The complex of G protein regulator RGS9-2 and Gβ5 controls sensitization and signaling kinetics of type 5 adenylyl cyclase in the striatum

Science Signaling

Volumn 5, Issue 239, 2012, Pages

  Xie, Keqiang ^a   Masuho, Ikuo ^a   Brand, Cameron ^b   Dessauer, Carmen W ^b   Martemyanov, Kirill A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE 5; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; OPIATE; RGS2 PROTEIN; RGS9 2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; HUMAN; HUMAN CELL; MOUSE; NERVE CELL PLASTICITY; NEUROCHEMISTRY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; ANIMALS; BLOTTING, WESTERN; CORPUS STRIATUM; CYCLIC AMP; FLUORESCENCE RESONANCE ENERGY TRANSFER; GTP-BINDING PROTEIN BETA SUBUNITS; IMMUNOPRECIPITATION; KINETICS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; OPIOID-RELATED DISORDERS; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT PROTEINS; RGS PROTEINS; SIGNAL TRANSDUCTION;

MUS;

EID: 84865688838     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002922     Document Type: Article

References (61)

1. L. A. Catapano, H. K. Manji, G protein-coupled receptors in major psychiatric disorders. Biochim. Biophys. Acta 1768, 976-993 (2007).
2. R. R. Gainetdinov, R. T. Premont, L. M. Bohn, R. J. Lefkowitz, M. G. Caron, Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107-144 (2004).
3. S. Offermanns, G-proteins as transducers in transmembrane signalling. Prog. Biophys. Mol. Biol. 83, 101-130 (2003).
4. R. Taussig, A. G. Gilman, Mammalian membrane-bound adenylyl cyclases. J. Biol. Chem. 270, 1-4 (1995).
5. S. Pierre, T. Eschenhagen, G. Geisslinger, K. Scholich, Capturing adenylyl cyclases as potential drug targets. Nat. Rev. Drug Discov. 8, 321-335 (2009).
6. S. Hollinger, J. R. Hepler, Cellular regulation of RGS proteins: Modulators and integrators of G protein signaling. Pharmacol. Rev. 54, 527-559 (2002).
7. G. R. Anderson, E. Posokhova, K. A. Martemyanov, The R7 RGS protein family: Multi-subunit regulators of neuronal G protein signaling. Cell Biochem. Biophys. 54, 33-46 (2009).
8. A. M. Graybiel, The basal ganglia. Curr. Biol. 10, R509-R511 (2000).
9. A. C. Kreitzer, R. C. Malenka, Striatal plasticity and basal ganglia circuit function. Neuron 60, 543-554 (2008).
10. K. W. Lee, J. H. Hong, I. Y. Choi, Y. Che, J. K. Lee, S. D. Yang, C. W. Song, H. S. Kang, J. H. Lee, J. S. Noh, H. S. Shin, P. L. Han, Impaired D2 dopamine receptor function in mice lacking type 5 adenylyl cyclase. J. Neurosci. 22, 7931-7940 (2002).
11. M. A. Kheirbek, J. P. Britt, J. A. Beeler, Y. Ishikawa, D. S. McGehee, X. Zhuang, Adenylyl cyclase type 5 contributes to corticostriatal plasticity and striatum-dependent learning. J. Neurosci. 29, 12115-12124 (2009).
12. K. S. Kim,K. W. Lee, I. S. Baek, C. M. Lim,V. Krishnan, J. K. Lee, E. J.Nestler, P. L.Han, Adenylyl cyclase-5 activity in the nucleus accumbens regulates anxiety-related behavior. J. Neurochem. 107, 105-115 (2008).
