G protein-coupled estrogen receptor 1/G protein-coupled receptor 30 localizes in the plasma membrane and traffics intracellularly on cytokeratin intermediate filaments

Molecular Pharmacology

Volumn 79, Issue 3, 2011, Pages 400-410

  Sandén, Caroline ^a   Broselid, Stefan ^a   Cornmark, Louise ^a   Andersson, Krister ^a   Daszkiewicz Nilsson, Joanna ^a   Mårtensson, Ulrika E A ^a   Olde, Björn ^a   Leeb Lundberg, L M Fredrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; CELL SURFACE RECEPTOR; CYCLIC AMP; CYTOKERATIN; CYTOKERATIN 7; CYTOKERATIN 8; ESTRADIOL; G PROTEIN COUPLED RECEPTOR 30;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELL MEMBRANE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; MICROTUBULE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; ARRESTINS; CYCLIC AMP; DOGS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; INTERMEDIATE FILAMENTS; KERATINS; MICE; MICROSCOPY, FLUORESCENCE; POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; TUMOR CELLS, CULTURED;

EID: 79951987933     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.069500     Document Type: Article

References (47)

1. Ahola TM, Manninen T, Alkio N, and Ylikomi T (2002) G protein-coupled receptor 30 is critical for a progestin-induced growth inhibition in MCF-7 breast cancer cells. Endocrinology 143:3376-3384. (Pubitemid 34925712)
2. Ariazi EA, Brailoiu E, Yerrum S, Shupp HA, Slifker MJ, Cunliffe HE, Black MA, Donato AL, Arterburn JB, Oprea TI, et al. (2010) The G protein-coupled receptor GPR30 inhibits proliferation of estrogen receptor-positive breast cancer cells. Cancer Res 70:1184-1194.
3. Barak LS, Ferguson SS, Zhang J, and Caron MG (1997) A beta-arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J Biol Chem 272:27497-27500. (Pubitemid 27473532)
4. Bologa CG, Revankar CM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA, et al. (2006) Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2:207-212.
5. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, and Dun NJ (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193:311-321.
6. Brothers SP, Janovick JA, and Conn PM (2003) Unexpected effects of epitope and chimeric tags on gonadotropin-releasing hormone receptors: implications for understanding the molecular etiology of hypogonadotropic hypogonadism. J Clin Endocrinol Metab 88:6107-6112. (Pubitemid 38033099)
7. Chomczynski P and Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159. (Pubitemid 17064313)
8. Enquist J, Skröder C, Whistler JL, and Leeb-Lundberg LM (2007) Kinins promote B2 receptor endocytosis and delay constitutive B1 receptor endocytosis. Mol Pharmacol 71:494-507. (Pubitemid 46147916)
9. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari HM, and Goldman RD (2009) Introducing intermediate filaments: from discovery to disease. J Clin Invest 119:1763-1771.
10. Ferrero M, Spyratos F, Desplaces A, Andrieu C, Phillips E, and Rouëssé J (1989) Cytokeratin analysis of breast and leukemia tumor cell lines by flow cytometry. Biol Cell 65:305-308. (Pubitemid 19162735)
11. Filardo E, Quinn J, Pang Y, Graeber C, Shaw S, Dong J, and 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)
12. Filardo EJ, Graeber CT, Quinn JA, Resnick MB, Giri D, DeLellis RA, Steinhoff MM, and Sabo E (2006) Distribution of GPR30, a seven membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathologic determinants of tumor progression. Clin Cancer Res 12:6359-6366. (Pubitemid 44799705)
13. Filardo EJ, Quinn JA, Frackelton AR Jr., and 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. (Pubitemid 34044499)
14. Filardo EJ and Thomas P (2005) GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab 16:362-367. (Pubitemid 41338741)
15. Funakoshi T, Yanai A, Shinoda K, Kawano MM, and Mizukami Y (2006) G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 346:904-910.
16. Galandrin S and Bouvier M (2006) Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol Pharmacol 70:1575-1584.
17. Gires O, Andratschke M, Schmitt B, Mack B, and Schaffrik M (2005) Cytokeratin 8 associates with the external leaflet of plasma membranes in tumour cells. Biochem Biophys Res Commun 328:1154-1162. (Pubitemid 40238755)
18. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Ström A, Treuter E, Warner M, et al. (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87:905-931. (Pubitemid 47084672)
19. Heuser JE and Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389-400. (Pubitemid 19065841)
20. Kenakin T (2007) Functional selectivity through protean and biased agonism: who steers the ship? Mol Pharmacol 72:1393-1401.
21. Kolkova Z, Noskova V, Ehinger A, Hansson S, and Casslén B (2010) G protein-coupled estrogen receptor 1 (GPER, GPR 30) in normal human endometrium and early pregnancy decidua. Mol Hum Reprod 16:743-751.
22. Kotarsky K, Owman C, and Olde B (2001) A chimeric reporter gene allowing for clone selection and high-throughput screening of reporter cell lines expressing G-protein-coupled receptors. Anal Biochem 288:209-215. (Pubitemid 32057987)
