Rab family proteins regulate the endosomal trafficking and function of RGS4

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21836-21849

  Bastin, Guillaume ^a,b   Heximer, Scott P ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b University Lille   (France)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN; INTRACELLULAR TRAFFICKING;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

CELL PROTEIN; CYSTEINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MUSCARINIC M1 RECEPTOR; PROTEIN M1R; RAB PROTEIN; RAB11 PROTEIN; RAB5 PROTEIN; RGS4 PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

CELL BIOLOGY; ENDOCYTOSIS; G-PROTEIN-COUPLED RECEPTORS (GPCR); G-PROTEINS; RGS PROTEINS; SIGNALING;

BLOTTING, WESTERN; CELL MEMBRANE; ENDOSOMES; HEK293 CELLS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MUTATION; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RECEPTOR, MUSCARINIC M1; RGS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84881227000     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.466888     Document Type: Article

References (95)

1. Ross, E. M., and Wilkie, T. M. (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGSlike proteins. Annu. Rev. Biochem. 69, 795-827
2. Hollinger, S., and Hepler, J. R. (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev. 54, 527-559
3. Berman, D. M., Kozasa, T., and Gilman, A. G. (1996) The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis. J. Biol. Chem. 271, 27209-27212
4. Watson, N., Linder, M. E., Druey, K. M., Kehrl, J. H., and Blumer, K. J. (1996) RGS family members: GTPase-activating proteins for heterotrimeric G-protein-subunits. Nature 383, 172-175
5. Pacey, L. K., Heximer, S. P., and Hampson, D. R. (2009) Increased GABAB receptor-mediated signaling reduces the susceptibility of fragile X knockout mice to audiogenic seizures. Mol. Pharmacol. 76, 18-24
6. Lerner, T. N., and Kreitzer, A. C. (2012) RGS4 is required for dopaminergic control of striatal LTD and susceptibility to parkinsonian motor deficits. Neuron 73, 347-359
7. Cifelli, C., Rose, R. A., Zhang, H., Voigtlaender-Bolz, J., Bolz, S. S., Backx, P. H., and Heximer, S. P. (2008) RGS4 regulates parasympathetic signaling and heart rate control in the sinoatrial node. Circ. Res. 103, 527-535
8. Ruiz de Azua, I., Scarselli, M., Rosemond, E., Gautam, D., Jou, W., Gavrilova, O., Ebert, P. J., Levitt, P., and Wess, J. (2010) RGS4 is a negative regulator of insulin release from pancreatic-cells in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 107, 7999-8004
9. Ruiz de Azua, I., Gautam, D., Guettier, J. M., and Wess, J. (2011) Novel insights into the function of-cellM3muscarinic acetylcholine receptors: therapeutic implications. Trends Endocrinol. Metab. 22, 74-80
10. Xie, Y., Wolff, D. W., Wei, T., Wang, B., Deng, C., Kirui, J. K., Jiang, H., Qin, J., Abel, P. W., and Tu, Y. (2009) Breast cancer migration and invasion depend on proteasome degradation of regulator of G-protein signaling 4. Cancer Res. 69, 5743-5751
11. Ding, L., and Hegde, A. N. (2009) Expression of RGS4 splice variants in dorsolateral prefrontal cortex of schizophrenic and bipolar disorder patients. Biol. Psychiatry 65, 541-545
12. Mirnics, K., Middleton, F. A., Stanwood, G. D., Lewis, D. A., and Levitt, P. (2001) Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia. Mol. Psychiatry 6, 293-301
13. Muma, N. A., Mariyappa, R., Williams, K., and Lee, J. M. (2003) Differences in regional and subcellular localization of Gq/11 and RGS4 protein levels in Alzheimer's disease: correlation with muscarinic M1 receptor binding parameters. Synapse 47, 58-65
14. Emilsson, L., Saetre, P., and Jazin, E. (2006) Low mRNA levels of RGS4 splice variants in Alzheimer's disease: association between a rare haplotype and decreased mRNA expression. Synapse 59, 173-176