13. K. S. Kim, K. W. Lee, K. W. Lee, J. Y. Im, J. Y. Yoo, S. W. Kim, J. K. Lee, E. J. Nestler, P. L. Han, Adenylyl cyclase type 5 (AC5) is an essential mediator of morphine action. Proc. Natl. Acad. Sci. U.S.A. 103, 3908-3913 (2006).
14. K. Xie, S. Ge, V. E. Collins, C. L. Haynes, K. J. Renner, R. L. Meisel, R. Lujan, K. A. Martemyanov, Gβ5-RGS complexes are gatekeepers of hyperactivity involved in control of multiple neurotransmitter systems. Psychopharmacology 219, 823 -834 (2012).
15. S. B. Hooks, G. L. Waldo, J. Corbitt, E. T. Bodor, A. M. Krumins, T. K. Harden, RGS6, RGS7, RGS9, and RGS11 stimulate GTPase activity of Gi family G-proteins with differential selectivity and maximal activity. J. Biol. Chem. 278, 10087 -10093 (2003).
16. K. A. Martemyanov, J. A. Hopp, V. Y. Arshavsky, Specificity of G protein-RGS protein recognition is regulated by affinity adapters. Neuron 38, 857-862 (2003).
17. X. Gao, R. Sadana, C. W. Dessauer, T. B. Patel, Conditional stimulation of type V and VI adenylyl cyclases by G protein bg subunits. J. Biol. Chem. 282, 294-302 (2007).
18. J. Celver, M. Sharma, A. Kovoor, RGS9-2 mediates specific inhibition of agonist-induced internalization of D2-dopamine receptors. J. Neurochem. 114, 739-749 (2010).
19. V. J. Watts, K. A. Neve, Sensitization of adenylate cyclase by Gαi/o-coupled receptors. Pharmacol. Ther. 106, 405-421 (2005).
20. P. Fan, Z. Jiang, I. Diamond, L. Yao, Up-regulation of AGS3 during morphine withdrawal promotes cAMP superactivation via adenylyl cyclase 5 and 7 in rat nucleus accumbens/striatal neurons. Mol. Pharmacol. 76, 526-533 (2009).
21. R. Z. Terwilliger, D. Beitner-Johnson, K. A. Sevarino, S. M. Crain, E. J. Nestler, A general role for adaptations in G-proteins and the cyclic AMP system in mediating the chronic actions of morphine and cocaine on neuronal function. Brain Res. 548, 100-110 (1991).
22. E. H. Chartoff, S. D. Mague, M. F. Barhight, A. M. Smith, W. A. Carlezon Jr., Behavioral and molecular effects of dopamine D1 receptor stimulation during naloxone-precipitated morphine withdrawal. J. Neurosci. 26, 6450-6457 (2006).
23. B. L. Kieffer, C. Gavériaux-Ruff, Exploring the opioid system by gene knockout. Prog. Neurobiol. 66, 285-306 (2002).
24. P. Y. Law, Y. H. Wong, H. H. Loh, Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40, 389-430 (2000).
25. K. Psifogeorgou, D. Terzi, M. M. Papachatzaki, A. Varidaki, D. Ferguson, S. J. Gold, V. Zachariou, A unique role of RGS9-2 in the striatum as a positive or negative regulator of opiate analgesia. J. Neurosci. 31, 5617-5624 (2011).
26. V. Zachariou, D. Georgescu, N. Sanchez, Z. Rahman, R. DiLeone, O. Berton, R. L. Neve, L. J. Sim-Selley, D. E. Selley, S. J. Gold, E. J. Nestler, Essential role for RGS9 in opiate action. Proc. Natl. Acad. Sci. U.S.A. 100, 13656-13661 (2003).
27. B. Sjögren, L. L. Blazer, R. R. Neubig, Regulators of G protein signaling proteins as targets for drug discovery. Prog. Mol. Biol. Transl. Sci. 91, 81-119 (2010).
28. K. L. McCoy, J. R. Hepler, Regulators of G protein signaling proteins as central components of G protein-coupled receptor signaling complexes. Prog. Mol. Biol. Transl. Sci. 86, 49-74 (2009).
