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Science 22 May 1998:
Vol. 280. no. 5367, pp. 1271 - 1274
DOI: 10.1126/science.280.5367.1271
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Reports

Molecular Basis for Interactions of G Protein beta gamma Subunits with Effectors

Carolyn E. Ford, * Nikolai P. Skiba, * Hyunsu Bae, Yehia Daaka, Eitan Reuveny, Lee R. Shekter, Ramon Rosal, Gezhi Weng, Chii-Shen Yang, Ravi Iyengar, Richard J. Miller, Lily Y. Jan, Robert J. Lefkowitz, Heidi E. Hamm dagger

Both the alpha  and beta gamma subunits of heterotrimeric guanine nucleotide-binding proteins (G proteins) communicate signals from receptors to effectors. Gbeta gamma subunits can regulate a diverse array of effectors, including ion channels and enzymes. Galpha subunits bound to guanine diphosphate (Galpha -GDP) inhibit signal transduction through Gbeta gamma subunits, suggesting a common interface on Gbeta gamma subunits for Galpha binding and effector interaction. The molecular basis for interaction of Gbeta gamma with effectors was characterized by mutational analysis of Gbeta residues that make contact with Galpha -GDP. Analysis of the ability of these mutants to regulate the activity of calcium and potassium channels, adenylyl cyclase 2, phospholipase C-beta 2, and beta -adrenergic receptor kinase revealed the Gbeta residues required for activation of each effector and provides evidence for partially overlapping domains on Gbeta for regulation of these effectors. This organization of interaction regions on Gbeta for different effectors and Galpha explains why subunit dissociation is crucial for signal transmission through Gbeta gamma subunits.

C. E. Ford, N. P. Skiba, H. Bae, C.-S. Yang, H. E. Hamm, Institute for Neuroscience and Department of Molecular Pharmacology and Biological Chemistry, Northwestern University, Chicago, IL 60611, USA.
Y. Daaka and R. J. Lefkowitz, Howard Hughes Medical Institute and Department of Medicine, Duke University Medical Center, Durham, NC 27710, USA.
E. Reuveny, Department of Membrane Research and Biophysics, Weizmann Institute of Science, Rehovot 76100, Israel.
L. R. Shekter and R. J. Miller, Department of Pharmacological and Physiological Sciences, University of Chicago, Chicago, IL 60637, USA.
R. Rosal, G. Weng, R. Iyengar, Department of Pharmacology, Mount Sinai School of Medicine, New York, NY 10029, USA.
L. Y. Jan, Howard Hughes Medical Institute and Department of Physiology and Biochemistry, University of California at San Francisco, San Francisco, CA 94143, USA.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: h-hamm{at}nwu.edu

