GIRK Channel Activation Involves a Local Rearrangement of a Preformed G Protein Channel Complex

Neuron

Volumn 51, Issue 5, 2006, Pages 561-573

  Riven, Inbal ^a   Iwanir, Shachar ^a   Reuveny, Eitan ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

CELLBIO; MOLNEURO; SIGNALING

Indexed keywords

G PROTEIN COUPLED POTASSIUM CHANNEL; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; PERTUSSIS TOXIN; POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL EXCITABILITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN CONFORMATION;

CELL LINE; FLUORESCENCE RESONANCE ENERGY TRANSFER; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GTP-BINDING PROTEINS; HUMANS; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, QUATERNARY; SIGNAL TRANSDUCTION;

EID: 33748062987     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.08.017     Document Type: Article

References (68)

1. Axelrod D. Total internal reflection fluorescence microscopy. Methods Cell Biol. 30 (1989) 245-270
2. Bauer P.H., Bluml K., Schroder S., Hegler J., Dees C., and Lohse M.J. Interactions of phosducin with the subunits of G-proteins. Binding to the alpha as well as the betagamma subunits. J. Biol. Chem. 273 (1998) 9465-9471
3. Bauer P.H., Muller S., Puzicha M., Pippig S., Obermaier B., Helmreich E.J., and Lohse M.J. Phosducin is a protein kinase A-regulated G-protein regulator. Nature 358 (1992) 73-76
4. Bean B.P. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340 (1989) 153-156
5. Benians A., Leaney J.L., Milligan G., and Tinker A. The dynamics of formation and action of the ternary complex revealed in living cells using a G-protein-gated K+ channel as a biosensor. J. Biol. Chem. 278 (2003) 10851-10858
6. Benians A., Nobles M., Hosny S., and Tinker A. Regulators of G-protein signaling form a quaternary complex with the agonist, receptor, and G-protein. A novel explanation for the acceleration of signaling activation kinetics. J. Biol. Chem. 280 (2005) 13383-13394
7. Berman D.M., Kozasa T., and Gilman A.G. The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis. J. Biol. Chem. 271 (1996) 27209-27212
8. i subfumily of G protein α subfamily. Cell 86 (1996) 445-452
9. Bunemann M., Frank M., and Lohse M.J. Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. USA 100 (2003) 16077-16082
10. Clancy S.M., Fowler C.E., Finley M., Suen K.F., Arrabit C., Berton F., Kosaza T., Casey P.J., and Slesinger P.A. 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 (2005) 375-389
11. Clapham D.E., and Neer E.J. G protein beta gamma subunits. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 167-203
12. Conklin B.R., Farfel Z., Lustig K.D., Julius D., and Bourne H.R. Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha. Nature 363 (1993) 274-276
13. Dale R.E., Eisinger J., and Blumberg W.E. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys. J. 26 (1979) 161-193
14. Dowal L., Elliott J., Popov S., Wilkie T.M., and Scarlata S. Determination of the contact energies between a regulator of G protein signaling and G protein subunits and phospholipase C beta 1. Biochemistry 40 (2001) 414-421
15. Finley M., Arrabit C., Fowler C., Suen K.F., and Slesinger P.A. betaL-betaM loop in the C-terminal domain of G protein-activated inwardly rectifying K(+) channels is important for G(betagamma) subunit activation. J. Physiol. 555 (2004) 643-657
16. Ford C.E., Skiba N.P., Bae H., Daaka Y., Reuveny E., Shekter L.R., Rosal R., Weng G., Yang C.S., Iyengar R., et al. Molecular basis for interactions of G protein betagamma subunits with effectors. Science 280 (1998) 1271-1274
17. Fu H.W., and Casey P.J. Enzymology and biology of CaaX protein prenylation. Recent Prog. Horm. Res. 54 (1999) 315-342
18. Gaudet R., Bohm A., and Sigler P.B. Crystal structure at 2.4 angstroms resolution of the complex of transducin betagamma and its regulator, phosducin. Cell 87 (1996) 577-588
19. Gaudet R., Savage J.R., McLaughlin J.N., Willardson B.M., and Sigler P.B. A molecular mechanism for the phosphorylation-dependent regulation of heterotrimeric G proteins by phosducin. Mol. Cell 3 (1999) 649-660
20. Gibson S.K., and Gilman A.G. Gialpha and Gbeta subunits both define selectivity of G protein activation by alpha2-adrenergic receptors. Proc. Natl. Acad. Sci. USA 103 (2006) 212-217