29. M. Abramow-Newerly, A. A. Roy, C. Nunn, P. Chidiac, RGS proteins have a signalling complex: Interactions between RGS proteins and GPCRs, effectors, and auxiliary proteins. Cell. Signal. 18, 579-591 (2006).
30. J. Hanoune, N. Defer, Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 41, 145-174 (2001).
31. K. C. Bradley, A. J. Mullins, R. L. Meisel, V. J. Watts, Sexual experience alters D1 receptor-mediated cyclic AMP production in the nucleus accumbens of female Syrian hamsters. Synapse 53, 20-27 (2004).
32. M. J. Miserendino, E. J. Nestler, Behavioral sensitization to cocaine: Modulation by the cyclic AMP system in the nucleus accumbens. Brain Res. 674, 299-306 (1995).
33. E. J. Nestler, Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2, 119-128 (2001).
34. E. V. Varga, M. Rubenzik, V. Grife, M. Sugiyama, D. Stropova, W. R. Roeske, H. I. Yamamura, Involvement of Raf-1 in chronic δ-opioid receptor agonist-mediated adenylyl cyclase superactivation. Eur. J. Pharmacol. 451, 101-102 (2002).
35. E. V. Varga, D. Stropova, M. Rubenzik, S. Waite, W. R. Roeske, H. I. Yamamura, Phosphorylation of adenylyl cyclase VI upon chronic δ-opioid receptor stimulation. Eur. J. Pharmacol. 364, R1-R3 (1999).
36. J. R. Traynor, D. Terzi, B. J. Caldarone, V. Zachariou, RGS9-2: Probing an intracellular modulator of behavior as a drug target. Trends Pharmacol. Sci. 30, 105-111 (2009).
37. R. Taussig, J. A. Iñiguez-Lluhi, A. G. Gilman, Inhibition of adenylyl cyclase by Giα. Science 261, 218- 221 (1993).
38. R. Taussig, W. J. Tang, J. R. Hepler, A. G. Gilman, Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases. J. Biol. Chem. 269, 6093-6100 (1994).
39. M. J. Clark, R. R. Neubig, J. R. Traynor, Endogenous regulator of G protein signaling proteins suppress Gαo-dependent, m-opioid agonist-mediated adenylyl cyclase supersensitization. J. Pharmacol. Exp. Ther. 310, 215-222 (2004).
40. S. Sinnarajah, C. W. Dessauer, D. Srikumar, J. Chen, J. Yuen, S. Yilma, J. C. Dennis, E. E. Morrison, V. Vodyanoy, J. H. Kehrl, RGS2 regulates signal transduction in olfactory neurons by attenuating activation of adenylyl cyclase III. Nature 409, 1051-1055 (2001).
41. S. Salim, S. Sinnarajah, J. H. Kehrl, C. W. Dessauer, Identification of RGS2 and type V adenylyl cyclase interaction sites. J. Biol. Chem. 278, 15842-15849 (2003).
42. P. Radivojac, L. M. Iakoucheva, C. J. Oldfield, Z. Obradovic, V. N. Uversky, A. K. Dunker, Intrinsic disorder and functional proteomics. Biophys. J. 92, 1439-1456 (2007).
43. H. J. Dyson, P. E. Wright, Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208 (2005).
44. M. Lomazzi, P. A. Slesinger, C. Lüscher, Addictive drugs modulate GIRK-channel signaling by regulating RGS proteins. Trends Pharmacol. Sci. 29, 544-549 (2008).
45. C. K. Chen, P. Eversole-Cire, H. Zhang, V. Mancino, Y. J. Chen, W. He, T. G. Wensel, M. I. Simon, Instability of GGL domain-containing RGS proteins in mice lacking the G protein β-subunit Gβ5. Proc. Natl. Acad. Sci. U.S.A. 100, 6604 -6609 (2003).
