Phosphorylation-independent desensitization of GABAB receptor by GRK4

EMBO Journal

Volumn 22, Issue 15, 2003, Pages 3816-3824

  Perroy, Julie ^a   Adam, Lynda ^a   Qanbar, Riad ^a   Chénier, Sébastien ^a   Bouvier, Michel ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Desensitization; GABABreceptor; GRK4

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; ENZYME; G PROTEIN COUPLED RECEPTOR KINASE 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CEREBELLUM; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; GRANULE CELL; HUMAN; HUMAN CELL; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION;

BLOTTING, WESTERN; CELL LINE; CEREBELLUM; CYTOPLASMIC GRANULES; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GABA-B;

ANIMALIA;

EID: 0042575596     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg383     Document Type: Article

References (50)

1. Ambrose, C., James, M., Bames, G., Lin, C., Bates, G., Altherr, M., Duyao, M., Groot, N., Church, D. and Wasmuth, J.J. (1992) A novel G protein-coupled receptor kinase gene cloned from 4p16.3. Hum. Mol. Genet., 1, 697-703.
2. Angers, S., Salahpour, A., Joly, E., Hilairet, S., Chelsky, D., Dennis, M. and Bouvier, M. (2000) Detection of β2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl Acad. Sci. USA, 97, 3684-3689.
3. Ango, F., Albani-Torregrossa, S., Joly, C., Robbe, D., Michel, J.M., Pin, J.P., Bockaert, J. and Fagni, L. (1999) A simple method to transfer plasmid DNA into neuronal primary cultures: functional expression of the mGlu5 receptor in cerebellar granule cells. Neuropharmacology, 38, 793-803.
4. B receptors. Trends Neurosci, 24, 277-282.
5. Carman, C.V., Lisanti, M.P. and Benovic, J.L. (1999a) Regulation of G protein-coupled receptor kinases by caveolin. J. Biol. Chem., 274, 8858-8864.
6. Carman, C.V., Parent, J.L., Day, P.W., Pronin, A.N., Stemweis, P.M., Wedegaertner, P.B., Gilman, A.G., Benovic, J.L. and Kozasa, T. (1999b) Selective regulation of Gα(q/11) by an RGS domain in the G protein-coupled receptor kinase, GRK2. J. Biol. Chem., 274, 34483-34492.
7. Carman, C.V., Barak, L.S., Chen, C., Liu-Chen, L.Y., Onorato, J.J., Kennedy, S.P., Caron, M.G. and Benovic, J.L. (2000) Mutational analysis of Gβγ and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem., 275, 10443-10452.
8. Couve, A., Moss, S.J. and Pangalos, M.N. (2000) GABAB receptors: a new paradigm in G protein signaling. Mol. Cell. Neurosci., 16, 296-312.
9. Couve, A., Thomas, P., Calver, A.R., Hirst, W.D., Pangalos, M.N., Walsh, F.S., Smart, T.G. and Moss, S.J. (2002) Cyclic AMP-dependent protein kinase phosphorylation facilitates GABAB receptor-effector coupling. Nat. Neurosci., 5, 415-424.
10. Dale, L.B., Bhattacharya, M., Anborgh, P.H., Murdoch, B., Bhatia, M., Nakanishi, S. and Ferguson, S.G. (2000) G protein-coupled receptor kinase-mediated desensitization of metabotropic glutamate receptor 1A protects against cell death. J. Biol. Chem., 275, 38213-38220
11. Dhami, G.K., Anborgh, P.H., Dale, L.B., Sterne-Marr, R. and Ferguson, S.S. (2002) Phosphorylation-independent regulation of metabotropic glutamate receptor signaling by G protein-coupled receptor kinase 2. J. Biol. Chem., 277, 25266-25272.
12. Dicker, F., Quitterer, U., Winstel, R., Honold, K. and Lohse, M.J. (1999) Phosphorylation-independent inhibition of parathyroid hormone receptor signaling by G protein-coupled receptor kinases. Proc. Natl Acad. Sci. USA, 96, 5476-5481.
13. Diviani, D., Lattion, A.L. and Cotecchia, S. (1997) Characterization of the phosphorylation sites involved in G protein-coupled receptor kinase- and protein kinase C-mediated desensitization of the α1B-adrenergic receptor. J. Biol. Chem., 272, 28712-28719.
14. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001a) Duplexes of 21-nucleotide RNAs mediate RNA intcrference in cultured mammalian cells. Nature, 411, 494-498.