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J. Biol. Chem. 275, 38961-38964
   Abstract »    Full Text »    PDF »
Selective Coupling of G Protein beta gamma Complexes to Inhibition of Ca2+ Channels.
M. Diverse-Pierluissi, W. E. McIntire, C.-S. Myung, M. A. Lindorfer, J. C. Garrison, M. F. Goy, and K. Dunlap (2000)
J. Biol. Chem. 275, 28380-28385
   Abstract »    Full Text »    PDF »
Functional Roles of the Two Domains of Phosducin and Phosducin-like Protein.
J. R. Savage, J. N. McLaughlin, N. P. Skiba, H. E. Hamm, and B. M. Willardson (2000)
J. Biol. Chem. 275, 30399-30407
   Abstract »    Full Text »    PDF »
Characterization of a Phospholipase C beta 2-Binding Site Near the Amino-terminal Coiled-coil of G Protein beta gamma Subunits.
D. M. Yoshikawa, K. Bresciano, M. Hatwar, and A. V. Smrcka (2001)
J. Biol. Chem. 276, 11246-11251
   Abstract »    Full Text »    PDF »
Dual Regulation of Akt/Protein Kinase B by Heterotrimeric G Protein Subunits.
R. K. Bommakanti, S. Vinayak, and W. F. Simonds (2000)
J. Biol. Chem. 275, 38870-38876
   Abstract »    Full Text »    PDF »
G Protein beta Subunit Types Differentially Interact with a Muscarinic Receptor but Not Adenylyl Cyclase Type II or Phospholipase C-beta 2/3.
Y. Hou, V. Chang, A. B. Capper, R. Taussig, and N. Gautam (2001)
J. Biol. Chem. 276, 19982-19988
   Abstract »    Full Text »    PDF »
Insulin and Insulin-like Growth Factor I Receptors Utilize Different G Protein Signaling Components.
S. Dalle, W. Ricketts, T. Imamura, P. Vollenweider, and J. M. Olefsky (2001)
J. Biol. Chem. 276, 15688-15695
   Abstract »    Full Text »    PDF »
Interaction Sites of the G Protein beta Subunit with Brain G Protein-coupled Inward Rectifier K+ Channel.
A. M. Albsoul-Younes, P. M. Sternweis, P. Zhao, H. Nakata, S. Nakajima, Y. Nakajima, and T. Kozasa (2001)
J. Biol. Chem. 276, 12712-12717
   Abstract »    Full Text »    PDF »
The G Protein beta Subunit Is a Determinant in the Coupling of Gs to the beta 1-Adrenergic and A2a Adenosine Receptors.
W. E. McIntire, G. MacCleery, and J. C. Garrison (2001)
J. Biol. Chem. 276, 15801-15809
   Abstract »    Full Text »    PDF »
Parallel Regulation of Mitogen-activated Protein Kinase Kinase 3 (MKK3) and MKK6 in Gq-signaling Cascade.
J. Yamauchi, G. Tsujimoto, Y. Kaziro, and H. Itoh (2001)
J. Biol. Chem. 276, 23362-23372
   Abstract »    Full Text »    PDF »
Regulator of G-protein Signaling 3 (RGS3) Inhibits Gbeta 1gamma 2-induced Inositol Phosphate Production, Mitogen-activated Protein Kinase Activation, and Akt Activation.
C.-S. Shi, S. B. Lee, S. Sinnarajah, C. W. Dessauer, S. G. Rhee, and J. H. Kehrl (2001)
J. Biol. Chem. 276, 24293-24300
   Abstract »    Full Text »    PDF »
Modulation of the G Protein Regulator Phosducin by Ca2+/Calmodulin-dependent Protein Kinase II Phosphorylation and 14-3-3 Protein Binding.
C. D. Thulin, J. R. Savage, J. N. McLaughlin, S. M. Truscott, W. M. Old, N. G. Ahn, K. A. Resing, H. E. Hamm, M. W. Bitensky, and B. M. Willardson (2001)
J. Biol. Chem. 276, 23805-23815
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The Role of Electrostatic Interactions in the Regulation of the Membrane Association of G Protein beta gamma Heterodimers.
D. Murray, S. McLaughlin, and B. Honig (2001)
J. Biol. Chem. 276, 45153-45159
   Abstract »    Full Text »    PDF »
RGS12 and RGS14 GoLoco Motifs Are Galpha i Interaction Sites with Guanine Nucleotide Dissociation Inhibitor Activity.
R. J. Kimple, L. De Vries, H. Tronchere, C. I. Behe, R. A. Morris, M. G. Farquhar, and D. P. Siderovski (2001)
J. Biol. Chem. 276, 29275-29281
   Abstract »    Full Text »    PDF »
Modular Design of Gbeta as the Basis for Reversible Specificity in Effector Stimulation.
E. Buck and R. Iyengar (2001)
J. Biol. Chem. 276, 36014-36019
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Binding of Galpha o N Terminus Is Responsible for the Voltage-resistant Inhibition of alpha 1A (P/Q-type, Cav2.1) Ca2+ Channels.
M. Kinoshita, T. Nukada, T. Asano, Y. Mori, A. Akaike, M. Satoh, and S. Kaneko (2001)
J. Biol. Chem. 276, 28731-28738
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Mutant G protein alpha subunit activated by Gbeta gamma : A model for receptor activation?.
P. Rondard, T. Iiri, S. Srinivasan, E. Meng, T. Fujita, and H. R. Bourne (2001)
PNAS 98, 6150-6155
   Abstract »    Full Text »    PDF »


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