagy in a transgenic mouse model. Cardiovasc Res. 2011;91:587–597.
   PubMed Web of Science ®Google Scholar
• Sisci D, Maris P, Cesario MG, et al. The estrogen receptor α is the key regulator of the bifunctional role of FoxO3a transcription factor in breast cancer motility and invasiveness. Cell Cycle. 2013;12:3405–3420.
   PubMed Web of Science ®Google Scholar
• Zekas E, Prossnitz ER. Estrogen-mediated inactivation of FOXO3a by the G protein-coupled estrogen receptor GPER. BMC Cancer. 2015;15:702.
   PubMed Web of Science ®Google Scholar
• Kenzelmann Broz D, Spano Mello S, Bieging KT, et al. Global genomic profiling reveals an extensive p53-regulated autophagy program contributing to key p53 responses. Genes Dev. 2013;27:1016–1031.
   PubMed Web of Science ®Google Scholar
• Konduri SD, Medisetty R, Liu W, et al. Mechanisms of estrogen receptor antagonism toward p53 and its implications in breast cancer therapeutic response and stem cell regulation. Proc Natl Acad Sci U S A. 2010;107:15081–15086.
   PubMed Web of Science ®Google Scholar
• Lu W, Katzenellenbogen BS. Estrogen Receptor-β modulation of the ERα-p53 loop regulating gene expression, proliferation, and apoptosis in breast cancer. Horm Cancer. 2017;8:230–242.
   PubMed Web of Science ®Google Scholar
• Caldon CE. Estrogen signaling and the DNA damage response in hormone dependent breast cancers. Front Oncol. 2014;4:106.
   PubMedGoogle Scholar
• Fullgrabe J, Klionsky DJ, Joseph B. The return of the nucleus: transcriptional and epigenetic control of autophagy. Nat Rev Mol Cell Biol. 2014;15:65–74.
   PubMed Web of Science ®Google Scholar
• Li Y, Xu M, Ding X, et al. Protein kinase C controls lysosome biogenesis independently of mTORC1. Nat Cell Biol. 2016;18:1065–1077.
   PubMed Web of Science ®Google Scholar
• Tamatani M, Che YH, Matsuzaki H, et al. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem. 1999;274:8531–8538.
   PubMed Web of Science ®Google Scholar
• Copetti T, Bertoli C, Dalla E, et al. p65/RelA modulates BECN1 transcription and autophagy. Mol Cell Biol. 2009;29:2594–2608.
   PubMed Web of Science ®Google Scholar
• Shaw J, Yurkova N, Zhang T, et al. Antagonism of E2F-1 regulated Bnip3 transcription by NF-kappaB is essential for basal cell survival. Proc Natl Acad Sci U S A. 2008;105:20734–20739.
   PubMed Web of Science ®Google Scholar
• Duran A, Linares JF, Galvez AS, et al. The signaling adaptor p62 is an important NF-kappaB mediator in tumorigenesis. Cancer Cell. 2008;13:343–354.
   PubMed Web of Science ®Google Scholar
• Kalaitzidis D, Gilmore TD. Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol Metab. 2005;16:46–52.
   PubMed Web of Science ®Google Scholar
• Liang S, Chen Z, Jiang G, et al. Activation of GPER suppresses migration and angiogenesis of triple negative breast cancer via inhibition of NF-κB/IL-6 signals. Cancer Lett. 2017;386:12–23.
   PubMed Web of Science ®Google Scholar
• Kang J, Chong SJF, Ooi VZQ, et al. Overexpression of Bcl-2 induces STAT-3 activation via an increase in mitochondrial superoxide. Oncotarget. 2015;6:34191–34205.
   PubMedGoogle Scholar
• Pratt J, Annabi B. Induction of autophagy biomarker BNIP3 requires a JAK2/STAT3 and MT1-MMP signaling interplay in Concanavalin-A-activated U87 glioblastoma cells. Cell Signal. 2014;26:917–924.
