Regulation of Constitutive GPR3 Signaling and Surface Localization by GRK2 and β-arrestin-2 Overexpression in HEK293 Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Lowther, Katie M ^a   Uliasz, Tracy F ^a   Götz, Konrad R ^b   Nikolaev, Viacheslav O ^b   Mehlmann, Lisa M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; CYCLIC AMP; DYNAMIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 3; G PROTEIN COUPLED RECEPTOR KINASE 2; UNCLASSIFIED DRUG; ADRBK1 PROTEIN, HUMAN; ARRB2 PROTEIN, HUMAN; GPR3 PROTEIN, HUMAN; GPR3 PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; INTERNALIZATION; INTRACELLULAR SIGNALING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HUMAN; INTRACELLULAR SPACE; METABOLISM; MOUSE; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

ANIMALS; BETA-ARRESTIN 2; CELL MEMBRANE; CYCLIC AMP; DYNAMINS; ENDOCYTOSIS; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HEK293 CELLS; HUMANS; INTRACELLULAR SPACE; MICE; MUTATION; PHOSPHORYLATION; PROTEIN DOMAINS; PROTEIN KINASE INHIBITORS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84879537892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065365     Document Type: Article

References (68)

1. Seifert R, Wenzel-Seifert K (2002) Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366, 381-416.
2. Maenhaut C, Van Sande J, Libert F, Abramowicz M, Parmentier M, et al. (1990) RDC8 codes for an adenosine A2 receptor with physiological constitutive activity. Biochem Biophys Res Commun 173, 1169-1178.
3. Song ZH, Young WS, Brownstein MJ, Bonner TI (1994) Molecular cloning of a novel candidate G protein-coupled receptor from rat brain. FEBS Lett 351, 375-379.
4. Eggerickx D, Denef JF, Labbe O, Hayashi Y, Refetoff S, et al. (1995) Molecular cloning of an orphan G-protein-coupled receptor that constitutively activates adenylate cyclase. Biochem J 309 (Pt 3), 837-843.
5. Freudzon L, Norris RP, Hand AR, Tanaka S, Saeki Y, et al. (2005) Regulation of meiotic prophase arrest in mouse oocytes by GPR3, a constitutive activator of the Gs G protein. J Cell Biol 171, 255-265.
6. Yin H, Chu A, Li W, Wang B, Shelton F, et al. (2009) Lipid G protein-coupled receptor ligand identification using beta-arrestin PathHunter assay. J Biol Chem 284, 12328-12338.
7. Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, et al. (2004) The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306, 1947-1950.
8. Ledent C, Demeestere I, Blum D, Petermans J, Hamalainen T, et al. (2005) Premature ovarian aging in mice deficient for Gpr3. Proc Natl Acad Sci U S A 102, 8922-8926.
9. Hinckley M., Vaccari S, Horner K, Chen R, Conti M (2005) The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol 287, 249-261.
10. Yang C, Wei Y, Qi S, Chen L, Zhang Q, et al. (2012) The G Protein Coupled Receptor 3 is involved in cAMP and cGMP Signaling and Maitenance of Meiotic Arrest in Porcine Oocytes. PLoS One 7, e38807.
11. DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, et al. (2008) Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol Reprod 78, 667-72.
12. Deng J, Lang S, Wylie C, Hammes SR (2008) The Xenopus laevis isoform of G protein-coupled receptor 3 (GPR3) is a constitutively active cell surface receptor that participates in maintaining meiotic arrest in X. laevis oocytes. Mol Endocrinol 22, 1853-1865.
13. Rios-Cardona D, Ricardo-Gonzalez RR, Chawla A, Ferrell JE, Jr. (2008) A role for GPRx, a novel GPR3/6/12-related G-protein coupled receptor, in the maintenance of meiotic arrest in Xenopus laevis oocytes. Dev Biol 317, 380-388.
