The role of Gα protein signaling in the membrane estrogen receptor-mediated signaling

References

• Nilsson S, Mäkelä S, Treuter E, et al. Mechanisms of estrogen action. Physiol Rev. 2001;81(4):1535–1565.
   PubMed Web of Science ®Google Scholar
• Matthews J, Gustafsson JA. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv. 2003;3(5):281–292.
   PubMedGoogle Scholar
• Levin ER. Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol. 2005;19(8):1951–1959.
   PubMedGoogle Scholar
• Simoncini T, Mannella P, Fornari L, et al. Genomic and non-genomic effects of estrogens on endothelial cells. Steroids. 2004;69(8-9):537–542.
   PubMed Web of Science ®Google Scholar
• Boonyaratanakornkit V, Edwards DP. Receptor mechanisms mediating non-genomic actions of sex steroids. Semin Reprod Med. 2007;25(3):139–153.
   PubMed Web of Science ®Google Scholar
• Ellis MJ, et al. Letrozole inhibits tumor proliferation more effectively than tamoxifen independent of HER1/2 expression status. Cancer Res. 2003;63(19):6523–6531.
   PubMed Web of Science ®Google Scholar
• Zhang XT, Kang LG, Ding L, et al. A positive feedback loop of ER-α36/EGFR promotes malignant growth of ER-negative breast cancer cells. Oncogene. 2011;30(7):770–780.
   PubMed Web of Science ®Google Scholar
• Prossnitz ER, Maggiolini M. Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol. 2009;308(1-2):32–38.
   PubMed Web of Science ®Google Scholar
• Qiu J, Bosch MA, Tobias SC, et al. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci. 2003;23(29):9529–9540.
   PubMed Web of Science ®Google Scholar
• Qiu J, Ronnekleiv OK, Kelly MJ. Modulation of hypothalamic neuronal activity through a novel G-protein-coupled estrogen membrane receptor. Steroids. 2008;73(9-10):985–991.
   PubMed Web of Science ®Google Scholar
• Toran-Allerand CD, Guan X, MacLusky NJ, et al. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci. 2002;22(19):8391–8401.
   PubMed Web of Science ®Google Scholar
• Kampa M, Notas G, Pelekanou V, et al. Early membrane initiated transcriptional effects of estrogens in breast cancer cells: first pharmacological evidence for a novel membrane estrogen receptor element (ERx). Steroids. 2012;77(10):959–967.
   PubMed Web of Science ®Google Scholar
• Simon MI, Strathmann MP, Gautam N. Diversity of G proteins in signal transduction. Science. 1991;252(5007):802–808.
   PubMed Web of Science ®Google Scholar
• Robillard L, Ethier N, Lachance M, et al. Gbetagamma subunit combinations differentially modulate receptor and effector coupling in vivo. Cell Signal. 2000;12(9-10):673–682.
   PubMed Web of Science ®Google Scholar
• Simoncini T, Scorticati C, Mannella P, et al. Estrogen receptor alpha interacts with Galpha13 to drive actin remodeling and endothelial cell migration via the RhoA/Rho kinase/moesin pathway. Mol Endocrinol. 2006;20(8):1756–1771.
   PubMedGoogle Scholar
• Xu X, Yan Q, Liu X, et al. 17β-Estradiol nongenomically induces vascular endothelial H2S release by promoting phosphorylation of cystathionine γ-lyase. J Biol Chem. 2019;294(43):15577–15592.
   PubMed Web of Science ®Google Scholar
• Sinchak K, Wagner EJ. Estradiol signaling in the regulation of reproduction and energy balance. Front Neuroendocrinol. 2012;33(4):342–363.
   PubMed Web of Science ®Google Scholar
• Giretti MS, Fu X-D, De Rosa G, et al. Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS One. 2008;3(5):e2238.
   PubMed Web of Science ®Google Scholar
• Qiu J, Bosch MA, Tobias SC, et al. A G-protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J Neurosci. 2006;26(21):5649–5655.
   PubMed Web of Science ®Google Scholar
• Pietras RJ, Szego CM. Partial purification and characterization of oestrogen receptors in subfractions of hepatocyte plasma membranes. Biochem J. 1980;191(3):743–760.
   PubMed Web of Science ®Google Scholar
• Micevych PE, Mermelstein PG. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol. 2008;38(1):66–77.
   PubMed Web of Science ®Google Scholar
• Pedram A, Razandi M, Kim JK, et al. Developmental phenotype of a membrane only estrogen receptor alpha (MOER) mouse. J Biol Chem. 2009;284(6):3488–3495.
   PubMed Web of Science ®Google Scholar
• Levin ER, Hammes SR. Nuclear receptors outside the nucleus: extranuclear signalling by steroid receptors. Nat Rev Mol Cell Biol. 2016;17(12):783–797.
   PubMed Web of Science ®Google Scholar
• Wang Z, Zhang X, Shen P, et al. A variant of estrogen receptor-{alpha}, hER-{alpha}36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signaling. Proc Natl Acad Sci USA. 2006;103(24):9063–9068.