   PubMed Web of Science ®Google Scholar
• Binai, N.A., Damert A, Carra G, et al. Expression of estrogen receptor alpha increases leptin-induced STAT3 activity in breast cancer cells. Int J Cancer. 2010;127:55–66.
   PubMed Web of Science ®Google Scholar
• Settembre C, De Cegli R, Mansueto G, et al. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol. 2013;15:647–658.
   PubMed Web of Science ®Google Scholar
• Napolitano G, Ballabio A. TFEB at a glance. J Cell Sci. 2016;129:2475–2481.
   PubMed Web of Science ®Google Scholar
• Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, et al. Regulation of TFEB and V-ATPases by mTORC1. Embo J. 2011;30:3242–3258.
   PubMed Web of Science ®Google Scholar
• Alayev A, Salamon RS, Berger SM, et al. mTORC1 directly phosphorylates and activates ERα upon estrogen stimulation. Oncogene. 2016;35:3535–3543.
   PubMed Web of Science ®Google Scholar
• Jerjees DA, Negm OH, Alabdullah ML, et al. The mammalian target of rapamycin complex 1 (mTORC1) in breast cancer: the impact of oestrogen receptor and HER2 pathways. Breast Cancer Res Treat. 2015;150:91–103.
   PubMed Web of Science ®Google Scholar
• Li DD, Wang -L-L, Deng R, et al. The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agents-induced autophagy in cancer cells. Oncogene. 2009;28:886–898.
   PubMed Web of Science ®Google Scholar
• Sun T, Li D, Wang L, et al. c-Jun NH2-terminal kinase activation is essential for up-regulation of LC3 during ceramide-induced autophagy in human nasopharyngeal carcinoma cells. J Transl Med. 2011;9:161.
   PubMed Web of Science ®Google Scholar
• Chimento A, Sirianni R, Casaburi I, et al. 17β-Estradiol activates GPER- and ESR1-dependent pathways inducing apoptosis in GC-2 cells, a mouse spermatocyte-derived cell line. Mol Cell Endocrinol. 2012;355:49–59.
   PubMed Web of Science ®Google Scholar
• Catalano, S, Giordano C, Panza S, et al. Tamoxifen through GPER upregulates aromatase expression: a novel mechanism sustaining tamoxifen-resistant breast cancer cell growth. Breast Cancer Res Treat. 2014;146:273–285.
   PubMed Web of Science ®Google Scholar
• Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283:10892–10903.
   PubMed Web of Science ®Google Scholar
• Lim, W, Park Y, Cho J, et al. Estrogen receptor beta inhibits transcriptional activity of hypoxia inducible factor-1 through the downregulation of arylhydrocarbon receptor nuclear translocator. Breast Cancer Res. 2011;13:R32.
   PubMed Web of Science ®Google Scholar
• De Francesco EM, Pellegrino M, Santolla MF, et al. GPER mediates activation of HIF1α/VEGF signaling by estrogens. Cancer Res. 2014;74:4053–4064.
   PubMed Web of Science ®Google Scholar
• Yang J, AlTahan A, Jones DT, et al. Estrogen receptor-α directly regulates the hypoxia-inducible factor 1 pathway associated with antiestrogen response in breast cancer. Proc Natl Acad Sci U S A. 2015;112:15172–15177.
   PubMed Web of Science ®Google Scholar
• Williams KC, Renthal NE, Gerard RD, et al. The microRNA (miR)-199a/214 cluster mediates opposing effects of progesterone and estrogen on uterine contractility during pregnancy and labor. Mol Endocrinol. 2012;26:1857–1867.
   PubMedGoogle Scholar
• Yu G, Wang J, Xu K, et al. Dynamic regulation of uncoupling protein 2 expression by microRNA-214 in hepatocellular carcinoma. Biosci Rep. 2016;36:e00335.