14. Tanaka S, Shaikh IM, Chiocca EA, Saeki Y (2009) The Gs-linked receptor GPR3 inhibits the proliferation of cerebellar granule cells during postnatal development. PLoS One 4, e5922.
15. Tanaka S, Ishii K, Kasai K, Yoon SO, Saeki Y (2007) Neural expression of G protein-coupled receptors GPR3, GPR6, and GPR12 up-regulates cyclic AMP levels and promotes neurite outgrowth. J Biol Chem 282, 10506-10515.
16. Thathiah A, Spittaels K, Hoffmann M, Staes M, Cohen A, et al. (2009) The orphan G protein-coupled receptor 3 modulates amyloid-beta peptide generation in neurons. Science 323, 946-951.
17. Ruiz-Medina J, Ledent C, Valverde O (2011) GPR3 orphan receptor is involved in neuropathic pain after peripheral nerve injury and regulates morphine-induced antinociception. Neuropharmacology 61, 43-50.
18. Tourino C, Valjent E, Ruiz-Medina J, Herve D, Ledent C, et al. (2012) The orphan receptor GPR3 modulates early phases of cocaine reinforcement. Br J Pharmacol.
19. Valverde O, Celerier E, Baranyi M, Vanderhaeghen P, Maldonado R, et al. (2009) GPR3 receptor, a novel actor in the emotional-like responses. PLoS One 4, e4704.
20. Shenoy SK, Lefkowitz RJ (2003) Multifaceted roles of beta-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem J 375, 503-515.
21. Lefkowitz RJ, Shenoy SK (2005) Transduction of receptor signals by beta-arrestins. Science 308, 512-517.
22. Perry SJ, Baillie GS, Kohout TA, McPhee I, Magiera MM, et al. (2002) Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science 298, 834-836.
23. Kohout TA, Lefkowitz RJ (2003) Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol Pharmacol 63, 9-18.
24. Ferrandon S, Feinstein TN, Castro M, Wang B, Bouley R, et al. (2009) Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 5, 734-742.
25. Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, et al. (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7, e1000172.
26. Calebiro D, Nikolaev VO, Lohse MJ (2010) Imaging of persistent cAMP signaling by internalized G protein-coupled receptors. J Mol Endocrinol 45, 1-8.
27. Feinstein TN, Wehbi VL, Ardura JA, Wheeler DS, Ferrandon S, et al. (2011) Retromer terminates the generation of cAMP by internalized PTH receptors. Nat Chem Biol 7, 278-84.
28. Kotowski SJ, Hopf FW, Seif T, Bonci A, von Zastrow M (2011) Endocytosis promotes rapid dopaminergic signaling. Neuron 71, 278-90.
29. Mullershausen F, Zecri F, Cetin C, Billich A, Guerini D, et al. (2009) Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat Chem Biol 5, 428-434.
30. Fraile-Ramos A, Kohout TA, Waldhoer M, Marsh M (2003) Endocytosis of the viral chemokine receptor US28 does not require beta-arrestins but is dependent on the clathrin-mediated pathway. Traffic 4, 243-53.
31. Lowther KM, Nikolaev VO, Mehlmann LM (2011) Endocytosis in the mouse oocyte and its contribution to cAMP signaling during meiotic arrest. Reproduction 141, 737-747.
32. Thathiah A, Horre K, Snellinx A, Vandewyer E, Huang Y, et al. (2013) beta-arrestin 2 regulates Abeta generation and gamma-secretase activity in Alzheimer's disease. Nat Med 19, 43-9.
33. Cao TT, Mays RW, von Zastrow M (1998) Regulated endocytosis of G-protein-coupled receptors by a biochemically and functionally distinct subpopulation of clathrin-coated pits. J Biol Chem 273, 24592-24602.
34. Mehlmann LM, Carpenter G, Rhee SG, Jaffe LA (1998) SH2 domain-mediated activation of phospholipase Cgamma is not required to initiate Ca2+ release at fertilization of mouse eggs. Dev Biol 203, 221-232.