15. Mittmann, C., Chung, C. H., Höppner, G., Michalek, C., Nose, M., Schüler, C., Schuh, A., Eschenhagen, T., Weil, J., Pieske, B., Hirt, S., and Wieland, T. (2002) Expression of 10 RGS proteins in human myocardium: functional characterization of an up-regulation of RGS4 in heart failure. Cardiovasc. Res. 55, 778-786
16. Bastin, G., Singh, K., Dissanayake, K., Mighiu, A. S., Nurmohamed, A., and Heximer, S. P. (2012) Amino-terminal cysteine residues differentially influence RGS4 protein plasma membrane targeting, intracellular trafficking, and function. J. Biol. Chem. 287, 28966-28974
17. Christoforidis, S., McBride, H. M., Burgoyne, R. D., and Zerial, M. (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397, 621-625
18. Simonsen, A., Lippé, R., Christoforidis, S., Gaullier, J. M., Brech, A., Callaghan, J., Toh, B. H., Murphy, C., Zerial, M., and Stenmark, H. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498
19. Baetz, N. W., and Goldenring, J. R. (2013) Rab11-family interacting proteins define spatially and temporally distinct regions within the dynamic Rab11a-dependent recycling system. Mol. Biol. Cell 24, 643-658
20. Sørensen, J. B., Wiederhold, K., Müller, E. M., Milosevic, I., Nagy, G., de Groot, B. L., Grubmüller, H., and Fasshauer, D. (2006) Sequential N-to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 25, 955-966
21. Luzio, J. P., Gray, S. R., and Bright, N. A. (2010) Endosome-lysosome fusion. Biochem. Soc. Trans. 38, 1413-1416
22. Ishida, M., Ohbayashi, N., Maruta, Y., Ebata, Y., and Fukuda, M. (2012) Functional involvement of Rab1A in microtubule-dependent anterograde melanosome transport in melanocytes. J. Cell Sci. 125, 5177-5187
23. Horgan, C. P., and McCaffrey, M. W. (2011) Rab GTPases and microtubule motors. Biochem. Soc. Trans. 39, 1202-1206
24. Feng, Y., Press, B., and Wandinger-Ness, A. (1995) Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 131, 1435-1452
25. Chavrier, P., Parton, R. G., Hauri, H. P., Simons, K., and Zerial, M. (1990) Localization of low molecular weight GTP-binding proteins to exocytic and endocytic compartments. Cell 62, 317-329
26. Urbé, S., Huber, L. A., Zerial, M., Tooze, S. A., and Parton, R. G. (1993) Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 334, 175-182
27. Cavalli, V., Corti, M., and Gruenberg, J. (2001) Endocytosis and signaling cascades: a close encounter. FEBS Lett. 498, 190-196
28. Burd, C. G. (2011) Physiology and pathology of endosome-to-Golgi retrograde sorting. Traffic 12, 948-955
29. Lau, A. W., and Chou, M. M. (2008) The adaptor complex AP-2 regulates post-endocytic trafficking through the non-clathrin Arf6-dependent endocytic pathway. J. Cell Sci. 121, 4008-4017
30. Tanabe, K., Torii, T., Natsume, W., Braesch-Andersen, S., Watanabe, T., and Satake, M. (2005) A novel GTPase-activating protein for ARF6 directly interacts with clathrin and regulates clathrin-dependent endocytosis. Mol. Biol. Cell 16, 1617-1628
31. Gu, S., He, J., Ho, W. T., Ramineni, S., Thal, D. M., Natesh, R., Tesmer, J. J., Hepler, J. R., and Heximer, S. P. (2007) Unique hydrophobic extension of the RGS2 amphipathic helix domain imparts increased plasma membrane binding and function relative to other RGS R4/B subfamily members. J. Biol. Chem. 282, 33064-33075
32. Paspalas, C. D., Selemon, L. D., and Arnsten, A. F. (2009) Mapping the regulator of G protein signaling 4 (RGS4): presynaptic and postsynaptic substrates for neuroregulation in prefrontal cortex. Cereb. Cortex 19, 2145-2155
33. Lee, M. J., Tasaki, T., Moroi, K., An, J. Y., Kimura, S., Davydov, I. V., and Kwon, Y. T. (2005) RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl. Acad. Sci. U.S.A. 102, 15030-15035