   PubMed Web of Science ®Google Scholar
• Marquez DC, et al. Estrogen receptors in membrane lipid rafts and signal transduction in breast cancer. Mol Cell Endocrinol. 2006;46(1-2):91–100.
   Google Scholar
• Li L, Haynes MP, Bender JR. Plasma membrane localization and function of the estrogen receptor alpha variant (ER46) in human endothelial cells. Proc Natl Acad Sci USA. 2003;100(8):4807–4812.
   PubMed Web of Science ®Google Scholar
• Sheldahl LC, Shapiro RA, Bryant DN, et al. Estrogen induces rapid translocation of estrogen receptor beta, but not estrogen receptor alpha, to the neuronal plasma membrane. Neuroscience. 2008;153(3):751–761.
   PubMed Web of Science ®Google Scholar
• Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem. 2002;277(44):41295–41298.
   PubMed Web of Science ®Google Scholar
• Acconcia F, Ascenzi P, Fabozzi G, et al. S-palmitoylation modulates human estrogen receptor-alpha functions. Biochem Biophys Res Commun. 2004;316(3):878–883.
   PubMed Web of Science ®Google Scholar
• Pedram A, Razandi M, Lubahn D, et al. Estrogen inhibits cardiac hypertrophy: role of estrogen receptor-beta to inhibit calcineurin. Endocrinology. 2008;149(7):3361–3369.
   PubMed Web of Science ®Google Scholar
• Boonyaratanakornkit V. Scaffolding proteins mediating membrane-initiated extra-nuclear actions of estrogen receptor. Steroids. 2011;76(9):877–884.
   PubMed Web of Science ®Google Scholar
• Boulware MI, Kordasiewicz H, Mermelstein PG. Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci. 2007;27(37):9941–9950.
   PubMed Web of Science ®Google Scholar
• Boonyaratanakornkit V, Hamilton N, Márquez-Garbán DC, et al. Extranuclear signaling by sex steroid receptors and clinical implications in breast cancer. Mol Cell Endocrinol. 2018;466:51–72.
   PubMed Web of Science ®Google Scholar
• Tominna R, Chokr S, Feri M, et al. Plasma membrane G protein-coupled estrogen receptor 1 (GPER) mediates rapid estradiol facilitation of sexual receptivity through the orphanin-FQ-ORL-1 system in estradiol primed female rats. Horm Behav. 2019;112:89–99.
   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(7):3236–3245.
   PubMed Web of Science ®Google Scholar
• Soltysik K, Czekaj P. Membrane estrogen receptors - is it an alternative way of estrogen action? J Physiol Pharmacol. 2013;64(2):129–142.
   PubMed Web of Science ®Google Scholar
• Moreira IS. Structural features of the G-protein/GPCR interactions. Biochim Biophys Acta. 2014;1840(1):16–33.
   PubMed Web of Science ®Google Scholar
• Evanko DS, Thiyagarajan MM, Siderovski DP, et al. Gbeta gamma isoforms selectively rescue plasma membrane localization and palmitoylation of mutant Galphas and Galphaq. J Biol Chem. 2001;276(26):23945–23953.
   PubMed Web of Science ®Google Scholar
• Lappano R, Maggiolini M. GPCRs and cancer. Acta Pharmacol Sin. 2012;33(3):351–362.
   PubMed Web of Science ®Google Scholar
• Sutherland EW, Rall TW. Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J Biol Chem. 1958;232(2):1077–1091.
   PubMed Web of Science ®Google Scholar
• Wettschureck N, Offermanns S. Mammalian G proteins and their cell type specific functions. Physiol Rev. 2005;85(4):1159–1204.
   PubMed Web of Science ®Google Scholar
• Hildebrandt JD, Birnbaumer L. Inhibitory regulation of adenylyl cyclase in the absence of stimulatory regulation. Requirements and kinetics of guanine nucleotide-induced inhibition of the cyc- S49 adenylyl cyclase. J Biol Chem. 1983;258(21):13141–13147.
   PubMed Web of Science ®Google Scholar
• Rhee SG. Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem. 2001;70:281–312.
   PubMed Web of Science ®Google Scholar
• Rhee SG, Bae YS. Regulation of phosphoinositide-specific phospholipase C isozymes. J Biol Chem. 1997;272(24):15045–15048.
   PubMed Web of Science ®Google Scholar
• Kozasa T, Jiang X, Hart MJ, et al. p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science. 1998;280(5372):2109–2111.
   PubMedGoogle Scholar
• Longenecker KL, Lewis ME, Chikumi H, et al. Structure of the RGS-like domain from PDZ-RhoGEF: linking heterotrimeric g protein-coupled signaling to Rho GTPases. Structure. 2001;9(7):559–569.
   PubMed Web of Science ®Google Scholar
• Fukuhara S, Chikumi H, Gutkind JS. RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene. 2001;20(13):1661–1668.
   PubMed Web of Science ®Google Scholar
• Sivaraj KK, Takefuji M, Schmidt I, et al. G13 controls angiogenesis through regulation of VEGFR-2 expression. Dev Cell. 2013;25(4):427–434.
