Nonenzymatic rapid control of GIRK channel function by a G protein-coupled receptor kinase

Cell

Volumn 143, Issue 5, 2010, Pages 750-760

  Raveh, Adi ^a   Cooper, Ayelet ^a   Guy David, Liora ^a   Reuveny, Eitan ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED RECEPTOR KINASE; GREEN FLUORESCENT PROTEIN;

ARTICLE; DESENSITIZATION; DOWN REGULATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

EID: 79251506646     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.10.018     Document Type: Article

References (63)

1. Aragay, A.M., Ruiz-Gomez, A., Penela, P., Sarnago, S., Elorza, A., Jimenez- Sainz, M.C., and Mayor, F., Jr. (1998). G protein-coupled receptor kinase 2 (GRK2): mechanisms of regulation and physiological functions. FEBS Lett. 430, 37-40.
2. Bender, K., Wellner-Kienitz, M.C., Inanobe, A., Meyer, T., Kurachi, Y., and Pott, L. (2001). Overexpression of monomeric and multimeric GIRK4 subunits in rat atrial myocytes removes fast desensitization and reduces inward rectification of muscarinic K(+) current (I(K(ACh))). Evidence for functional homomeric GIRK4 channels. J. Biol. Chem. 276, 28873-28880.
3. Berlot, C.H. (2002). A highly effective dominant negative alpha s construct containing mutations that affect distinct functions inhibits multiple Gs-coupled receptor signaling pathways. J. Biol. Chem. 277, 21080-21085.
4. Blanchet, C., and Luscher, C. (2002). Desensitization of mu-opioid receptorevoked potassium currents: initiation at the receptor, expression at the effector. Proc. Natl. Acad. Sci. USA 99, 4674-4679.
5. Bunemann, M., Lee, K.B., Pals-Rylaarsdam, R., Roseberry, A.G., and Hosey, M.M. (1999). Desensitization of G-protein-coupled receptors in the cardiovascular system. Annu. Rev. Physiol. 61, 169-192.
6. Carman, C.V., Parent, J.L., Day, P.W., Pronin, A.N., Sternweis, P.M., Wedegaertner, P.B., Gilman, A.G., Benovic, J.L., and Kozasa, T. (1999). Selective regulation of Galpha(q/11) by an RGS domain in the G proteincoupled 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 Gbetagamma and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 275 10443-10452
8. Clancy, S.M., Fowler, C.E., Finley, M., Suen, K.F., Arrabit, C., Berton, F., Kosaza, T., Casey, P.J., and Slesinger, P.A. (2005). Pertussis-toxin- sensitive Galpha subunits selectively bind to C-terminal domain of neuronal GIRK channels: evidence for a heterotrimeric G-protein-channel complex. Mol. Cell. Neurosci. 28, 375-389.
9. Claycomb, W.C., Lanson, N.A., Jr., Stallworth, B.S., Egeland, D.B., Delcarpio, J.B., Bahinski, A., and Izzo, N.J., Jr. (1998). HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc. Natl. Acad. Sci. USA 95, 2979-2984.
10. Cordeaux, Y., Ijzerman, A.P., and Hill, S.J. (2004). Coupling of the human A1 adenosine receptor to different heterotrimeric G proteins: evidence for agonist-specific G protein activation. Br. J. Pharmacol. 143, 705-714.
11. Dang, V.C., Napier, I.A., and Christie, M.J. (2009). Two distinct mechanisms mediate acute mu-opioid receptor desensitization in native neurons. J. Neurosci. 29, 3322-3327.
12. Day, P.W., Tesmer, J.J., Sterne-Marr, R., Freeman, L.C., Benovic, J.L., and Wedegaertner, P.B. (2004). Characterization of the GRK2 binding site of Galphaq. J. Biol. Chem. 279, 53643-53652.