34. Davydov, I. V., and Varshavsky, A. (2000) RGS4 is arginylated and degraded by the N-end rule pathway in vitro. J. Biol. Chem. 275, 22931-22941
35. García-Mata, R., Bebök, Z., Sorscher, E. J., and Sztul, E. S. (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146, 1239-1254
36. Grimsey, N. L., Goodfellow, C. E., Dragunow, M., and Glass, M. (2011) Cannabinoid receptor 2 undergoes Rab5-mediated internalization and recycles via a Rab11-dependent pathway. Biochim. Biophys. Acta 1813, 1554-1560
37. Esseltine, J. L., Dale, L. B., and Ferguson, S. S. (2011) Rab GTPases bind at a common site within the angiotensin II type I receptor carboxyl-terminal tail: evidence that Rab4 regulates receptor phosphorylation, desensitization, and resensitization. Mol. Pharmacol. 79, 175-184
38. Hinkle, P. M., Gehret, A. U., and Jones, B. W. (2012) Desensitization, trafficking, and resensitization of the pituitary thyrotropin-releasing hormone receptor. Front. Neurosci. 6, 180
39. Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R. T., and Lefkowitz, R. J. (2001)-Arrestin-mediated ADP-ribosylation factor 6 activation and2-adrenergic receptor endocytosis. J. Biol. Chem. 276, 42509-42513
40. Fan, G. H., Lapierre, L. A., Goldenring, J. R., and Richmond, A. (2003) Differential regulation of CXCR2 trafficking by Rab GTPases. Blood 101, 2115-2124
41. Bouley, R., Lin, H. Y., Raychowdhury, M. K., Marshansky, V., Brown, D., and Ausiello, D. A. (2005) Down-regulation of the vasopressin type 2 receptor after vasopressin-induced internalization: involvement of a lysosomal degradation pathway. Am. J. Physiol. Cell Physiol. 288, C1390-C1401
42. Anborgh, P. H., Seachrist, J. L., Dale, L. B., and Ferguson, S. S. (2000) Receptor/-arrestin complex formation and the differential trafficking and resensitization of2-adrenergic and angiotensin II type 1A receptors. Mol. Endocrinol. 14, 2040-2053
43. Kantamneni, S., Holman, D., Wilkinson, K. A., Nishimune, A., and Henley, J. M. (2009) GISP increases neurotransmitter receptor stability by downregulating ESCRT-mediated lysosomal degradation. Neurosci. Lett. 452, 106-110
44. Dores, M. R., Chen, B., Lin, H., Soh, U. J., Paing, M. M., Montagne, W. A., Meerloo, T., and Trejo, J. (2012) ALIX binds a YPX(3)L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting. J. Cell Biol. 197, 407-419
45. Tatenhorst, L., Senner, V., Püttmann, S., and Paulus, W. (2004) Regulators of G-protein signaling 3 and 4 (RGS3, RGS4) are associated with glioma cell motility. J. Neuropathol. Exp. Neurol. 63, 210-222
46. Hurst, J. H., Mendpara, N., and Hooks, S. B. (2009) Regulator of G-protein signalling expression and function in ovarian cancer cell lines. Cell. Mol. Biol. Lett. 14, 153-174
47. Wang, Q., and Traynor, J. R. (2011) Opioid-induced down-regulation of RGS4: role of ubiquitination and implications for receptor cross-talk. J. Biol. Chem. 286, 7854-7864
48. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., and van Deurs, B. (2000) Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11, 467-480
49. Takahashi, S., Kubo, K., Waguri, S., Yabashi, A., Shin, H. W., Katoh, Y., and Nakayama, K. (2012) Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J. Cell Sci. 125, 4049-4057
50. Gidon, A., Bardin, S., Cinquin, B., Boulanger, J., Waharte, F., Heliot, L., de la Salle, H., Hanau, D., Kervrann, C., Goud, B., and Salamero, J. (2012) A Rab11A/myosin Vb/Rab11-FIP2 complex frames two late recycling steps of langerin from the ERC to the plasma membrane. Traffic 13, 815-833
51. Maxfield, F. R., and McGraw, T. E. (2004) Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132
52. Tsutsumi, R., Fukata, Y., Noritake, J., Iwanaga, T., Perez, F., and Fukata, M. (2009) Identification of G protein α subunit-palmitoylating enzyme. Mol. Cell. Biol. 29, 435-447