   Web of Science ®Google Scholar
• Diano S, Horvath TL. Mitochondrial uncoupling protein 2 (UCP2) in glucose and lipid metabolism. Trends Mol Med. 2012;18:52–58.
   PubMed Web of Science ®Google Scholar
• Teng Y, Litchfield LM, Ivanova MM, et al. Dehydroepiandrosterone-induces miR-21 transcription in HepG2 cells through estrogen receptor β and androgen receptor. Mol Cell Endocrinol. 2014;392:23–36.
   PubMed Web of Science ®Google Scholar
• Klinge CM. miRNAs and estrogen action. Trends Endocrinol Metab. 2012;23:223–233.
   PubMed Web of Science ®Google Scholar
• Young NA, Valiente GR, Hampton JM, et al. Estrogen-regulated STAT1 activation promotes TLR8 expression to facilitate signaling via microRNA-21 in systemic lupus erythematosus. Clin Immunology. 2017;176:12–22.
   PubMed Web of Science ®Google Scholar
• Chan SR, Vermi W, Luo J, et al. STAT1-deficient mice spontaneously develop estrogen receptor alpha-positive luminal mammary carcinomas. Breast Cancer Res. 2012;14:R16.
   PubMed Web of Science ®Google Scholar
• McCormick J, Suleman N, Scarabelli TM, et al. STAT1 deficiency in the heart protects against myocardial infarction by enhancing autophagy. J Cell Mol Med. 2012;16:386–393.
   PubMed Web of Science ®Google Scholar
• Sims EK, Lakhter AJ, Anderson-Baucum E, et al. MicroRNA 21 targets BCL2 mRNA to increase apoptosis in rat and human beta cells. Diabetologia. 2017;60:1057–1065.
   PubMed Web of Science ®Google Scholar
• Tao S, He H, Chen Q. Estradiol induces HOTAIR levels via GPER-mediated miR-148a inhibition in breast cancer. J Transl Med. 2015;13:131.
   PubMed Web of Science ®Google Scholar
• Yang L, Zhang X, Li H, et al. The long noncoding RNA HOTAIR activates autophagy by upregulating ATG3 and ATG7 in hepatocellular carcinoma. Mol Biosyst. 2016;12:2605–2612.
   PubMedGoogle Scholar
• Sun MY, Zhu J-Y, Zhang C-Y, et al. Autophagy regulated by lncRNA HOTAIR contributes to the cisplatin-induced resistance in endometrial cancer cells. Biotechnol Lett. 2017;39:1477–1484.
   PubMed Web of Science ®Google Scholar
• Zhou J, Yao W, Liu K, et al. MicroRNA let-7g regulates mouse granulosa cell autophagy by targeting insulin-like growth factor 1 receptor. Int J Biochem Cell Biol. 2016;78:130–140.
   PubMed Web of Science ®Google Scholar
• Qian P, Zuo Z, Wu Z, et al. Pivotal role of reduced let-7g expression in breast cancer invasion and metastasis. Cancer Res. 2011;71:6463–6474.
   PubMed Web of Science ®Google Scholar
• Kim MY, Woo EM, Chong YTE, et al. Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol Endocrinol. 2006;20:1479–1493.
   PubMedGoogle Scholar
• Moresi V, Carrer M, Grueter CE, et al. Histone deacetylases 1 and 2 regulate autophagy flux and skeletal muscle homeostasis in mice. Proc Natl Acad Sci U S A. 2012;109:1649–1654.
   PubMed Web of Science ®Google Scholar
• Gammoh N, Lam D, Puente C, et al. Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci U S A. 2012;109:6561–6565.
   PubMed Web of Science ®Google Scholar
• Pedram A, Razandi M, Narayanan R, et al. Estrogen regulates histone deacetylases to prevent cardiac hypertrophy. Mol Biol Cell. 2013;24:3805–3818.