21. Gilman A.G. G proteins: Transducers of receptor-generated signals. Annu. Rev. Biochem. 56 (1987) 615-649
22. Hamm H.E. The many faces of G protein signaling. J. Biol. Chem. 273 (1998) 669-672
23. Hein P., Frank M., Hoffmann C., Lohse M.J., and Bunemann M. Dynamics of receptor/G protein coupling in living cells. EMBO J. 24 (2005) 4106-4114
24. Hepler J.R. Emerging roles for RGS proteins in cell signalling. Trends Pharmacol. Sci. 20 (1999) 376-382
25. + channel is important for channel activation. Neuron 15 (1995) 1133-1143
26. Huang C.L., Feng S., and Hilgemann D.W. Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391 (1998) 803-806
27. Huang C.L., Jan Y.N., and Jan L.Y. Binding of the G protein betagamma subunit to multiple regions of G protein-gated inward-rectifying K+ channels. FEBS Lett. 405 (1997) 291-298
28. Inanobe A., Morishige K.I., Takahashi N., Ito H., Yamada M., Takumi T., Nishina H., Takahashi K., Kanaho Y., Katada T., et al. G beta gamma directly binds to the carboxyl terminus of the G protein-gated muscarinic K+ channel, GIRK1. Biochem. Biophys. Res. Commun. 212 (1995) 1022-1028
29. Ivanina T., Rishal I., Varon D., Mullner C., Frohnwieser-Steinecker B., Schreibmayer W., Dessauer C.W., and Dascal N. Mapping the Gbg-binding sites in GIRK1 and GIRK2 subunits of the G protein-activated K+ channel. J. Biol. Chem. 278 (2003) 29174-29183
30. Ivanina T., Varon D., Peleg S., Rishal I., Porozov Y., Dessauer C.W., Keren-Raifman T., and Dascal N. Galphai1 and Galphai3 differentially interact with, and regulate, the G protein-activated K+ channel. J. Biol. Chem. 279 (2004) 17260-17268
31. Janetopoulos C., Jin T., and Devreotes P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 291 (2001) 2408-2411
32. Krapivinsky G., Medina I., Eng L., Krapivinsky L., Yang Y., and Clapham D.E. A novel inward rectifier K+ channel with unique pore properties. Neuron 20 (1998) 995-1005
33. Kunkel M.T., and Peralta E.G. Identification of domains conferring G protein regulation on inward rectifier potassium channels. Cell 83 (1995) 443-449
34. Kuo A., Gulbis J.M., Antcliff J.F., Rahman T., Lowe E.D., Zimmer J., Cuthbertson J., Ashcroft F.M., Ezaki T., and Doyle D.A. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300 (2003) 1922-1926
35. Lambright D.G., Sondek J., Bohm A., Skiba N.P., Hamm H.E., and Sigler P.B. The 2.0 A crystal structure of a heterotrimeric G protein. Nature 379 (1996) 311-319
36. Leaney J.L., and Tinker A. The role of members of the pertussis toxin-sensitive family of G proteins in coupling receptors to the activation of the G protein-gated inwardly rectifying potassium channel. Proc. Natl. Acad. Sci. USA 97 (2000) 5651-5656
37. Leaney J.L., Milligan G., and Tinker A. The G protein alpha subunit has a key role in determining the specificity of coupling to, but not the activation of, G protein-gated inwardly rectifying K(+) channels. J. Biol. Chem. 275 (2000) 921-929
38. Lei Q., Jones M.B., Talley E.M., Schrier A.D., McIntire W.E., Garrison J.C., and Bayliss D.A. Activation and inhibition of G protein-coupled inwardly rectifying potassium (Kir3) channels by G protein beta gamma subunits. Proc. Natl. Acad. Sci. USA 97 (2000) 9771-9776
39. Lei Q., Jones M.B., Talley E.M., Garrison J.C., and Bayliss D.A. Molecular mechanisms mediating inhibition of G protein-coupled inwardly-rectifying K+ channels. Mol. Cells 15 (2003) 1-9
40. Leifert W.R., Bailey K., Cooper T.H., Aloia A.L., Glatz R.V., and McMurchie E.J. Measurement of heterotrimeric G-protein and regulators of G-protein signaling interactions by time-resolved fluorescence resonance energy transfer. Anal. Biochem. 355 (2006) 201-212
41. Liu J., Conklin B.R., Blin N., Yun J., and Wess J. Identification of a receptor/G-protein contact site critical for signaling specificity and G-protein activation. Proc. Natl. Acad. Sci. USA 92 (1995) 11642-11646
42. + channel in heart. Nature 325 (1987) 321-326
43. + channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hyppocampal neurons. Neuron 19 (1997) 687-695
44. Mirshahi T., Mittal V., Zhang H., Linder M.E., and Logothetis D.E. Distinct sites on G protein beta gamma subunits regulate different effector functions. J. Biol. Chem. 277 (2002) 36345-36350