53. Roy, A. A., Lemberg, K. E., and Chidiac, P. (2003) Recruitment of RGS2 and RGS4 to the plasma membrane by G proteins and receptors reflects functional interactions. Mol. Pharmacol. 64, 587-593
54. Huang, J., and Fisher, R. A. (2009) Nuclear trafficking of regulator of G protein signaling proteins and their roles in the nucleus. Prog. Mol. Biol. Transl. Sci. 86, 115-156
55. Chatterjee, T. K., Liu, Z., and Fisher, R. A. (2003) Human RGS6 gene structure, complex alternative splicing, and role of N terminus and G protein-subunit-like (GGL) domain in subcellular localization of RGS6 splice variants. J. Biol. Chem. 278, 30261-30271
56. Grabowska, D., Jayaraman, M., Kaltenbronn, K. M., Sandiford, S. L., Wang, Q., Jenkins, S., Slepak, V. Z., Smith, Y., and Blumer, K. J. (2008) Postnatal induction and localization of R7BP, a membrane-anchoring protein for regulator of G protein signaling 7 family-G-5 complexes in brain. Neuroscience 151, 969-982
57. Bernstein, L. S., Grillo, A. A., Loranger, S. S., and Linder, M. E. (2000) RGS4 binds to membranes through an amphipathic-helix. J. Biol. Chem. 275, 18520-18526
58. Delaney, K. A., Murph, M. M., Brown, L. M., and Radhakrishna, H. (2002) Transfer of M2 muscarinic acetylcholine receptors to clathrin-derived early endosomes following clathrin-independent endocytosis. J. Biol. Chem. 277, 33439-33446
59. Giguère, P., Rochdi, M. D., Laroche, G., Dupré, E., Whorton, M. R., Sunahara, R. K., Claing, A., Dupuis, G., and Parent, J. L. (2006) ARF6 activation by G-q signaling: G-q forms molecular complexes with ARNO and ARF6. Cell. Signal. 18, 1988-1994
60. Laroche, G., Giguère, P. M., Dupré, E., Dupuis, G., and Parent, J. L. (2007) The N-terminal coiled-coil domain of the cytohesin/ARNO family of guanine nucleotide exchange factors interacts with G-q. Mol. Cell. Biochem. 306, 141-152
61. Moreau, K., Ravikumar, B., Puri, C., and Rubinsztein, D. C. (2012) Arf6 promotes autophagosome formation via effects on phosphatidylinositol 4,5-bisphosphate and phospholipase D. J. Cell Biol. 196, 483-496
62. Macia, E., Partisani, M., Paleotti, O., Luton, F., and Franco, M. (2012) Arf6 negatively controls the rapid recycling of the2 adrenergic receptor. J. Cell Sci. 125, 4026-4035
63. Reiner, C., and Nathanson, N. M. (2008) The internalization of theM2and M4 muscarinic acetylcholine receptors involves distinct subsets of small G-proteins. Life Sci. 82, 718-727
64. Kanamarlapudi, V., Owens, S. E., Saha, K., Pope, R. J., and Mundell, S. J. (2012) ARF6-dependent regulation of P2Y receptor traffic and function in human platelets. PLoS One 7, e43532
65. Borroni, V., and Barrantes, F. J. (2011) Cholesterol modulates the rate and mechanism of acetylcholine receptor internalization. J. Biol. Chem. 286, 17122-17132
66. Fielding, A. B., Schonteich, E., Matheson, J., Wilson, G., Yu, X., Hickson, G. R., Srivastava, S., Baldwin, S. A., Prekeris, R., and Gould, G. W. (2005) Rab11-FIP3 and-FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389-3399
67. Prigent, M., Dubois, T., Raposo, G., Derrien, V., Tenza, D., Rossé, C., Camonis, J., and Chavrier, P. (2003) ARF6 controls post-endocytic recycling through its downstream exocyst complex effector. J. Cell Biol. 163, 1111-1121
68. Boshans, R. L., Szanto, S., van Aelst, L., and D'souza-Schorey, C. (2000) ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol. Cell. Biol. 20, 3685-3694
69. Bose, A., Cherniack, A. D., Langille, S. E., Nicoloro, S. M., Buxton, J. M., Park, J. G., Chawla, A., and Czech, M. P. (2001) G(-)11 signaling through ARF6 regulates F-actin mobilization and GLUT4 glucose transporter translocation to the plasma membrane. Mol. Cell. Biol. 21, 5262-5275