13. Dhami, G.K., Dale, L.B., Anborgh, P.H., O'Connor-Halligan, K.E., Sterne-Marr, R., and Ferguson, S.S. (2004). G Protein-coupled receptor kinase 2 regulator of G protein signaling homology domain binds to both metabotropic glutamate receptor 1a and Galphaq to attenuate signaling. J. Biol. Chem. 279, 16614-16620.
14. Doupnik, C.A. (2008). GPCR-Kir channel signaling complexes: defining rules of engagement. J. Recept. Signal Transduct. Res. 28, 83-91.
15. Dupre, D.J., Robitaille, M., Rebois, R.V., and Hebert, T.E. (2009). The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu. Rev. Pharmacol. Toxicol. 49, 31-56.
16. Ferguson, S.S. (2007). Phosphorylation-independent attenuation of GPCR signalling. Trends Pharmacol. Sci. 28, 173-179.
17. Garcia-Higuera, I., Penela, P., Murga, C., Egea, G., Bonay, P., Benovic, J.L., and Mayor, F., Jr. (1994). Association of the regulatory beta-adrenergic receptor kinase with rat liver microsomal membranes. J. Biol. Chem. 269, 1348-1355.
18. Goedhart, J., Vermeer, J.E., Adjobo-Hermans, M.J., van Weeren, L., and Gadella, T.W., Jr. (2007). Sensitive detection of p65 homodimers using red-shifted and fluorescent protein-based FRET couples. PLoS ONE 2, e1011.
19. Huang, C.L., Feng, S., and Hilgemann, D.W. (1998). Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391, 803-806.
20. Keselman, I., Fribourg, M., Felsenfeld, D.P., and Logothetis, D.E. (2007). Mechanism of PLC-mediated Kir3 current inhibition. Channels (Austin) 1, 113-123.
21. Kobrinsky, E., Mirshahi, T., Zhang, H., Jin, T., and Logothetis, D.E. (2000). Receptor-mediated hydrolysis of plasma membrane messenger PIP2 leads to K+-current desensitization. Nat. Cell Biol. 2, 507-514.
22. Koike-Tani, M., Collins, J.M., Kawano, T., Zhao, P., Zhao, Q., Kozasa, T., Nakajima, S., and Nakajima, Y. (2005). Signal transduction pathway for the substance P-induced inhibition of rat Kir3 (GIRK) channel. J. Physiol. 564, 489-500.
23. Kong, G., Penn, R., and Benovic, J.L. (1994). A beta-adrenergic receptor kinase dominant negative mutant attenuates desensitization of the beta 2-adrenergic receptor. J. Biol. Chem. 269, 13084-13087.
24. Krapivinsky, G., Krapivinsky, L., Wickman, K., and Clapham, D.E. (1995). G beta gamma binds directly to the G protein-gated K+ channel, IKACh. J. Biol. Chem. 270, 29059-29062.
25. Kremers, G.J., Goedhart, J., van Munster, E.B., and Gadella, T.W., Jr. (2006). Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 45, 6570-6580.
26. Li, J., Xiang, B., Su, W., Zhang, X., Huang, Y., and Ma, L. (2003). Agonistinduced formation of opioid receptor-G protein-coupled receptor kinase (GRK)-G beta gamma complex on membrane is required for GRK2 function in vivo. J. Biol. Chem. 278, 30219-30226.
27. Lleres, D., Swift, S., and Lamond, A.I. (2007). Detecting protein-protein interactions in vivo with FRET using multiphoton fluorescence lifetime imaging microscopy (FLIM). Curr. Protoc. Cytom. Chapter 12, Unit12.10.
28. Logothetis, D.E., Kurachi, Y., Galper, J., Neer, E.J., and Clapham, D.E. (1987). The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature 325, 321-326.
29. Massoulie, J., Pezzementi, L., Bon, S., Krejci, E., and Vallette, F.M. (1993). Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 41, 31-91.
