X-ray structure of the mammalian GIRK2-βγ G-protein complex

Nature

Volumn 498, Issue 7453, 2013, Pages 190-197

  Whorton, Matthew R ^a   MacKinnon, Roderick ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR3.2; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SODIUM ION; UNCLASSIFIED DRUG;

LIGAND; LIPID; NEUROLOGY; PROTEIN; SIGNALING; X-RAY SPECTROSCOPY;

ARTICLE; CHANNEL GATING; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SODIUM CELL LEVEL; STATIC ELECTRICITY; X RAY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; ION CHANNEL GATING; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; SODIUM; STATIC ELECTRICITY;

MAMMALIA;

EID: 84878996278     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12241     Document Type: Article

References (47)

1. Loewi, O.Über humorale übertragbarkeit der herznervenwirkung. Pflugers Arch. 189, 239-242 (1921)
2. Loewi, O. The chemical transmission of nerve action (1936 Nobel lecture) in Nobel Lectures in Physiology or Medicine 1922-1941 (World Scientific Publishing, 1999)
3. Loewi, O. & Navratil, E.Über humorale übertragbarkeit der herznervenwirkung. Pflugers Arch. 214, 678-688 (1926)
4. Gilman, A. G. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649 (1987)
5. Logothetis, D. E., Kurachi, Y., Galper, J., Neer, E. J. & Clapham, D. E. The bc subunits of GTP-binding proteins activate the muscarinic K1 channel in heart. Nature 325, 321-326 (1987) (Pubitemid 17053169)
6. Reuveny, E. et al. Activation of the cloned muscarinic potassium channel by G protein bc subunits. Nature 370, 143-146 (1994) (Pubitemid 24229126)
7. Wickman, K. D. et al. Recombinant G-protein bc-subunits activate the muscarinicgated atrial potassium channel. Nature 368, 255-257 (1994)
8. Pfaffinger, P. J.,Martin, J. M.,Hunter, D. D., Nathanson, N. M.&Hille, B.GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature 317, 536-538 (1985)
9. Breitwieser, G. E. & Szabo, G. Uncoupling of cardiac muscarinic and b-adrenergic receptors from ion channels by a guanine nucleotide analogue. Nature 317, 538-540 (1985) (Pubitemid 16224161)
10. Soejima, M. & Noma, A. Mode of regulation of the ACh-sensitive K-channel by the muscarinic receptor in rabbit atrial cells. Pflugers Arch. 400, 424-431 (1984) (Pubitemid 14115046)
11. Trautwein, W. & Dudel, J. Zum mechanismus der membranwirkung des acetylcholin an der herzmuskelfaser. Pflugers Arch. 266, 324-334 (1958)
12. Lüscher, C.&Slesinger, P.A.Emerging roles forGprotein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nature Rev. Neurosci 11, 301-315 (2010)
13. Ford, C. E. et al. Molecular basis for interactions of G protein bc subunits with effectors. Science 280, 1271-1274 (1998) (Pubitemid 28269623)
14. Albsoul-Younes, A. M. et al. Interaction sites of the G protein b subunit with brain G protein-coupled inward rectifier K1 channel. J. Biol. Chem. 276, 12712-12717 (2001)
15. Mirshahi, T., Robillard, L.,Zhang, H.,Hebert, T. E.&Logothetis, D. E.Gb residues that do not interact with Ga underlie agonist-independent activity of K1 channels. J. Biol. Chem. 277, 7348-7355 (2002) (Pubitemid 34953130)
16. Zhao, Q. et al. Interaction of G protein b subunit with inward rectifier K1 channel Kir3. Mol. Pharmacol. 64, 1085-1091 (2003) (Pubitemid 37310741)
17. Zhao, Q. et al. Dominant negative effects of a Gb mutant on G-protein coupled inward rectifier K1 channel. FEBS Lett. 580, 3879-3882 (2006) (Pubitemid 43946877)
18. He, C., Zhang, H., Mirshahi, T. & Logothetis, D. E. Identification of a potassium channel site that interacts with G protein bc subunits to mediate agonist-induced signaling. J. Biol. Chem. 274, 12517-12524 (1999)
19. Finley, M., Arrabit, C., Fowler, C., Suen, K. F. & Slesinger, P. A. bL- bM loop in the C-terminal domain of G protein-activated inwardly rectifying K1 channels is important for Gbc subunit activation. J. Physiol. (Lond.) 555, 643-657 (2004) (Pubitemid 38404587)
20. Yokogawa, M., Osawa, M., Takeuchi, K., Mase, Y. & Shimada, I.NMR analyses of the Gbc binding and conformational rearrangements of the cytoplasmic pore of G protein-activated inwardly rectifying potassium channel 1 (GIRK1). J. Biol. Chem 286, 2215-2223 (2011)
21. Slesinger, P. A., Reuveny, E., Jan, Y. N. & Jan, L. Y. Identification of structural elements involved inGprotein gating of the GIRK1 potassiumchannel. Neuron 15, 1145-1156 (1995)
