Mechanisms of estradiol-induced insulin secretion by the G protein-coupled estrogen receptor GPR30/GPER in pancreatic β-cells

Endocrinology

Volumn 152, Issue 8, 2011, Pages 3030-3039

  Sharma, Geetanjali ^a   Prossnitz, Eric R ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; G PROTEIN COUPLED RECEPTOR 30; GLUCOSE; INSULIN; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ESTROGEN ACTIVITY; FEMALE; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLOPENTANES; ESTRADIOL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLINOSITOL 3-KINASES; QUINOLINES; RECEPTORS, G-PROTEIN-COUPLED;

EID: 79960705272     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-0091     Document Type: Article

References (52)

1. Liu S, Mauvais-Jarvis F 2010 Minireview: estrogenic protection of β-cell failure in metabolic diseases. Endocrinology 151:859-864
2. Mauvais-Jarvis F 2011 Estrogen and androgen receptors: regulators of fuel homeostasis and emerging targets for diabetes and obesity. Trends Endocrinol Metab 22:24-33
3. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A 2006 The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environ Health Perspect 114:106-112 (Pubitemid 43056876)
4. Casals-Casas C, Desvergne B 2011 Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73:135-162
5. Szkudelska K, Nogowski L 2007 Genistein - a dietary compound inducing hormonal and metabolic changes. J Steroid Biochem Mol Biol 105:37-45 (Pubitemid 47211954)
6. Watson CS, Jeng YJ, Kochukov MY 2010 Nongenomic signaling pathways of estrogen toxicity. Toxicol Sci 115:1-11
7. Hewitt SC, Harrell JC, Korach KS 2005 Lessons in estrogen biology from knockout and transgenic animals. Annu Rev Physiol 67:285-308 (Pubitemid 40404493)
8. Levin ER 2008 Rapid signaling by steroid receptors. Am J Physiol Regul Integr Comp Physiol 295:R1425-R1430
9. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ 2008 Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165-190 (Pubitemid 351738176)
10. Filardo E, Quinn J, Pang Y, Graeber C, Shaw S, Dong J, Thomas P 2007 Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology 148:3236-3245 (Pubitemid 46997004)
11. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Andò S, Maggiolini M 2007 G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67:1859-1866 (Pubitemid 46383413)
12. Filardo EJ, Quinn JA, Frackelton Jr AR, Bland KI 2002 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 16:70-84
13. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER 2005 A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630 (Pubitemid 40354745)
14. Mizukami Y 2010 In vivo functions of GPR30/GPER-1, a membrane receptor for estrogen: from discovery to functions in vivo. Endocr J 57:101-107
15. Schneider JG, Tompkins C, Blumenthal RS, Mora S 2006 The metabolic syndrome in women. Cardiol Rev 14:286-291 (Pubitemid 44624587)
16. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS 2000 Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc Natl Acad Sci USA 97:12729-12734
17. Jones ME, Thorburn AW, Britt KL, Hewitt KN, Wreford NG, Proietto J, Oz OK, Leury BJ, Robertson KM, Yao S, Simpson ER 2000 Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc Natl Acad Sci USA 97:12735-12740
18. Nadal A, Alonso-Magdalena P, Soriano S, Ripoll C, Fuentes E, Quesada I, Ropero AB 2011 Role of estrogen receptors α,β and GPER1/GPR30 in pancreatic β-cells. Front Biosci 16:251-260
19. Balhuizen A, Kumar R, Amisten S, Lundquist I, Salehi A 2010 Activation of G protein-coupled receptor 30 modulates hormone secretion and counteracts cytokine-induced apoptosis in pancreatic islets of female mice. Mol Cell Endocrinol 320:16-24