46. C. K. Chen, M. E. Burns, W. He, T. G. Wensel, D. A. Baylor, M. I. Simon, Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403, 557-560 (2000).
47. J. H. Song, J. J. Waataja, K. A. Martemyanov, Subcellular targeting of RGS9-2 is controlled by multiple molecular determinants on its membrane anchor, R7BP. J. Biol. Chem. 281, 15361-15369 (2006).
48. G. R. Anderson, A. Semenov, J. H. Song, K. A. Martemyanov, The membrane anchor R7BP controls the proteolytic stability of the striatal specific RGS protein, RGS9-2. J. Biol. Chem. 282, 4772-4781 (2007).
49. M. S. Kapiloff, L. A. Piggott, R. Sadana, J. Li, L. A. Heredia, E. Henson, R. Efendiev, C. W. Dessauer, An adenylyl cyclase-mAKAP b signaling complex regulates cAMP levels in cardiac myocytes. J. Biol. Chem. 284, 23540-23546 (2009).
50. C. W. Dessauer, J. J. Tesmer, S. R. Sprang, A. G. Gilman, Identification of a Giα binding site on type V adenylyl cyclase. J. Biol. Chem. 273, 25831-25839 (1998).
51. N. P. Skiba, K. A. Martemyanov, A. Elfenbein, J. A. Hopp, A. Bohm, W. F. Simonds, V. Y. Arshavsky, RGS9-Gβ5 substrate selectivity in photoreceptors. Opposing effects of constituent domains yield high affinity of RGS interaction with the G protein-effector complex. J. Biol. Chem. 276, 37365-37372 (2001).
52. K. A. Martemyanov, P. J. Yoo, N. P. Skiba, V. Y. Arshavsky, R7BP, a novel neuronal protein interacting with RGS proteins of the R7 family. J. Biol. Chem. 280, 5133-5136 (2005).
53. R. E. Whisnant, A. G. Gilman, C. W. Dessauer, Interaction of the two cytosolic domains of mammalian adenylyl cyclase. Proc. Natl. Acad. Sci. U.S.A. 93, 6621-6625 (1996).
54. T. Kozasa, Purification of G protein subunits from Sf9 insect cells using hexahistidine-tagged α and βγ subunits. Methods Mol. Biol. 237, 21-38 (2004).
55. B. Hollins, S. Kuravi, G. J. Digby, N. A. Lambert, The c-terminus of GRK3 indicates rapid dissociation of G protein heterotrimers. Cell. Signal. 21, 1015-1021 (2009).
56. C. W. Dessauer, Kinetic analysis of the action of P-site analogs. Methods Enzymol. 345, 112-126 (2002).
57. K. A. Martemyanov, P. J. Yoo, N. P. Skiba, V. Y. Arshavsky, R7BP, a novel neuronal protein interacting with RGS proteins of the R7 family. J. Biol. Chem. 280, 5133-5136 (2005).
58. J. H. Zhang, W. F. Simonds, Copurification of brain G-protein β5 with RGS6 and RGS7. J. Neurosci. 20, RC59 (2000).
59. J. B. Klarenbeek, J. Goedhart, M. A. Hink, T. W. Gadella, K. Jalink, A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS One 6, e19170 (2011).
60. K. Xie, K. L. Allen, S. Kourrich, J. Cólon-Saez, M. J. Thomas, K.Wickman, K. A.Martemyanov, Gβ5 recruits R7 RGS proteins to GIRK channels to regulate the timing of neuronal inhibitory signaling. Nat. Neurosci. 13, 661-663 (2010).
61. N. A. Lambert, C. A. Johnston, S. D. Cappell, S. Kuravi, A. J. Kimple, F. S. Willard, D. P. Siderovski, Regulators of G-protein signaling accelerate GPCR signaling kinetics and govern sensitivity solely by accelerating GTPase activity. Proc. Natl. Acad. Sci. U.S.A. 107, 7066-7071 (2010).