45. Mirshahi T., Robillard L., Zhang H., Hebert T.E., and Logothetis D.E. Gbeta residues that do not interact with Galpha underlie agonist-independent activity of K+ channels. J. Biol. Chem. 277 (2002) 7348-7355
46. Miyawaki A., Griesbeck O., Heim R., and Tsien R.Y. Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. USA 96 (1999) 2135-2140
47. Mullner C., Vorobiov D., Bera A.K., Uezono Y., Yakubovich D., Frohnwieser-Steinecker B., Dascal N., and Schreibmayer W. Heterologous facilitation of G protein-activated K(+) channels by beta- adrenergic stimulation via cAMP-dependent protein kinase. J. Gen. Physiol. 115 (2000) 547-558
48. Nishida M., and MacKinnon R. Structural basis of inward rectification: cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8 A resolution. Cell 111 (2002) 957-965
49. Nobles M., Benians A., and Tinker A. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc. Natl. Acad. Sci. USA 102 (2005) 18706-18711
50. Peleg S., Varon D., Ivanina T., Dessauer C.W., and Dascal N. G(alpha)(i) controls the gating of the G protein-activated K(+) channel, GIRK. Neuron 33 (2002) 87-99
51. Rebois R.V., Robitaille M., Gales C., Dupre D.J., Baragli A., Trieu P., Ethier N., Bouvier M., and Hebert T.E. Heterotrimeric G proteins form stable complexes with adenylyl cyclase and Kir3.1 channels in living cells. J. Cell Sci. 119 (2006) 2807-2818
52. 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. Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature 370 (1994) 143-146
53. Rishal I., Porozov Y., Yakubovich D., Varon D., and Dascal N. Gbetagamma-dependent and Gbetagamma-independent basal activity of G protein-activated K+ channels. J. Biol. Chem. 280 (2005) 16685-16694
54. Riven I., Kalmanzon E., Segev L., and Reuveny E. Conformational rearrangements associated with the gating of the G protein-coupled potassium channel revealed by FRET microscopy. Neuron 38 (2003) 225-235
55. Roy A.A., Lemberg K.E., and Chidiac P. Recruitment of RGS2 and RGS4 to the plasma membrane by G proteins and receptors reflects functional interactions. Mol. Pharmacol. 64 (2003) 587-593
56. Sadja R., Alagem N., and Reuveny E. Gating of GIRK channels: details of an intricate, membrane-delimited signaling complex. Neuron 39 (2003) 9-12
57. Slesinger P.A., Reuveny E., Jan Y.N., and Jan L.Y. Identification of structural elements involved in G protein gating of the GIRK1 potassium channel. Neuron 15 (1995) 1145-1156
58. Sodickson D.L., and Bean B.P. GABA-B receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J. Neurosci. 16 (1996) 6374-6385
59. Sondek J., Bohm A., Lambright D.G., Hamm H.E., and Sigler P.B. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379 (1996) 369-374
60. Stanfield P.R., Nakajima S., and Nakajima Y. Constitutively active and G-protein coupled inward rectifier K+ channels: Kir2.0 and Kir3.0. Rev. Physiol. Biochem. Pharmacol. 145 (2002) 47-179
61. Takida S., and Wedegaertner P.B. Heterotrimer formation, together with isoprenylation, is required for plasma membrane targeting of Gbetagamma. J. Biol. Chem. 278 (2003) 17284-17290
62. Tesmer V.M., Kawano T., Shankaranarayanan A., Kozasa T., and Tesmer J.J. Snapshot of activated G proteins at the membrane: the Galphaq-GRK2-Gbetagamma complex. Science 310 (2005) 1686-1690
63. Van Der Meer B.W., Cocker G., and Chen S.-Y.S. Resonance Energy Transfer: Theory and Data (1994), VCH, New York
64. Wall M.A., Coleman D.E., Lee E., Iniguez-Lluhi J.A., Posner B.A., Gilman A.G., and Sprang S.R. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83 (1995) 1047-1058
65. Wickman K.D., Iniguez-Lluhl J.A., Davenport P.A., Taussig R., Krapivinsky G.B., Linder M.E., Gilman A.G., and Clapham D.E. Recombinant G-protein βγ-subunits activate the muscarinic-gated atrial potassium channel. Nature 368 (1994) 255-257
66. Zhang H., He C., Yan X., Mirshahi T., and Logothetis D.E. Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P2 interactions. Nat. Cell Biol. 1 (1999) 183-188
67. Zhang Q., Pacheco M.A., and Doupnik C.A. Gating properties of GIRK channels activated by Galpha(o)- and Galpha(i)-coupled muscarinic m2 receptors in Xenopus oocytes: the role of receptor precoupling in RGS modulation. J. Physiol. 545 (2002) 355-373
68. Zhao Q., Kawano T., Nakata H., Nakajima Y., Nakajima S., and Kozasa T. Interaction of G protein beta subunit with inward rectifier K(+) channel Kir3. Mol. Pharmacol. 64 (2003) 1085-1091