A computational model predicts that Gbg acts at a cleft between channel subunits to activate GIRK1 channels

Science Signaling

Volumn 6, Issue 288, 2013, Pages

  Mahajan, Rahul ^a   Ha, Junghoon ^a   Zhang, Miao ^a   Kawano, Takeharu ^a,b   Kozasa, Tohru ^b   Logothetis, Diomedes E ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CYSTEINE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL 1; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CROSS LINKING; DISULFIDE BOND; ELECTROSTATIC IMAGING SYSTEM; FEMALE; MOLECULAR DOCKING; MOLECULAR MODEL; MUTATION; NONHUMAN; OOCYTE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SCORING SYSTEM; STATIC ELECTRICITY; STEREOSPECIFICITY; XENOPUS;

COMPUTATIONAL BIOLOGY; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; ION CHANNEL GATING; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTAGENESIS; PROTEIN BINDING; PROTEIN CONFORMATION; STATIC ELECTRICITY;

EID: 84884130212     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004075     Document Type: Article

References (49)

1. W. Trautwein, J. Dudel, Mechanism of membrane effect of acetylcholine on myocardial fibers. Pflugers Arch. 266, 324-334 (1958).
2. D. E. Logothetis, Y. Kurachi, J. Galper, E. J. Neer, D. E. Clapham, The bg subunits of GTP-Binding proteins activate the muscarinic K+ channel in heart. Nature 325, 321-326 (1987).
3. T. M. Cabrera-Vera, J. Vanhauwe, T. O. Thomas, M. Medkova, A. Preininger, M. R. Mazzoni, H. E. Hamm, Insights into G protein structure, function, and regulation. Endocr. Rev. 24, 765-781 (2003).
4. R. Gaudet, A. Bohm, P. B. Sigler, Crystal structure at 2.4 Å resolution of the complex of transducin bg and its regulator, phosducin. Cell 87, 577-588 (1996).
5. J. J. G. Tesmer, V. M. Tesmer, D. T. Lodowski, H. Steinhagen, J. Huber, Structure of human G protein-Coupled receptor kinase 2 in complex with the kinase inhibitor balanol. J. Med. Chem. 53, 1867-1870 (2010).
6. N. Dascal, W. Schreibmayer, N. F. Lim, W. Wang, C. Chavkin, L. DiMagno, C. Labarca, B. L. Kieffer, C. Gaveriaux-Ruff, D. Trollinger, H. A. Lester, N. Davidson, Atrial G proteinactivated K+ channel: Expression cloning and molecular properties. Proc. Natl. Acad. Sci. U.S.A. 90, 10235-10239 (1993).
7. G. Krapivinsky, E. A. Gordon, K. Wickman, B. Vellimirovi, L. Krapvinsky, D. E. Clapham, The G-Protein-Gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K+-Channel proteins. Nature 374, 135-141 (1995).
8. Y. Kubo, E. Reuveny, P. A. Slesinger, Y. N. Jan, L. Y. Jan, Primary structure and functional expression of a rat G-Protein-Coupled muscarinic potassium channel. Nature 364, 802-806 (1993).
9. F. Lesage, F. Duprat, M. Fink, E. Guillemare, T. Coppola, M. Lazdunski, J. P. Hugnot, Cloning provides evidence for a family of inward rectifier and G-Protein coupled K+ channels in the brain. FEBS Lett. 353, 37-42 (1994).
10. H. Hibino, A. Inanobe, K. Furutani, S. Murakami, I. Findlay, Y. Kurachi, Inwardly rectifying potassium channels: Their structure, function, and physiological roles. Physiol. Rev. 90, 291-366 (2010).
11. J. M. Lewohl, W. R. Wilson, R. D. Mayfield, S. J. Brozowski, R. A. Morrisett, R. A. Harris, G-Protein-Coupled inwardly rectifying potassium channels are targets of alcohol action. Nat. Neurosci. 2, 1084-1090 (1999).
