G protein-coupled estrogen receptor is required for the neuritogenic mechanism of 17β-estradiol in developing hippocampal neurons

Molecular and Cellular Endocrinology

Volumn 372, Issue 1-2, 2013, Pages 105-115

  Ruiz Palmero, Isabel ^a   Hernando, Maria ^a   Garcia Segura, Luis M ^a   Arevalo, Maria Angeles ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Akt; G1; G15; GPR30; Neurogenin 3; Phosphoinositide 3 kinase

Indexed keywords

ESTRADIOL; FULVESTRANT; G PROTEIN COUPLED RECEPTOR 30; NEUROGENIN 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECEPTOR BLOCKING AGENT; SERINE; SMALL INTERFERING RNA; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; HORMONE ACTION; MOUSE; NERVE CELL DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM;

ANDROSTADIENES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MICE; NERVE TISSUE PROTEINS; NEURITES; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84877139520     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.03.018     Document Type: Article

References (63)

1. Al Sweidi S., Sánchez M.G., Bourque M., Morissette M., Dluzen D., Di Paolo T. Oestrogen receptors and signalling pathways: implications for neuroprotective effects of sex steroids in Parkinson's disease. J. Neuroendocrinol. 2012, 24:48-61.
2. Arevalo M.A., Ruiz-Palmero I., Scerbo M.J., Acaz-Fonseca E., Cambiasso M.J., Garcia-Segura L.M. Molecular mechanisms involved in the regulation of neuritogenesis by estradiol: recent advances. J. Steroid. Biochem. Mol. Biol. 2012, 131:52-56.
3. Barton M. Position paper: the membrane estrogen receptor GPER/GPR30: clues and questions. Steroids 2012, 77:935-942.
4. Blasko E., Haskell C.A., Leung S., Gualtieri G., Halks-Miller M., Mahmoudi M., Dennis M.K., Prossnitz E.R., Karpus W.J., Horuk R. Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis. J. Neuroimmunol. 2009, 214:67-77.
5. Bodhankar S., Offner H. GPR30 Forms an integral part of E2-protective pathway in experimental autoimmune encephalomyelitis. Immunol. Endocr. Metab. Agents Med. Chem. 2011, 11:262-274.
6. Bologa C.G., Revankar C.M., Young S.M., Edwards B.S., Arterburn J.B., Kiselyov A.S., Parker M.A., Tkachenko S.E., Savchuck N.P., Sklar L.A., Oprea T.I., Prossnitz E.R. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2006, 2:207-212.
7. Bourque M., Dluzen D.E., Di Paolo T. Signaling pathways mediating the neuroprotective effects of sex steroids and SERMs in Parkinson's disease. Front. Neuroendocrinol. 2012, 33:169-178.
8. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
9. Canonaco M., Giusi G., Madeo A., Facciolo R.M., Lappano R., Canonaco A., Maggiolini M. A sexually dimorphic distribution pattern of the novel estrogen receptor G-protein-coupled receptor 30 in some brain areas of the hamster. J. Endocrinol. 2008, 196:131-138.
10. Cardona-Gomez P., Perez M., Avila J., Garcia-Segura L.M., Wandosell F. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors, GSK3, and beta-catenin in the hippocampus. Mol. Cell. Neurosci. 2004, 25:363-373.
11. Carmeci C., Thompson D.A., Ring H.Z., Francke U., Weigel R.J. 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.
12. Dennis M.K., Burai R., Ramesh C., Petrie W.K., Alcon S.N., Nayak T.K., Bologa C.G., Leitao A., Brailoiu E., Deliu E., Dun N.J., Sklar L.A., Hathaway H.J., Arterburn J.B., Oprea T.I., Prossnitz E.R. In vivo effects of a GPR30 antagonist. Nat. Chem. Biol. 2009, 5:421-427.
13. Dominguez R., Jalali C., de Lacalle S. Morphological effects of estrogen on cholinergic neurons in vitro involves activation of extracellular signal-regulated kinases. J. Neurosci. 2004, 24:982-990.
14. Dun S.L., Brailoiu G.C., Gao X., Brailoiu E., Arterburn J.B., Prossnitz E.R., Oprea T.I., Dun N.J. Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia. J. Neurosci. Res. 2009, 87:1610-1619.
15. Filardo E.J., Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol. Metab. 2005, 16:362-367.
16. Filardo E.J., Thomas P. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology 2012, 153:2953-2962.
17. Filardo E.J., Quinn J.A., Bland K.I., Frackelton A.R. 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, 14:1649-1660.
18. Garcia-Segura L.M., Arevalo M.A., Azcoitia I. Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Prog. Brain Res. 2010, 181:251-272.