22. Huang, C. L., Slesinger, P. A., Casey, P. J., Jan, Y. N. & Jan, L. Y. Evidence that direct binding of Gbc to the GIRK1 G protein-gated inwardly rectifying K1 channel is important for channel activation. Neuron 15, 1133-1143 (1995)
23. Kofuji, P., Davidson, N. & Lester, H. A. Evidence that neuronal G-protein-gated inwardly rectifying K1 channels are activated by Gbc subunits and function as heteromultimers. Proc. Natl Acad. Sci. USA 92, 6542-6546 (1995)
24. Kubo, Y., Reuveny, E., Slesinger, P. A., Jan, Y. N. & Jan, L. Y. Primary structure and functional expression of a rat G-protein-coupled muscarinic potassium channel. Nature 364, 802-806 (1993) (Pubitemid 23261760)
25. Jin, W. & Lu, Z. Synthesis of a stable form of tertiapin: a high-affinity inhibitor for inward-rectifier K1 channels. Biochemistry 38, 14286-14293 (1999)
26. Ho, I. H. & Murrell-Lagnado, R. D. Molecular mechanism for sodium-dependent activation ofGprotein-gatedK1 channels. J. Physiol. (Lond.) 520, 645-651 (1999) (Pubitemid 29533024)
27. Ho, I. H. & Murrell-Lagnado, R. D. Molecular determinants for sodium-dependent activation of G protein-gated K1 channels. J. Biol. Chem. 274, 8639-8648 (1999) (Pubitemid 29164658)
28. Sui, J. L., Petit-Jacques, J.& Logothetis, D. E. Activation of the atrial KACh channel by the bc subunits of G proteins or intracellular Na1 ions depends on the presence of phosphatidylinositol phosphates. Proc. Natl Acad. Sci. USA 95, 1307-1312 (1998)
29. Sui, J. L.,Chan, K.W.&Logothetis, D. E.Na1activationof themuscarinicK1channel by a G-protein-independent mechanism. J. Gen. Physiol. 108, 381-391 (1996)
30. Wall, M. A. et al. The structure of the G protein heterotrimer Gia1b1c 2. Cell 83, 1047-1058 (1995)
31. Whorton, M. R. & MacKinnon, R. Crystal structure of the mammalian GIRK2 K1 channel and gating regulation byGproteins, PIP2, and sodium. Cell 147, 199-208 (2011)
32. Huang, C. L., Feng, S. & Hilgemann, D. W. Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbc. Nature 391, 803-806 (1998) (Pubitemid 28099680)
33. Mumby, S. M., Casey, P. J., Gilman, A. G., Gutowski, S. & Sternweis, P. C. G protein gamma subunits contain a 20-carbon isoprenoid. Proc. Natl Acad. Sci. USA 87, 5873-5877 (1990)
34. Yamane, H. K. et al. Brain G protein c subunits contain an all-transgeranylgeranylcysteine methyl ester at their carboxyl termini. Proc. Natl Acad. Sci. USA 87, 5868-5872 (1990)
35. Rasmussen, S. G. et al. Crystal structure of the b2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011)
36. Hibino, H. et al. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev. 90, 291-366 (2010)
37. Sheinerman, F. B., Norel, R. & Honig, B. Electrostatic aspects of protein-protein interactions. Curr. Opin. Struct. Biol. 10, 153-159 (2000) (Pubitemid 30198940)
38. McLaughlin, S. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18, 113-136 (1989)
39. Cheever, M. L. et al. Crystal structure of the multifunctional Gb5-RGS9 complex. Nature Struct. Biol. 15, 155-162 (2008) (Pubitemid 351227317)
40. Zachariou, V. et al. Essential role for RGS9 in opiate action. Proc. Natl Acad. Sci. USA 100, 13656-13661 (2003) (Pubitemid 37444795)
41. Rahman, Z. et al.RGS9modulates dopamine signaling in the basal ganglia.Neuron 38, 941-952 (2003) (Pubitemid 36782384)
42. Kovoor, A. et al. D2 dopamine receptors colocalize regulator of G-protein signaling 9-2 (RGS9-2) via the RGS9 DEP domain, and RGS9 knock-out mice developdyskinesias associated with dopamine pathways. J. Neurosci 25, 2157-2165 (2005) (Pubitemid 40289421)
43. Jiang, Y. et al. X-ray structure of a voltage-dependent K1 channel. Nature 423, 33-41 (2003)
44. Jiang, Y. et al. The open pore conformation of potassium channels. Nature 417, 523-526 (2002) (Pubitemid 34595913)
45. Long, S. B., Tao, X., Campbell, E. B. & MacKinnon, R. Atomic structure of a voltagedependent K1 channel in a lipid membrane-like environment. Nature 450, 376-382 (2007) (Pubitemid 350126743)
46. Long, S. B., Campbell, E. B. & Mackinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K1 channel. Science 309, 897-903 (2005). (Pubitemid 41099919)
47. Hansen, S. B., Tao, X. & MacKinnon, R. Structural basis of PIP2 activation of the classical inward rectifier K1 channel Kir2.2. Nature 477, 495-498 (2011).