20. Liu S, Le May C, Wong WP, Ward RD, Clegg DJ, Marcelli M, Korach KS, Mauvais-Jarvis F 2009 Importance of extranuclear estrogen receptor-α and membrane G protein-coupled estrogen receptor in pancreatic islet survival. Diabetes 58:2292-2302
21. Mårtensson UE, Salehi SA, Windahl S, Gomez MF, Swärd K, Daszkiewicz-Nilsson J, Wendt A, Andersson N, Hellstrand P, Grände PO, Owman C, Rosen CJ, Adamo ML, Lundquist I, Rorsman P, Nilsson BO, Ohlsson C, Olde B, Leeb-Lundberg LM 2009 Deletion of the G protein-coupled receptor 30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice. Endocrinology 150:687-698
22. Bologa CG, Revankar CM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA, Oprea TI, Prossnitz ER 2006 Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2:207-212
23. Dennis MK, Burai R, Ramesh C, Petrie WK, Alcon SN, Nayak TK, Bologa CG, Leitao A, Brailoiu E, Deliu E, Dun NJ, Sklar LA, Hathaway HJ, Arterburn JB, Oprea TI, Prossnitz ER 2009 In vivo effects of a GPR30 antagonist. Nat Chem Biol 5:421-427
24. Miyazaki J, Araki K, Yamato E, Ikegami H, Asano T, Shibasaki Y, Oka Y, Yamamura K 1990 Establishment of a pancreatic β cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127:126-132 (Pubitemid 20228111)
25. Wang C, Dehghani B, Magrisso IJ, Rick EA, Bonhomme E, Cody DB, Elenich LA, Subramanian S, Murphy SJ, Kelly MJ, Rosenbaum JS, Vandenbark AA, Offner H 2008 GPR30 contributes to estrogen-induced thymic atrophy. Mol Endocrinol 22:636-648 (Pubitemid 351397791)
26. Carter JD, Dula SB, Corbin KL, Wu R, Nunemaker CS 2009 A practical guide to rodent islet isolation and assessment. Biol Proced Online 11:3-31
27. Al-Majed HT, Squires PE, Persaud SJ, Huang GC, Amiel S, Whitehouse BJ, Jones PM 2005 Effect of 17β-estradiol on insulin secretion and cytosolic calcium in Min6 mouse insulinoma cells and human islets of Langerhans. Pancreas 30:307-313 (Pubitemid 40586806)
28. Liu D, Zhen W, Yang Z, Carter JD, Si H, Reynolds KA 2006 Genistein acutely stimulates insulin secretion in pancreatic β-cells through a cAMP-dependent protein kinase pathway. Diabetes 55:1043-1050 (Pubitemid 44100180)
29. Sandén C, Broselid S, Cornmark L, Andersson K, Daszkiewicz-Nilsson J, Mårtensson UE, Olde B, Leeb-Lundberg LM 2011 G protein-coupled estrogen receptor 1/G protein-coupled receptor 30 localizes in the plasma membrane and traffics intracellularly on cytokeratin intermediate filaments. Mol Pharmacol 79:400-410
30. Kasai H, Hatakeyama H, Ohno M, Takahashi N 2010 Exocytosis in islet β-cells. Adv Exp Med Biol 654:305-338
31. Filardo EJ, Quinn JA, Bland KI, Frackelton Jr AR 2000 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 14:1649-1660
32. Benes C, Roisin MP, Van Tan H, Creuzet C, Miyazaki J, Fagard R 1998 Rapid activation and nuclear translocation of mitogen-activated protein kinases in response to physiological concentration of glucose in the MIN6 pancreatic β cell line. J Biol Chem 273:15507-15513 (Pubitemid 28298160)
33. Srinivasan S, Bernal-Mizrachi E, Ohsugi M, Permutt MA 2002 Glucose promotes pancreatic islet β-cell survival through a PI 3-kinase/Akt- signaling pathway. Am J Physiol Endocrinol Metab 283:E784-E793
34. Brown LM, Clegg DJ 2010 Central effects of estradiol in the regulation of food intake, body weight, and adiposity. J Steroid Biochem Mol Biol 122:65-73
35. Nadal A, Alonso-Magdalena P, Soriano S, Ropero AB, Quesada I 2009 The role of oestrogens in the adaptation of islets to insulin resistance. J Physiol 587:5031-5037