30. Meyer, T., Wellner-Kienitz, M.C., Biewald, A., Bender, K., Eickel, A., and Pott, L. (2001). Depletion of phosphatidylinositol 4, 5-bisphosphate by activation of phospholipase C-coupled receptors causes slow inhibition but not desensitization of G protein-gated inward rectifier K+ current in atrial myocytes. J. Biol. Chem. 276, 5650-5658.
31. Murga, C., Penela, P., Zafra, F., and Mayor, F., Jr. (1998). The subcellular and cellular distribution of G protein-coupled receptor kinase 2 in rat brain. Neuroscience 87, 631-637.
32. Nikolov, E.N., and Ivanova-Nikolova, T.T. (2004). Coordination of membrane excitability through a GIRK1 signaling complex in the atria. J. Biol. Chem. 279, 23630-23636.
33. Nobles, M., Sebastian, S., and Tinker, A. (2010). HL-1 cells express an inwardly rectifying K+ current activated via muscarinic receptors comparable to that in mouse atrial myocytes. Pflugers Arch. 460, 99-108.
34. Palczewski, K. (1997). GTP-binding-protein-coupled receptor kinases-two mechanistic models. Eur. J. Biochem. 248, 261-269.
35. Peter, M., Ameer-Beg, S.M., Hughes, M.K., Keppler, M.D., Prag, S., Marsh, M., Vojnovic, B., and Ng, T. (2005). Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions. Biophys. J. 88, 1224-1237.
36. Pierce, K.L., Premont, R.T., and Lefkowitz, R.J. (2002). Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650.
37. Pitcher, J.A., Inglese, J., Higgins, J.B., Arriza, J.L., Casey, P.J., Kim, C., Benovic, J.L., Kwatra, M.M., Caron, M.G., and Lefkowitz, R.J. (1992). Role of beta gamma subunits of G proteins in targeting the beta-adrenergic receptor kinase to membrane-bound receptors. Science 257, 1264-1267.
38. Pitcher, J.A., Touhara, K., Payne, E.S., and Lefkowitz, R.J. (1995). Pleckstrin homology domain-mediated membrane association and activation of the beta-adrenergic receptor kinase requires coordinate interaction with G beta gamma subunits and lipid. J. Biol. Chem. 270, 11707-11710.
39. Pitcher, J.A., Freedman, N.J., and Lefkowitz, R.J. (1998). G protein-coupled receptor kinases. Annu. Rev. Biochem. 67, 653-692.
40. Raveh, A., Riven, I., and Reuveny, E. (2008). The use of FRET microscopy to elucidate steady state channel conformational rearrangements and G protein interaction with the GIRK channels. Methods Mol. Biol. 491, 199-212.
41. Reiter, E., and Lefkowitz, R.J. (2006). GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab. 17, 159-165.
42. Reuveny, E., Slesinger, P.A., Inglese, J., Morales, J.M., Iniguez-Lluhi, J.A., Lefkowitz, R.J., Bourne, H.R., Jan, Y.N., and Jan, L.Y. (1994). Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature 370, 143-146.
43. Rishal, I., Porozov, Y., Yakubovich, D., Varon, D., and Dascal, N. (2005). Gbetagamma-dependent and Gbetagamma-independent basal activity of G protein-activated K+ channels. J. Biol. Chem. 280, 16685-16694.
44. Riven, I., Kalmanzon, E., Segev, L., and Reuveny, E. (2003). Conformational rearrangements associated with the gating of the G protein-coupled potassium channel revealed by FRET microscopy. Neuron 38, 225-235.
45. Riven, I., Iwanir, S., and Reuveny, E. (2006). GIRK channel activation involves a local rearrangement of a preformed G protein channel complex. Neuron 51, 561-573.
46. Sadja, R., and Reuveny, E. (2009). Activation gating kinetics of GIRK channels are mediated by cytoplasmic residues adjacent to transmembrane domains. Channels (Austin) 3, 205-214.