   PubMed Web of Science ®Google Scholar
• Ma H, Li L, Dou G, et al. Z-ligustilide restores tamoxifen sensitivity of ERa negative breast cancer cells by reversing MTA1/IFI16/HDACs complex mediated epigenetic repression of ERa. Oncotarget. 2017;8:29328–29345.
   PubMedGoogle Scholar
• Jia YL, Xu M, Dou C-W, et al. P300/CBP-associated factor (PCAF) inhibits the growth of hepatocellular carcinoma by promoting cell autophagy. Cell Death Dis. 2016;7:e2400.
   PubMed Web of Science ®Google Scholar
• Iizuka M, Susa T, Tamamori-Adachi M, et al. Intrinsic ubiquitin E3 ligase activity of histone acetyltransferase Hbo1 for estrogen receptor α. Proc Jpn Acad Ser B Phys Biol Sci. 2017;93:498–510.
   PubMed Web of Science ®Google Scholar
• Fullgrabe J, Lynch-Day MA, Heldring N, et al. The histone H4 lysine 16 acetyltransferase hMOF regulates the outcome of autophagy. Nature. 2013;500:468–471.
   PubMed Web of Science ®Google Scholar
• Guo JM, Shu H, Wang L, et al. SIRT1-dependent AMPK pathway in the protection of estrogen against ischemic brain injury. CNS Neurosci Ther. 2017;23:360–369.
   PubMed Web of Science ®Google Scholar
• Elangovan S, Ramachandran S, Venkatesan N, et al. SIRT1 is essential for oncogenic signaling by estrogen/estrogen receptor α in breast cancer. Cancer Res. 2011;71:6654–6664.
   PubMed Web of Science ®Google Scholar
• Schoenlein PV, Periyasamy-Thandavan S, Samaddar JS, et al. Autophagy facilitates the progression of ERalpha-positive breast cancer cells to antiestrogen resistance. Autophagy. 2009;5:400–403.
   PubMed Web of Science ®Google Scholar
• Periyasamy-Thandavan S, Jackson WH, Samaddar JS, et al. Bortezomib blocks the catabolic process of autophagy via a cathepsin-dependent mechanism, affects endoplasmic reticulum stress and induces caspase-dependent cell death in antiestrogen-sensitive and resistant ER+ breast cancer cells. Autophagy. 2010;6:19–35.
   PubMed Web of Science ®Google Scholar
• Karunakaran S, Ramachandran S, Coothankandaswamy V, et al. SLC6A14 (ATB0,+) protein, a highly concentrative and broad specific amino acid transporter, is a novel and effective drug target for treatment of estrogen receptor-positive breast cancer. J Biol Chem. 2011;286:31830–31838.
   PubMed Web of Science ®Google Scholar
• Cook KL, Clarke R. Estrogen receptor-alpha signaling and localization regulates autophagy and unfolded protein response activation in ER+ breast cancer. Receptors Clin Investig. 2014;1:e316.
   Google Scholar
• Tran AT, Ramalinga M, Kedir H, et al. Autophagy inhibitor 3-methyladenine potentiates apoptosis induced by dietary tocotrienols in breast cancer cells. Eur J Nutr. 2015;54:265–272.
   PubMed Web of Science ®Google Scholar
• Thorburn A, Thamm DH, Gustafson DL. Autophagy and cancer therapy. Mol Pharmacol. 2014;85:830–838.
   PubMed Web of Science ®Google Scholar
• Lin S-R, Fu Y-S, Tsai M-J, et al. Natural compounds from herbs that can potentially execute as autophagy inducers for cancer therapy. Int J Mol Sci. 2017;18:1412.
   Web of Science ®Google Scholar
• Buckley KM, Hess DL, Sazonova IY, et al. Rapamycin up-regulation of autophagy reduces infarct size and improves outcomes in both permanent MCAL, and embolic MCAO, murine models of stroke. Exp Transl Stroke Med. 2014;6:8.