36. Leiter EH 1982 Multiple low-dose streptozotocin-induced hyperglycemia and insulitis in C57BL mice: influence of inbred background, sex, and thymus. Proc Natl Acad Sci USA 79:630-634 (Pubitemid 12137765)
37. Yamabe N, Kang KS, Zhu BT 2010 Beneficial effect of 17β-estradiol on hyperglycemia and islet β-cell functions in a streptozotocin-induced diabetic rat model. Toxicol Appl Pharmacol 249:76-85
38. Ribas V, Nguyen MT, Henstridge DC, Nguyen AK, Beaven SW, Watt MJ, Hevener AL 2010 Impaired oxidative metabolism and inflammation are associated with insulin resistance in ERα-deficient mice. Am J Physiol Endocrinol Metab 298:E304-E319
39. Nadal A, Rovira JM, Laribi O, Leon-quinto T, Andreu E, Ripoll C, Soria B 1998 Rapid insulinotropic effect of 17β-estradiol via a plasma membrane receptor. FASEB J 12:1341-1348 (Pubitemid 28475575)
40. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B 2000 Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor α and estrogen receptor β. Proc Natl Acad Sci USA 97:11603-11608
41. Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y 2006 G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 346:904-910
42. Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, BaquiéM, Gauthier BR, Nef S, Stefani E, Nadal A 2008 A Pancreatic insulin content regulation by the estrogen receptor ERα. PLoS One 3:e2069
43. Al-Majed HT, Jones PM, Persaud SJ, Sugden D, Huang GC, Amiel S, Whitehouse BJ 2004 ACTH stimulates insulin secretion from MIN6 cells and primary mouse and human islets of Langerhans. J Endocrinol 180:155-166 (Pubitemid 38180767)
44. Filardo EJ 2002 Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 80:231-238 (Pubitemid 34233742)
45. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Andò S 2004 The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17β-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279:27008-27016 (Pubitemid 38812536)
46. Youl E, Bardy G, Magous R, Cros G, Sejalon F, Virsolvy A, Richard S, Quignard JF, Gross R, Petit P, Bataille D, Oiry C 2010 Quercetin potentiates insulin secretion and protects INS-1 pancreatic β-cells against oxidative damage via the ERK1/2 pathway. Br J Pharmacol 161:799-814
47. Longuet C, Broca C, Costes S, Hani EH, Bataille D, Dalle S 2005 Extracellularly regulated kinases 1/2 (p44/42 mitogen-activated protein kinases) phosphorylate synapsin I and regulate insulin secretion in the MIN6 β-cell line and islets of Langerhans. Endocrinology 146:643-654 (Pubitemid 40129820)
48. Hagiwara S, Sakurai T, Tashiro F, Hashimoto Y, Matsuda Y, Nonomura Y, Miyazaki J 1995 An inhibitory role for phosphatidylinositol 3-kinase in insulin secretion from pancreatic B cell line MIN6. Biochem Biophys Res Commun 214:51-59
49. Miettinen P, Ormio P, Hakonen E, Banerjee M, Otonkoski T 2008 EGF receptor in pancreatic β-cell mass regulation. Biochem Soc Trans 36:280-285 (Pubitemid 351839316)
50. Lee HY, Yea K, Kim J, Lee BD, Chae YC, Kim HS, Lee DW, Kim SH, Cho JH, Jin CJ, Koh DS, Park KS, Suh PG, Ryu SH 2008 Epidermal growth factor increases insulin secretion and lowers blood glucose in diabetic mice. J Cell Mol Med 12:1593-1604
51. Collier JJ, White SM, Dick GM, Scott DK 2004 Phosphatidylinositol 3-kinase inhibitors reveal a unique mechanism of enhancing insulin secretion in 832/13 rat insulinoma cells. Biochem Biophys Res Commun 324:1018-1023 (Pubitemid 39361610)
52. Yang W, Wang S, Li L, Liang Z, Wang L 2011 Genistein reduces hyperglycemia and islet cell loss in a high-dosage manner in rats with alloxan-induced pancreatic damage. Pancreas 40:396-402