23. Lin BC, Suzawa M, Blind RD, Tobias SC, Bulun SE, Scanlan TS, and Ingraham HA (2009) Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation. Cancer Res 69:5415-5423.
24. Long X and Nephew KP (2006) Fulvestrant (ICI 182,780)-dependent interacting proteins mediate immobilization and degradation of estrogen receptor-alpha. J Biol Chem 281:9607-9615. (Pubitemid 43864679)
25. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, and Andò S (2004) The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279:27008-27016. (Pubitemid 38812536)
26. Mårtensson UE, Salehi SA, Windahl S, Gomez MF, Swärd K, Daszkiewicz-Nilsson J, Wendt A, Andersson N, Hellstrand P, Grände PO, et al. (2009) Deletion of the G protein-coupled receptor GPR30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice. Endocrinology 150:687-698.
27. Matsuda K, Sakamoto H, Mori H, Hosokawa K, Kawamura A, Itose M, Nishi M, Prossnitz ER, and Kawata M (2008) Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci Lett 441:94-99.
28. Meier KE, Snavely MD, Brown SL, Brown JH, and Insel PA (1983) Alpha 1- and beta 2-adrenergic receptor expression in the Madin-Darby canine kidney epithelial cell line. J Cell Biol 97:405-415.
29. Moll R, Divo M, and Langbein L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129:705-733.
30. Olde B and Leeb-Lundberg LM (2009) GPR30/GPER1: searching for a role in estrogen physiology. Trends Endocrinol Metab 20:409-416.
31. Olink-Coux M, Arcangeletti C, Pinardi F, Minisini R, Huesca M, Chezzi C, and Scherrer K (1994) Cytolocation of prosome antigens on intermediate filament subnetworks of cytokeratin, vimentin and desmin type. J Cell Sci 107:353-366. (Pubitemid 24091843)
32. Otto C, Rohde-Schulz B, Schwarz G, Fuchs I, Klewer M, Brittain D, Langer G, Bader B, Prelle K, Nubbemeyer R, et al. (2008) G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology 149:4846-4856.
33. Pandey DP, Lappano R, Albanito L, Madeo A, Maggiolini M, and Picard D (2009) Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO J 28:523-532.
34. Pollack V, Scheiber K, Pfaller W, and Schramek H (1997) Loss of cytokeratin expression and formation of actin stress fibers in dedifferentiated MDCK-C7 cell lines. Biochem Biophys Res Commun 241:541-547. (Pubitemid 28020137)
35. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, and Hathaway HJ (2008) Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165-190. (Pubitemid 351738176)
36. Razandi M, Pedram A, Merchenthaler I, Greene GL, and Levin ER (2004) Plasma membrane estrogen receptors exist and functions as dimers. Mol Endocrinol 18:2854-2865. (Pubitemid 39577911)
37. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, and Prossnitz ER (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630. (Pubitemid 40354745)
38. Revankar CM, Mitchell HD, Field AS, Burai R, Corona C, Ramesh C, Sklar LA, Arterburn JB, and Prossnitz ER (2007) Synthetic estrogen derivatives demonstrate the functionality of intracellular GPR30. ACS Chem Biol 2:536-544. (Pubitemid 350011324)
39. Sakamoto H, Matsuda K, Hosokawa K, Nishi M, Morris JF, Prossnitz ER, and Kawata M (2007) Expression of G protein-coupled receptor-30, a G protein-coupled membrane estrogen receptor, in oxytocin neurons of the rat paraventricular and supraoptic nuclei. Endocrinology 148:5842-5850. (Pubitemid 350146173)
40. Schweizer J, Bowden PE, Coulombe PA, Langbein L, Lane EB, Magin TM, Maltais L, Omary MB, Parry DA, Rogers MA, et al. (2006) New consensus nomenclature for mammalian keratins. J Cell Biol 174:169-174. (Pubitemid 44079852)
41. Smith HO, Leslie KK, Singh M, Qualls CR, Revankar CM, Joste NE, and Prossnitz ER (2007) GPR30: a novel indicator of poor survival for endometrial carcinoma. Am J Obstet Gynecol 196:386.e1-e11.
42. Styers ML, Salazar G, Love R, Peden AA, Kowalczyk AP, and Faundez V (2004) The endo-lysosomal sorting machinery interacts with the intermediate filament cytoskeleton. Mol Biol Cell 15:5369-5382. (Pubitemid 39564731)
43. Thomas P, Pang Y, Filardo EJ, and Dong J (2005) Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146:624-632. (Pubitemid 40129818)
44. Toivola DM, Tao GZ, Habtezion A, Liao J, and Omary MB (2005) Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments. Trends Cell Biol 15:608-617. (Pubitemid 41619425)
45. Vijayaraj P, Kröger C, Reuter U, Windoffer R, Leube RE, and Magin TM (2009) Keratins regulate protein biosynthesis through localization of GLUT1 and -3 upstream of AMP kinase and Raptor. J Cell Biol 187:175-184.
46. Whistler JL, Enquist J, Marley A, Fong J, Gladher F, Tsuruda P, Murray SR, and Von Zastrow M (2002) Modulation of postendocytic sorting of G protein-coupled receptors. Science 297:615-620. (Pubitemid 34815348)
47. Windahl SH, Andersson N, Chagin AS, Mårtensson UE, Carlsten H, Olde B, Swanson C, Movérare-Skrtic S, Sävendahl L, Lagerquist MK, et al. (2009) The role of the G protein-coupled receptor GPR30 in the effects of estrogen in ovariectomized mice. Am J Physiol Endocrinol Metab 296:E490-E496.