35. Ponsioen B, Zhao J, Riedl J, Zwartkruis F, van der Krogt G, et al. (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 5, 1176-1180.
36. Borner S, Schwede F, Schlipp A, Berisha F, Calebiro D, et al. (2011) FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat Protoc 6, 427-438.
37. Iancu RV, Ramamurthy G, Warrier S, Nikolaev VO, Lohse MJ, et al. (2008) Cytoplasmic cAMP concentrations in intact cardiac myocytes. Am J Physiol Cell Physiol 295, C414-22.
38. van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, et al. (1993) Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 122, 553-563.
39. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, et al. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10, 961-974.
40. Padmanabhan S, Myers AG, Prasad BM (2009) Constitutively active GPR6 is located in the intracellular compartments. FEBS Lett 583, 107-112.
41. Zhang BL, Li Y, Ding JH, Dong FL, Hou YJ, et al. (2012) Sphingosine 1-phosphate acts as an activator for the porcine Gpr3 of constitutively active G protein-coupled receptors. J Zhejiang Univ Sci B 13, 555-566.
42. Leurs R, Smit MJ, Alewijnse AE, Timmerman H (1998) Agonist-independent regulation of constitutively active G-protein-coupled receptors. Trends Biochem Sci 23, 418-422.
43. Droese J, Mokros T, Hermosilla R, Schulein R, Lipp M, et al. (2004) HCMV-encoded chemokine receptor US28 employs multiple routes for internalization. Biochem Biophys Res Commun 322, 42-49.
44. Miller WE, Houtz DA, Nelson CD, Kolattukudy PE, Lefkowitz RJ (2003) G-protein-coupled receptor (GPCR) kinase phosphorylation and beta-arrestin recruitment regulate the constitutive signaling activity of the human cytomegalovirus US28 GPCR. J Biol Chem 278, 21663-21671.
45. Mokros T, Rehm A, Droese J, Oppermann M, Lipp M, et al. (2002) Surface expression and endocytosis of the human cytomegalovirus-encoded chemokine receptor US28 is regulated by agonist-independent phosphorylation. J Biol Chem 277, 45122-45128.
46. Casarosa P, Bakker RA, Verzijl D, Navis M, Timmerman H, et al. (2001) Constitutive signaling of the human cytomegalovirus-encoded chemokine receptor US28. J Biol Chem 276, 1133-1137.
47. Fraile-Ramos A, Kledal TN, Pelchen-Matthews A, Bowers K, Schwartz TW, et al. (2001) The human cytomegalovirus US28 protein is located in endocytic vesicles and undergoes constitutive endocytosis and recycling. Mol Biol Cell 12, 1737-1749.
48. Waldhoer M, Casarosa P, Rosenkilde MM, Smit MJ, Leurs R, et al. (2003) The carboxyl terminus of human cytomegalovirus-encoded 7 transmembrane receptor US28 camouflages agonism by mediating constitutive endocytosis. J Biol Chem 278, 19473-19482.
49. Dupre DJ, Robitaille M, Ethier N, Villeneuve LR, Mamarbachi AM, et al. (2006) Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking. J Biol Chem 281, 34561-34573.
50. Dupre DJ, Baragli A, Rebois RV, Ethier N, Hebert TE (2007) Signalling complexes associated with adenylyl cyclase II are assembled during their biosynthesis. Cell Signal 19, 481-489.
51. El-Jouni W, Haun S, Hodeify R, Hosein Walker A, Machaca K (2007) Vesicular traffic at the cell membrane regulates oocyte meiotic arrest. Development 134, 3307-3315.
52. Damaj BB, McColl SR, Neote K, Songqing N, Ogborn KT, et al. (1996) Identification of G-protein binding sites of the human interleukin-8 receptors by functional mapping of the intracellular loops. Faseb J 10, 1426-1434.