19. Gingerich S., Kim G.L., Chalmers J.A., Koletar M.M., Wang X., Wang Y., Belsham D.D. Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 2010, 170:54-66.
20. Gorosito S.V., Cambiasso M.J. Axogenic effect of estrogen in male rat hypothalamic neurons involves Ca(2+), protein kinase C, and extracellular signal-regulated kinase signaling. J. Neurosci. Res. 2008, 86:145-157.
21. Goslin K., Banker G. Experimental observations on the development of polarity by hippocampal neurons in culture. J. Cell. Biol. 1989, 108:1507-1516.
22. Hammond R., Mauk R., Ninaci D., Nelson D., Gibbs R.B. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm. Behav. 2009, 56:309-314.
23. Hammond R., Nelson D., Gibbs R.B. GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus. Psychoneuroendocrinology 2011, 36:182-192.
24. Hazell G.G., Yao S.T., Roper J.A., Prossnitz E.R., O'Carroll A.M., Lolait S.J. Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J. Endocrinol. 2009, 202:223-236.
25. Isensee J., Meoli L., Zazzu V., Nabzdyk C., Witt H., Soewarto D., Effertz K., Fuchs H., Gailus-Durner V., Busch D., Adler T., de Angelis M.H., Irgang M., Otto C., Noppinger P.R. Expression pattern of G protein-coupled receptor 30 in LacZ reporter mice. Endocrinology 2009, 150:1722-1730.
26. Kanda N., Watanabe S. 17Beta-estradiol enhances the production of nerve growth factor in THP-1-derived macrophages or peripheral blood monocyte-derived macrophages. J. Invest. Dermatol. 2003, 121:771-780.
27. Kanda N., Watanabe S. 17Beta-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J. Invest. Dermatol. 2003, 121:1500-1509.
28. Kanda N., Watanabe S. 17Beta-estradiol stimulates the growth of human keratinocytes by inducing cyclin D2 expression. J. Invest. Dermatol. 2004, 123:319-328.
29. Kang L., Zhang X., Xie Y., Tu Y., Wang D., Liu Z., Wang Z.Y. Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling. Mol. Endocrinol. 2010, 24:709-721.
30. Kastenberger I., Lutsch C., Schwarzer C. Activation of the G-protein-coupled receptor GPR30 induces anxiogenic effects in mice, similar to oestradiol. Psychopharmacology (Berlin) 2012, 221:527-535.
31. Langer G., Bader B., Meoli L., Isensee J., Delbeck M., Noppinger P.R., Otto C. A critical review of fundamental controversies in the field of GPR30 research. Steroids 2010, 75:603-610.
32. Lebesgue D., Chevaleyre V., Zukin R.S., Etgen A.M. Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids 2009, 74:555-561.
33. Levin E.R. G protein-coupled receptor 30: estrogen receptor or collaborator?. Endocrinology 2009, 150:1563-1565.
34. Liu S.B., Han J., Zhang N., Tian Z., Li X.B., Zhao M.G. Neuroprotective effects of oestrogen against oxidative toxicity through activation of G-protein-coupled receptor 30 receptor. Clin. Exp. Pharmacol. Physiol. 2011, 38:577-585.
35. Liu S.B., Zhang N., Guo Y.Y., Zhao R., Shi T.Y., Feng S.F., Wang S.Q., Yang Q., Li X.Q., Wu Y.M., Ma L., Hou Y., Xiong L.Z., Zhang W., Zhao M.G. G-protein-coupled receptor 30 mediates rapid neuroprotective effects of estrogen via depression of NR2B-containing NMDA receptors. J. Neurosci. 2012, 32:4887-4900.
36. Maggiolini M., Picard D. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J. Endocrinol. 2010, 204:105-114.
37. Matsuda K., Sakamoto H., Mori H., Hosokawa K., Kawamura A., Itose M., Nishi M., Prossnitz E.R., Kawata M. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci. Lett. 2008, 441:94-99.
38. McAllister C.E., Creech R.D., Kimball P.A., Muma N.A., Li Q. GPR30 is necessary for estradiol-induced desensitization of 5-HT(1A) receptor signaling in the paraventricular nucleus of the rat hypothalamus. Psychoneuroendocrinology 2012, 37:1248-1260.
39. Miñano A., Xifró X., Pérez V., Barneda-Zahonero B., Saura C.A., Rodríguez-Alvarez J. Estradiol facilitates neurite maintenance by a Src/Ras/ERK signalling pathway. Mol. Cell. Neurosci. 2008, 39:143-151.
40. O'Dowd B.F., Nguyen T., Marchese A., Cheng R., Lynch K.R., Heng H.H., Kolakowski L.F., George S.R. Discovery of three novel G-protein-coupled receptor genes. Genomics 1998, 47:310-313.