47. Sadja, R., Smadja, K., Alagem, N., and Reuveny, E. (2001). Coupling Gbetagamma-dependent activation to channel opening via pore elements in inwardly rectifying potassium channels. Neuron 29, 669-680.
48. Sadja, R., Alagem, N., and Reuveny, E. (2002). Graded contribution of the Gbeta gamma binding domains to GIRK channel activation. Proc. Natl. Acad. Sci. USA 99, 10783-10788.
49. Shui, Z., Khan, I.A., Tsuga, H., Haga, T., and Boyett, M.R. (1998). Role of receptor kinase in short-term desensitization of cardiac muscarinic K+ channels expressed in Chinese hamster ovary cells. J. Physiol. 507, 325-334.
50. Sickmann, T., and Alzheimer, C. (2003). Short-term desensitization of G-protein-activated, inwardly rectifying K+ (GIRK) currents in pyramidal neurons of rat neocortex. J. Neurophysiol. 90, 2494-2503.
51. Sickmann, T., Klose, A., Huth, T., and Alzheimer, C. (2008). Unexpected suppression of neuronal G protein-activated, inwardly rectifying K+ current by common phospholipase C inhibitor. Neurosci. Lett. 436, 102-106.
52. Sterne-Marr, R., Tesmer, J.J., Day, P.W., Stracquatanio, R.P., Cilente, J.A., O'Connor, K.E., Pronin, A.N., Benovic, J.L., and Wedegaertner, P.B. (2003). G protein-coupled receptor Kinase 2/G alpha q/11 interaction. A novel surface on a regulator of G protein signaling homology domain for binding G alpha subunits. J. Biol. Chem. 278, 6050-6058.
53. Sui, J.L., Petit-Jacques, J., and Logothetis, D.E. (1998). Activation of the atrial KACh channel by the betagamma subunits of G proteins or intracellular Na+ ions depends on the presence of phosphatidylinositol phosphates. Proc. Natl. Acad. Sci. USA 95, 1307-1312.
54. Tesmer, V.M., Kawano, T., Shankaranarayanan, A., Kozasa, T., and Tesmer, J.J. (2005). Snapshot of activated G proteins at the membrane: the Galphaq-GRK2-Gbetagamma complex. Science 310, 1686-1690.
55. Torres, G.E., Gainetdinov, R.R., and Caron, M.G. (2003). Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 4, 13-25.
56. Touhara, K., Koch, W.J., Hawes, B.E., and Lefkowitz, R.J. (1995). Mutational analysis of the pleckstrin homology domain of the beta-adrenergic receptor kinase. Differential effects on G beta gamma and phosphatidylinositol 4, 5-bisphosphate binding. J. Biol. Chem. 270, 17000-17005.
57. Tsao, P., and von Zastrow, M. (2000). Downregulation of G protein-coupled receptors. Curr. Opin. Neurobiol. 10, 365-369.
58. Violin, J.D., Ren, X.R., and Lefkowitz, R.J. (2006). G-protein-coupled receptor kinase specificity for beta-arrestin recruitment to the beta2-adrenergic receptor revealed by fluorescence resonance energy transfer. J. Biol. Chem. 281, 20577-20588.
59. Wallrabe, H., and Periasamy, A. (2005). Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16, 19-27.
60. Wu, G., Benovic, J.L., Hildebrandt, J.D., and Lanier, S.M. (1998). Receptor docking sites for G-protein betagamma subunits. Implications for signal regulation. J. Biol. Chem. 273, 7197-7200. (Pubitemid 28152734)
61. Yasuda, R., Harvey, C.D., Zhong, H., Sobczyk, A., van Aelst, L., and Svoboda, K. (2006). Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat. Neurosci. 9, 283-291.
62. Zacharias, D.A., Violin, J.D., Newton, A.C., and Tsien, R.Y. (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916.
63. Zhang, H., He, C., Yan, X., Mirshahi, T., and Logothetis, D.E. (1999). Activation of inwardly rectifying K+ channels by distinct PtdIns(4, 5)P2 interactions. Nat. Cell Biol. 1, 183-188.