15. Elbashir, S.M., Martinez, J., Patkaniowska, A., Lendeckel, W. and Tuschl, T. (2001b) Functional anatomy of siRNAs for mediating efficient RNAI in Drosophila melanogaster embryo lysate. EMBO J., 20, 6877-6888.
16. Ferguson, S.S., Barak, L.S., Zhang, J. and Caron, M.G. (1996) G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins. Can. J. Physiol. Pharmacol., 74, 1095-1110.
17. Freedman, N.J., Ament, A.S., Oppermann, M., Stoffel, R.H., Exum, S.T. and Lefkowitz, R.J. (1997) Phosphorylation and desensitization of human endothelin A and B receptors. Evidence for G protein-coupled receptor kinase specificity. J. Biol. Chem., 272, 17734-17743.
18. Goodman, O.B., Jr, Krupnick, J.G., Gurevich, V.V., Benovic, J.L. and Keen, J.H. (1997) Arrestin/clathrin interaction. Localization of the arrestin binding locus to the clathrin terminal domain. J. Biol. Chem., 272, 15017-15022.
19. Hargrave, P.A. and McDowell, J.H. (1992) Rhodopsin and phototransduction: a model system for G protein-linked receptors. FASEB J., 6, 2323-2331.
20. Iacovelli, L., Sallese, M., Mariggio, S. and De Blasi, A. (1999) Regulation of G-protein-coupled receptor kinase subtypes by calcium sensor proteins. FASEB J., 13, 1-8.
21. Iacovelli, L. et al. (2003) Role of G protein-coupled receptor kinase 4 and β-arrestin 1 in agonist-stimulated metabotropic glutamate receptor 1 internalisation and activation of mitogen-activated protein kinases. J. Biol. Chem., 278, 12433-12442.
22. Ige, A.O., Bolam, J.P., Billinton, A., White, J.H., Marshall, F.H. and Emson, P.C. (2000) Cellular and sub-cellular localisation of GABA(B1) and GABA(B2) receptor proteins in the rat cerebellum. Mol. Brain Res., 83, 72-80.
23. Krupnick, J.G., Goodman, O.B., Jr, Keen, J.H. and Benovic, J.L. (1997) Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus. J. Biol. Chem., 272, 15011-15016.
24. Laporte, S.A., Oakley, R.H., Zhang, J., Holt, J.A., Ferguson, S.S., Caron, M.G. and Barak, L.S. (1999) The β2-adrenergic receptor/β-arrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl Acad. Sci. USA, 96, 3712-3717.
25. Laporte, S.A., Oakley, R.H., Holt, J.A., Barak, L.S. and Caron, M.G. (2000) The interaction of β-arrestin with the AP-2 adaptor is required for the clustering of β2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem., 275, 23120-23126.
26. Lavoie, C. et al. (2002) β1/β2-adrenergic receptor heterodimerization regulates β2-adrenergic receptor internalization and ERK signaling efficacy. J. Biol. Chem., 277, 35402-35410.
27. Mellon, P., Parker, V., Gluzman, Y. and Maniatis, T. (1981) Identification of DNA sequences required for transcription of the human α1-globin gene in a new SV40 host-vector system. Cell, 27, 279-288.
28. Mercier, J.F., Salahpour, A., Angers, S., Breit, A. and Bouvier, M. (2002) Quantitative assessment of β1- and β2-adrenergic receptor homo- and hetero-dimerization by bioluminescence resonance energy transfer. J. Biol. Chem., 277, 44925-44931.
29. Morello, J.P. et al. (2000) Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J. Clin. Invest., 105, 887-895.
30. Munshi, U.M., Peegel, H. and Menon, K.M. (2001) Palmitoylation of the luteinizing hormone/human chorionic gonadotropin receptor regulates receptor interaction with the arrestin-mediated internalization pathway. Eur. J. Biochem., 268, 1631-1639.
31. Naga Prasad, S.V., Barak, L.S., Rapacciuolo, A., Caron, M.G. and Rockman, H.A. (2001) Agonist-dependent recruitment of phosphoinositide 3-kinase to the membrane by β-adrenergic receptor kinase 1. A role in receptor sequestration. J. Biol. Chem., 276, 18953-18959.
32. Nelson, G., Chandrashekar, J., Hoon, M.A., Feng, L., Zhao, G., Ryba, N.J. and Zuker, C.S. (2002) An amino-acid taste receptor. Nature, 416, 199-202.