53. Wade SM, Lim WK, Lan KL, Chung DA, Nanamori M, et al. (1999) G(i) activator region of alpha(2A)-adrenergic receptors: distinct basic residues mediate G(i) versus G(s) activation. Mol Pharmacol 56, 1005-1013.
54. Prezeau L, Richman JG, Edwards SW, Limbird LE (1999) The zeta isoform of 14-3-3 proteins interacts with the third intracellular loop of different alpha2-adrenergic receptor subtypes. J Biol Chem 274, 13462-13469.
55. Richman JG, Brady AE, Wang Q, Hensel JL, Colbran RJ, et al. (2001) Agonist-regulated Interaction between alpha2-adrenergic receptors and spinophilin. J Biol Chem 276, 15003-15008.
56. Wu G, Krupnick JG, Benovic JL, Lanier SM (1997) Interaction of arrestins with intracellular domains of muscarinic and alpha2-adrenergic receptors. J Biol Chem 272, 17836-17842.
57. Chee MJ, Morl K, Lindner D, Merten N, Zamponi GW, et al. (2008) The third intracellular loop stabilizes the inactive state of the neuropeptide Y1 receptor. J Biol Chem 283, 33337-33346.
58. Wehbi VL, Stevenson HP, Feinstein TN, Calero G, Romero G, et al. (2013) Noncanonical GPCR signaling arising from a PTH receptor-arrestin-Gbetagamma complex. Proc Natl Acad Sci U S A 110, 1530-5.
59. Dhami GK, Anborgh PH, Dale LB, Sterne-Marr R, Ferguson SS (2002) Phosphorylation-independent regulation of metabotropic glutamate receptor signaling by G protein-coupled receptor kinase 2. J Biol Chem 277, 25266-72.
60. Dicker F, Quitterer U, Winstel R, Honold K, Lohse MJ (1999) Phosphorylation-independent inhibition of parathyroid hormone receptor signaling by G protein-coupled receptor kinases. Proc Natl Acad Sci U S A 96, 5476-81.
61. Oppermann M, Freedman NJ, Alexander RW, Lefkowitz RJ (1996) Phosphorylation of the type 1A angiotensin II receptor by G protein-coupled receptor kinases and protein kinase C. J Biol Chem 271, 13266-72.
62. Ferguson SS (2007) Phosphorylation-independent attenuation of GPCR signalling. Trends Pharmacol Sci 28, 173-179.
63. Carman CV, Parent JL, Day PW, Pronin AN, Sternweis PM, et al. (1999) Selective regulation of Galpha(q/11) by an RGS domain in the G protein-coupled receptor kinase, GRK2. J Biol Chem 274, 34483-92.
64. Fernandez N, Gottardo FL, Alonso MN, Monczor F, Shayo C, et al. (2011) Roles of phosphorylation-dependent and-independent mechanisms in the regulation of histamine H2 receptor by G protein-coupled receptor kinase 2. J Biol Chem 286, 28697-28706.
65. Tobin AB (2008) G-protein-coupled receptor phosphorylation: where, when and by whom. Br J Pharmacol 153 Suppl 1, S167-176.
66. Saeki Y, Ueno S, Mizuno R, Nishimura T, Fujimura H, et al. (1993) Molecular cloning of a novel putative G protein-coupled receptor (GPCR21) which is expressed predominantly in mouse central nervous system. FEBS Lett 336, 317-322.
67. Kovanci E, Simpson JL, Amato P, Rohozinski J, Heard MJ, et al. (2008) Oocyte-specific G-protein-coupled receptor 3 (GPR3): no perturbations found in 82 women with premature ovarian failure (first report). Fertil Steril 90, 1269-71.
68. Zhou S, Wang B, Ni F, Wang J, Cao Y, et al. (2009) GPR3 may not be a potential candidate gene fore premature ovarian failure. Reprod Biomed Online 20, 53-5.