   PubMed Web of Science ®Google Scholar
• Shan D, Chen L, Wang D, et al. The G protein G alpha(13) is required for growth factor-induced cell migration. Dev Cell. 2006;10(6):707–718.
   PubMed Web of Science ®Google Scholar
• Kumar P, Wu Q, Chambliss KL, et al. Direct interactions with G α i and G βγ mediate nongenomic signaling by estrogen receptor α. Mol Endocrinol. 2007;21(6):1370–1380.
   PubMedGoogle Scholar
• Kelly P, Moeller BJ, Juneja J, et al. The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis. Proc Natl Acad Sci USA. 2006;103(21):8173–8178.
   PubMed Web of Science ®Google Scholar
• Yagi H, Tan W, Dillenburg-Pilla P, et al. A synthetic biology approach reveals a CXCR4-G13-Rho signaling axis driving transendothelial migration of metastatic breast cancer cells. Sci Signal. 2011;4(191):ra60.
   PubMed Web of Science ®Google Scholar
• Zheng S, Huang J, Zhou K, et al. 17β-Estradiol enhances breast cancer cell motility and invasion via extra-nuclear activation of actin-binding protein ezrin. PLoS One. 2011;6(7):e22439.
   PubMed Web of Science ®Google Scholar
• Filardo EJ, Quinn JA, Frackelton AR, et al. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol. 2002;16(1):70–84.
   PubMed Web of Science ®Google Scholar
• Filardo EJ, Quinn JA, Bland KI, et al. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol. 2000;14(10):1649–1660.
   PubMed Web of Science ®Google Scholar
• Albanito L, Madeo A, Lappano R, et al. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 2007;67(4):1859–1866.
   PubMed Web of Science ®Google Scholar
• Choi J-M, Kim S-S, Choi C-I, et al. Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in Go-deficient mice. Proc Natl Acad Sci USA. 2016;113(39):10974–10979.
   PubMed Web of Science ®Google Scholar
• Cha HL, Choi J-M, Oh H-H, et al. Deletion of the α subunit of the heterotrimeric Go protein impairs cerebellar cortical development in mice. Mol Brain. 2019;12(1):57.
   PubMedGoogle Scholar
• Hu P, Liu J, Yasrebi A, et al. Gq protein-coupled membrane-initiated estrogen signaling rapidly excites corticotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus in female mice. Endocrinology. 2016;157(9) :3604–3620.
   PubMed Web of Science ®Google Scholar
• Nag S, Mokha SS. Activation of a Gq-coupled membrane estrogen receptor rapidly attenuates α2-adrenoceptor-induced antinociception via an ERK I/II-dependent, non-genomic mechanism in the female rat. Neuroscience. 2014;267:122–134.
   PubMed Web of Science ®Google Scholar
• Kuo J, Hariri OR, Bondar G, et al. Membrane estrogen receptor-alpha interacts with metabotropic glutamate receptor type 1a to mobilize intracellular calcium in hypothalamic astrocytes. Endocrinology. 2009;150(3):1369–1376.
   PubMed Web of Science ®Google Scholar
• Malyala A, Kelly MJ, Ronnekleiv OK. Estrogen modulation of hypothalamic neurons: activation of multiple signaling pathways and gene expression changes. Steroids. 2005;70(5-7):397–406.
   PubMed Web of Science ®Google Scholar
• Roepke TA. Oestrogen modulates hypothalamic control of energy homeostasis through multiple mechanisms. J Neuroendocrinol. 2009;21(2):141–150.
   PubMed Web of Science ®Google Scholar
• Gao Q, Horvath TL. Neurobiology of feeding and energy expenditure. Annu Rev Neurosci. 2007;30:367–398.
   PubMed Web of Science ®Google Scholar
• Smith AW, Bosch MA, Wagner EJ, et al. The membrane estrogen receptor ligand STX rapidly enhances GABAergic signaling in NPY/AgRP neurons: role in mediating the anorexigenic effects of 17β-estradiol. Am J Physiol Endocrinol Metab. 2013;305(5):E632–40.
   PubMed Web of Science ®Google Scholar
• Swaab DF, Bao AM, Lucassen PJ. The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev. 2005;4(2):141–194.
   PubMed Web of Science ®Google Scholar
• Boulware MI, Weick JP, Becklund BR, et al. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci. 2005;25(20):5066–5078.
   PubMed Web of Science ®Google Scholar
• Zur Nieden R, Deitmer JW. The role of metabotropic glutamate receptors for the generation of calcium oscillations in rat hippocampal astrocytes in situ. Cereb Cortex. 2006;16(5):676–687.
   PubMed Web of Science ®Google Scholar
• Wu M, Chen W, Lu Y, et al. Gα13 negatively controls osteoclastogenesis through inhibition of the Akt-GSK3β-NFATc1 signalling pathway. Nat Commun. 2017;8:13700.
   PubMed Web of Science ®Google Scholar
• Lieberherr M, Grosse B, Kachkache M, et al. Cell signaling and estrogens in female rat osteoblasts: a possible involvement of unconventional nonnuclear receptors. J Bone Miner Res. 1993;8(11):1365–1376.
   PubMed Web of Science ®Google Scholar