   PubMedGoogle Scholar
• Martinez-Outschoorn UE, Pavlides S, Whitaker-Menezes D, et al. Tumor cells induce the cancer associated fibroblast phenotype via caveolin-1 degradation: implications for breast cancer and DCIS therapy with autophagy inhibitors. Cell Cycle. 2010;9:2423–2433.
   PubMed Web of Science ®Google Scholar
• Massarweh S, Romond E, Black EP, et al. A phase II study of combined fulvestrant and everolimus in patients with metastatic estrogen receptor (ER)-positive breast cancer after aromatase inhibitor (AI) failure. Breast Cancer Res Treat. 2014;143:325–332.
   PubMed Web of Science ®Google Scholar
• Periyasamy-Thandavan S, Jiang M, Schoenlein P, et al. Autophagy: molecular machinery, regulation, and implications for renal pathophysiology. Am J Physiol Renal Physiol. 2009;297:F244–256.
   PubMed Web of Science ®Google Scholar
• Tyson JJ, Baumann WT, Chen C, et al. Dynamic modelling of oestrogen signalling and cell fate in breast cancer cells. Nat Rev Cancer. 2011;11:523–532.
   PubMed Web of Science ®Google Scholar
• Petherick KJ, Williams AC, Lane JD, et al. Autolysosomal β-catenin degradation regulates Wnt-autophagy-p62 crosstalk. Embo J. 2013;32:1903–1916.
   PubMed Web of Science ®Google Scholar
• Petrovski G, Zahuczky G, Katona K, et al. Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death Differ. 2007;14:1117–1128.
   PubMed Web of Science ®Google Scholar
• Blessing AM, Rajapakshe K, Reddy Bollu L, et al. Transcriptional regulation of core autophagy and lysosomal genes by the androgen receptor promotes prostate cancer progression. Autophagy. 2017;13:506–521.
   PubMed Web of Science ®Google Scholar
• Dai R, Ahmed SA. Sexual dimorphism of miRNA expression: a new perspective in understanding the sex bias of autoimmune diseases. Ther Clin Risk Manag. 2014;10:151–163.
   PubMed Web of Science ®Google Scholar
• Nikoletopoulou V, Papandreou M-E, Tavernarakis N. Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ. 2015;22:398–407.
   PubMed Web of Science ®Google Scholar
• Valenti MT, Dalle Carbonare L, Mottes M. Role of autophagy in bone and muscle biology. World J Stem Cells. 2016;8:396–398.
   PubMed Web of Science ®Google Scholar
• Hainsworth, JD, Shih, KC, Shepard, GC, et al. Phase II study of concurrent radiation therapy, temozolomide, and bevacizumab followed by bevacizumab/everolimus as first-line treatment for patients with glioblastoma. Clin Adv Hematol Oncol. 2012;10:240–246.
   PubMedGoogle Scholar
• Odia Y, Kreisl TN, Aregawi D, et al. A phase II trial of tamoxifen and bortezomib in patients with recurrent malignant gliomas. J Neurooncol. 2015;125:191–195.
   PubMed Web of Science ®Google Scholar
• Niehof M, Manns MP, Trautwein C. CREB controls LAP/C/EBP beta transcription. Mol Cell Biol. 1997;17:3600–3613.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Goodwin JG, Chauhan S, et al. ZKSCAN3 is a master transcriptional repressor of autophagy. Molecular Cell. 2013;50:16–28.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Weidberg H, Gonen C, et al. p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation. Proc Natl Acad Sci U S A. 2010;107:18511–18516.
   PubMed Web of Science ®Google Scholar
• Webb AE, Brunet A. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014;39:159–169.
   PubMed Web of Science ®Google Scholar
• Kouzmenko AP, Takeyama K-I, Ito S, et al. Wnt/beta-catenin and estrogen signaling converge in vivo. J Biol Chem. 2004;279:40255–40258.
   PubMed Web of Science ®Google Scholar