12. T. Kobayashi, K. Ikeda, H. Kojima, H. Niki, R. Yano, T. Yoshioka, T. Kumanishi, Ethanol opens G-Protein-Activated inwardly rectifying K+ channels. Nat. Neurosci. 2, 1091-1097 (1999).
13. J. L. Sui, K. W. Chan, D. E. Logothetis, Na+ activation of the muscarinic K+ channel by a G-Protein-Independent mechanism. J. Gen. Physiol. 108, 381-391 (1996).
14. J. L. Sui, J. Petit-Jacques, D. E. Logothetis, Activation of the atrial KACh channel by the bg subunits of G proteins or intracellular Na+ ions depends on the presence of phosphatidylinositol phosphates. Proc. Natl. Acad. Sci. U.S.A. 95, 1307-1312 (1998).
15. M. Vivaudou, K. W. Chan, J. L. Sui, L. Y. Jan, E. Reuveny, D. E. Logothetis, Probing the G-Protein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J. Biol. Chem. 272, 31553-31560 (1997).
16. M. A. Wall, D. E. Coleman, E. Lee, J. A. Iñiguez-Lluhi, B. A. Posner, A. G. Gilman, S. R. Sprang, The structure of the G protein heterotrimer Gia1b1g2. Cell 83, 1047-1058 (1995).
17. D. G. Lambright, J. Sondek, A. Bohm, N. P. Skiba, H. E. Hamm, P. B. Sigler, The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379, 311-319 (1996).
18. J. Sondek, A. Bohm, D. G. Lambright, H. E. Hamm, P. B. Sigler, Crystal structure of a GA protein bg dimer at 2.1 Å resolution. Nature 379, 369-374 (1996).
19. M. Nishida, M. Cadene, B. T. Chait, R. MacKinnon, Crystal structure of a Kir3.1-Prokaryotic Kir channel chimera. EMBO J. 26, 4005-4015 (2007).
20. S. Pegan, C. Arrabit, W. Zhou, W. Kwiatkowski, A. Collins, P. A. Slesinger, S. Choe, Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification. Nat. Neurosci. 8, 279-287 (2005).
21. A. Inanobe, T. Matsuura, A. Nakagawa, Y. Kurachi, Structural diversity in the cytoplasmic region of G Protein-Gated inward rectifier K+ channels. Channels 1, 39-45 (2007).
22. M. R. Whorton, R. MacKinnon, Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147, 199-208 (2011).
23. M. R. Whorton, R. MacKinnon, X-Ray structure of the mammalian GIRK2-Bg G-Protein complex. Nature 498, 190-197 (2013).
24. E. Leal-Pinto, Y. Gómez-Llorente, S. Sundaram, Q.-Y. Tang, T. Ivanova-Nikolova, R. Mahajan, L. Baki, Z. Zhang, J. Chavez, I. Ubarretxena-Belandia, D. E. Logothetis, Gating of a G protein-Sensitive mammalian Kir3.1 prokaryotic Kir channel chimera in planar lipid bilayers. J. Biol. Chem. 285, 39790-39800 (2010).
25. M. Finley, C. Arrabit, C. Fowler, K. F. Suen, P. A. Slesinger, bL-BM loop in the C-Terminal domain of G protein-Activated inwardly rectifying K+ channels is important for Gbg subunit activation. J. Physiol. 555, 643-657 (2004).
26. C. He, H. Zhang, T. Mirshahi, D. E. Logothetis, Identification of a potassium channel site that interacts with G protein bg subunits to mediate agonist-Induced signaling. J. Biol. Chem. 274, 12517-12524 (1999).
27. T. Ivanina, I. Rishal, D. Varon, C. Mullner, B. Frohnwieser-Steinecke, W. Schreibmayer, C. W. Dessauer, N. Dascal, Mapping the Gbg-Binding sites in GIRK1 and GIRK2 subunits of the G protein-Activated K+ channel. J. Biol. Chem. 278, 29174-29183 (2003).
28. V. M. Tesmer, T. Kawano, A. Shankaranarayanan, T. Kozasa, J. J. G. Tesmer, Snapshot of activated G proteins at the membrane: The Gaq-GRK2-Gbg complex. Science 310, 1686-1690 (2005).
29. S. Vajda, D. Kozakov, Convergence and combination of methods in protein-Protein docking. Curr. Opin. Struct. Biol. 19, 164-170 (2009).
30. B. Pierce, Z. Weng, A combination of rescoring and refinement significantly improves protein docking performance. Proteins 72, 270-279 (2008).