41. Owman C., Blay P., Nilsson C., Lolait S.J. Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt's lymphoma and widely distributed in brain and peripheral tissues. Biochem. Biophys. Res. Commun. 1996, 228:285-292.
42. Prossnitz E.R., Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat. Rev. Endocrinol. 2011, 7:715-726.
43. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005, 307:1625-1630.
44. Ropero A.B., Pang Y., Alonso-Magdalena P., Thomas P., Nadal A. Role of ERβ and GPR30 in the endocrine pancreas: a matter of estrogen dose. Steroids 2012, 77:951-958.
45. Ruiz-Palmero I., Simon-Areces J., Garcia-Segura L.M., Arevalo M.A. Notch/neurogenin 3 signalling is involved in the neuritogenic actions of oestradiol in developing hippocampal neurones. J. Neuroendocrinol. 2011, 23:355-364.
46. Salama-Cohen P., Arévalo M.A., Grantyn R., Rodríguez-Tébar A. Notch and NGF/p75NTR control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through neurogenin 3. J. Neurochem. 2006, 97:1269-1278.
47. Shepherd C., Banerjee L., Cheung C.W., Mansour M.R., Jenkinson S., Gale R.E., Khwaja A. PI3K/mTOR inhibition upregulates NOTCH-MYC signalling leading to an impaired cytotoxic response. Leukemia 2013, 27:650-660.
48. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
49. Simon-Areces J., Membrive G., Garcia-Fernandez C., Garcia-Segura L.M., Arevalo M.A. Neurogenin 3 cellular and subcellular localization in the developing and adult hippocampus. J. Comp. Neurol. 2010, 518:1814-1824.
50. Takanami K., Sakamoto H., Matsuda K., Hosokawa K., Nishi M., Prossnitz E.R., Kawata M. Expression of G protein-coupled receptor 30 in the spinal somatosensory system. Brain Res. 2010, 1310:17-28.
51. Terasawa E., Noel S.D., Keen K.L. Rapid action of oestrogen in luteinising hormone-releasing hormone neurones: the role of GPR30. J. Neuroendocrinol. 2009, 21:316-321.
52. Thomas P., Pang Y., Filardo E.J., Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005, 146:624-632.
53. Thomas P., Alyea R., Pang Y., Peyton C., Dong J., Berg A.H. Conserved estrogen binding and signaling functions of the G protein-coupled estrogen receptor 1 (GPER) in mammals and fish. Steroids 2010, 75:595-602.
54. Varea O., Garrido J.J., Dopazo A., Mendez P., Garcia-Segura L.M., Wandosell F. Estradiol activates beta-catenin dependent transcription in neurons. PLoS One 2009, 4:e5153.
55. Vivacqua A., Lappano R., De Marco P., Sisci D., Aquila S., De Amicis F., Fuqua S.A., Andò S., Maggiolini M. G protein-coupled receptor 30 expression is up-regulated by EGF and TGF alpha in estrogen receptor alpha-positive cancer cells. Mol. Endocrinol. 2009, 23:1815-1826.
56. Wallacides A., Chesnel A., Ajj H., Chillet M., Flament S., Dumond H. Estrogens promote proliferation of the seminoma-like TCam-2 cell line through a GPER-dependent ERα36 induction. Mol. Cell. Endocrinol. 2012, 350:61-71.
57. Wei Y., Zhang Z., Liao H., Wu L., Wu X., Zhou D., Xi X., Zhu Y., Feng Y. Nuclear estrogen receptor-mediated Notch signaling and GPR30-mediated PI3K/AKT signaling in the regulation of endometrial cancer cell proliferation. Oncol. Rep. 2012, 27:504-510.
58. Wong G.W., Knowles G.C., Mak T.W., Ferrando A.A., Zúñiga-Pflücker J.C. HES1 opposes a PTEN-dependent check on survival, differentiation, and proliferation of TCRbeta-selected mouse thymocytes. Blood 2012, 120:1439-1448.
59. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 2005, 135:59-72.
60. Xu H., Qin S., Carrasco G.A., Dai Y., Filardo E.J., Prossnitz E.R., Battaglia G., DonCarlos L.L., Muma N.A. Extra-nuclear estrogen receptor GPR30 regulates serotonin function in rat hypothalamus. Neuroscience 2009, 158:1560-1599.
61. Yates M.A., Li Y., Chlebeck P.J., Offner H. GPR30, but not estrogen receptor-alpha, is crucial in the treatment of experimental autoimmune encephalomyelitis by oral ethinyl estradiol. BMC Immunol. 2010, 11:20.
62. Zhang Q.G., Wang R., Khan M., Mahesh V., Brann D.W. Role of Dickkopf-1, an antagonist of the Wnt/beta-catenin signaling pathway, in estrogen-induced neuroprotection and attenuation of tau phosphorylation. J. Neurosci. 2008, 28:8430-8441.
63. Zhang B., Subramanian S., Dziennis S., Jia J., Uchida M., Akiyoshi K., Migliati E., Lewis A.D., Vandenbark A.A., Offner H., Hurn P.D. Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. J. Immunol. 2010, 184:4087-4094.