33. Petaja-Repo, U.E., Hogue, M., Bhalla, S., Laperriere, A., Morello, J.P. and Bouvier, M. (2002) Ligands act as pharmacological chaperones and increase the efficiency of delta opioid receptor maturation. EMBO J., 21, 1628-1637.
34. Pitcher, J.A. et al. (1992) Role of βγ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science, 257, 1264-1267.
35. Pitcher, J.A., Freedman, N.J. and Lefkowitz, R.J. (1998a) G protein-coupled receptor kinases. Annu. Rev. Biochem., 67, 653-692.
36. Pitcher, J.A. et al. (1998b) The G protein-coupled receptor kinase 2 is a microtubule-associated protein kinase that phosphorylates tubulin. J. Biol. Chem., 273, 12316-12324.
37. Premont, R.T., Inglese, J. and Lefkowitz, R.J. (1995) Protein kinases that phosphorylate activated G protein-coupled receptors. FASEB J., 9, 175-182.
38. Premont, R.T., Macrae, A.D., Stoffel, R.H., Chung, N., Pitcher, J.A., Ambrose, C., Inglese, J., MacDonald, M.E. and Lefkowitz, R.J. (1996) Characterization of the G protein-coupled receptor kinase GRK4. Identification of four splice variants. J. Biol. Chem., 271, 6403-6410.
39. Premont, R.T., Claing, A., Vitale, N., Freeman, J.L., Pitcher, J.A., Patton, W.A., Moss, J., Vaughan, M. and Lefkowitz, R.J. (1998) β2-adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc. Natl Acad. Sci. USA, 95, 14082-14087.
40. Sallese, M., Lombardi, M.S. and De Blasi, A. (1994) Two isoforms of G protein-coupled receptor kinase 4 identified by molecular cloning. Biochem. Biophys. Res. Commun., 199, 848-854.
41. Sallese, M., Mariggio, S., Collodel, G., Moretti, E., Piomboni, P., Baccetti, B. and De Blasi, A. (1997) G protein-coupled receptor kinase GRK4. Molecular analysis of the four isoforms and ultrastructural localization in spermatozoa and germinal cells. J. Biol. Chem., 272, 10188-10195.
42. Sallese, M., Mariggio, S., D'Urbano, E., Iacovelli, L. and De Blasi, A. (2000a) Selective regulation of Gq signaling by G protein-coupled receptor kinase 2: direct interaction of kinase N terminus with activated Gαq. Mol. Pharmacol., 57, 826-831.
43. Sallese, M., Salvatore, L., D'Urbano, E., Sala, G., Storto, M., Launey, T., Nicoletti, F., Knopfel, T. and De Blasi, A. (2000b) The G-protein-coupled receptor kinase GRK4 mediates homologous desensitization of metabotropic glutamate receptor 1. FASEB J., 14, 2569-2580.
44. Shiina, T., Arai, K., Tanabe, S., Yoshida, N., Haga, T., Nagao, T. and Kurose, H. (2001) Clathrin box in G protein-coupled receptor kinase 2. J. Biol. Chem., 276, 33019-33026.
45. Usui, H. et al. (2000) RGS domain in the amino-terminus of G protein-coupled receptor kinase 2 inhibits Gq-mediated signaling. Int. J. Mol. Med., 5, 335-340.
46. Van Vliet, B.J., Sebben, M., Dumuis, A., Gabrion, J., Bockaert, J. and Pin, J.P. (1989) Endogenous amino acid release from cultured cerebellar neuronal cells: effect of tetanus toxin on glutamate release. J. Neurochem., 52, 1229-1239.
47. Virlon, B., Firsov, D., Cheval, L., Reiter, E., Troispoux, C., Guillou, F. and Elalouf, J.M. (1998) Rat G protein-coupled receptor kinase GRK4: identification, functional expression and differential tissue distribution of two splice variants. Endocrinology, 139, 2784-2795.
48. Watanabe, H., Xu, J., Bengra, C., Jose, P.A. and Felder, R.A. (2002) Desensitization of human renal D1 dopamine receptors by G protein-coupled receptor kinase 4. Kidney Int., 62, 790-798.
49. Weiss, E.R., Ducceschi, M.H., Horner, T.J., Li, A., Craft, C.M. and Osawa, S. (2001) Species-specific differences in expression of G-protein-coupled receptor kinase (GRK) 7 and GRK1 in mammalian cone photoreceptor cells: implications for cone cell phototransduction. J. Neurosci., 21, 9175-9184.
50. Xu, Y., Piston, D.W. and Johnson, C.H. (1999) A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc. Natl Acad. Sci. USA, 96, 151-156.