31. D. Kozakov, O. Schueler-Furman, S. Vajda, Discrimination of near-Native structures in protein-Protein docking by testing the stability of local minima. Proteins 72, 993-1004 (2008).
32. S. R. Comeau, D. W. Gatchell, S. Vajda, C. J. Camacho, ClusPro: An automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20, 45-50 (2004).
33. J. Mintseris, B. Pierce, K. Wiehe, R. Anderson, R. Chen, Z. Weng, Integrating statistical pair potentials into protein complex prediction. Proteins 69, 511-520 (2007).
34. J. J. Gray, S. Moughon, C. Wang, O. Schueler-Furman, B. Kuhlman, C. A. Rohl, D. Baker, Protein-Protein docking with simultaneous optimization of rigid-Body displacement and side-Chain conformations. J. Mol. Biol. 331, 281-299 (2003).
35. M. Yokogawa, M. Osawa, K. Takeuchi, Y. Mase, I. Shimada, NMR analyses of the Gbg binding and conformational rearrangements of the cytoplasmic pore of G proteinactivated inwardly rectifying potassium channel 1 (GIRK1). J. Biol. Chem. 286, 2215-2223 (2011).
36. X.-Y. Meng, H.-X. Zhang, D. E. Logothetis, M. Cui, The molecular mechanism by which PIP2 opens the intracellular G-loop gate of a Kir3.1 channel. Biophys. J. 102, 2049-2059 (2012).
37. C. E. Ford, N. P. Skiba, H. Bae, Y. Daaka, E. Reuveny, L. R. Shekter, R. Rosal, G. Weng, C. Yang, R. Iyengar, R. J. Miller, L. Y. Jan, R. J. Lefkowitz, H. E. Hamm, Molecular basis for interactions of G protein bg subunits with effectors. Science 280, 1271-1274 (1998).
38. M. Nishida, R. MacKinnon, Structural basis of inward rectification: Cytoplasmic pore of the G protein-Gated inward rectifier GIRK1 at 1.8 Å resolution. Cell 111, 957-965 (2002).
39. T. Kozasa, Purification of G protein subunits from Sf9 insect cells using hexahistidinetagged a and bg subunits. Methods Mol. Biol. 237, 21-38 (2004).
40. P. Aryal, H. Dvir, S. Choe, P. A. Slesinger, A discrete alcohol pocket involved in GIRK channel activation. Nat. Neurosci. 12, 988-995 (2009).
41. C. J. Camacho, Z. Weng, S. Vajda, C. DeLisi, Free energy landscapes of encounter complexes in protein-Protein association. Biophys. J. 76, 1166-1178 (1999).
42. C. J. Camacho, S. Vajda, Protein docking along smooth association pathways. Proc. Natl. Acad. Sci. U.S.A. 98, 10636-10641 (2001).
43. Q. Zhao, T. Kawano, H. Nakata, Y. Nakajima, S. Nakajima, T. Kozasa, Interaction of G protein b subunit with inward rectifier K+ channel Kir3. Mol. Pharmacol. 64, 1085-1091 (2003).
44. T. Mirshahi, L. Robillard, H. Zhang, T. E. Hébert, D. E. Logothetis, Gb residues that do not interact with Ga underlie agonist-Independent activity of K+ channels. J. Biol. Chem. 277, 7348-7355 (2002).
45. A. Sali, T. L. Blundell, Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993).
46. D. Kozakov, K. H. Clodfelter, S. Vajda, C. J. Camacho, Optimal clustering for detecting near-Native conformations in protein docking. Biophys. J. 89, 867-875 (2005).
47. J.P. Buonaccorsi, Fieller's theorem. Encyclopedia Biostat. 10.1002/0470011815.b2a15045 (2005).
48. M. J. Knol, W. R. Pestman, D. E. Grobbee, The misuse of overlap of confidence intervals to assess effect modification. Eur. J. Epidemiol. 26, 253-254 (2011).
49. R. Wolfenden, L. Andersson, P. M. Cullis, C. C. B. Southgate, Affinities of amino acid side chains for solvent water. Biochemistry 20, 849-855 (1981).