70. Zeigerer, A., Gilleron, J., Bogorad, R. L., Marsico, G., Nonaka, H., Seifert, S., Epstein-Barash, H., Kuchimanchi, S., Peng, C. G., Ruda, V. M., Del Conte-Zerial, P., Hengstler, J. G., Kalaidzidis, Y., Koteliansky, V., and Zerial, M. (2012) Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485, 465-470
71. Stokes, L. (2013) Rab5 regulates internalisation of P2X4 receptors and potentiation by ivermectin. Purinergic Signal. 9, 113-121
72. Dale, L. B., Seachrist, J. L., Babwah, A. V., and Ferguson, S. S. (2004) Regulation of angiotensin II type 1A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J. Biol. Chem. 279, 13110-13118
73. Shin, H. W., Hayashi, M., Christoforidis, S., Lacas-Gervais, S., Hoepfner, S., Wenk, M. R., Modregger, J., Uttenweiler-Joseph, S., Wilm, M., Nystuen, A., Frankel, W. N., Solimena, M., De Camilli, P., and Zerial, M. (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J. Cell Biol. 170, 607-618
74. Huotari, J., and Helenius, A. (2011) Endosome maturation. EMBO J. 30, 3481-3500
75. Rink, J., Ghigo, E., Kalaidzidis, Y., and Zerial, M. (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749
76. Hagiwara, M., Shirai, Y., Nomura, R., Sasaki, M., Kobayashi, K., Tadokoro, T., and Yamamoto, Y. (2009) Caveolin-1 activates Rab5 and enhances endocytosis through direct interaction. Biochem. Biophys. Res. Commun. 378, 73-78
77. Pelkmans, L., Bürli, T., Zerial, M., and Helenius, A. (2004) Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767-780
78. Seachrist, J. L., and Ferguson, S. S. (2003) Regulation of G protein-coupled receptor endocytosis and trafficking by Rab GTPases. Life Sci. 74, 225-235
79. Hubbard, V. M., Valdor, R., Patel, B., Singh, R., Cuervo, A. M., and Macian, F. (2010) Macroautophagy regulates energy metabolism during effector T cell activation. J. Immunol. 185, 7349-7357
80. Korolchuk, V. I., Saiki, S., Lichtenberg, M., Siddiqi, F. H., Roberts, E. A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F. M., O'Kane, C. J., Deretic, V., and Rubinsztein, D. C. (2011) Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 13, 453-460
81. Ioannou, Y. A., Bishop, D. F., and Desnick, R. J. (1992) Overexpression of human-galactosidase A results in its intracellular aggregation, crystallization in lysosomes, and selective secretion. J. Cell Biol. 119, 1137-1150
82. Svensson, L., Stanley, P., Willenbrock, F., and Hogg, N. (2012) The G-q/11 proteins contribute to T lymphocyte migration by promoting turnover of integrin LFA-1 through recycling. PLoS One 7, e38517
83. Chia, P. Z., Gasnereau, I., Lieu, Z. Z., and Gleeson, P. A. (2011) Rab9-dependent retrograde transport and endosomal sorting of the endopeptidase furin. J. Cell Sci. 124, 2401-2413
84. Smith, D. C., Spooner, R. A., Watson, P. D., Murray, J. L., Hodge, T. W., Amessou, M., Johannes, L., Lord, J. M., and Roberts, L. M. (2006) Internalized Pseudomonas exotoxin A can exploit multiple pathways to reach the endoplasmic reticulum. Traffic 7, 379-393
85. Ng, E. L., Gan, B. Q., Ng, F., and Tang, B. L. (2012) Rab GTPases regulating receptor trafficking at the late endosome-lysosome membranes. Cell Biochem. Funct. 30, 515-523
86. Sullivan, B. M., Harrison-Lavoie, K. J., Marshansky, V., Lin, H. Y., Kehrl, J. H., Ausiello, D. A., Brown, D., and Druey, K. M. (2000) RGS4 and RGS2 bind coatomer and inhibit COPI association with Golgi membranes and intracellular transport. Mol. Biol. Cell 11, 3155-3168
87. Takata, K. (2006) Aquaporin-2 (AQP2): its intracellular compartment and trafficking. Cell. Mol. Biol. 52, 34-39
88. Jing, J., Junutula, J. R., Wu, C., Burden, J., Matern, H., Peden, A. A., and Prekeris, R. (2010) FIP1/RCP binding to Golgin-97 regulates retrograde transport from recycling endosomes to the trans-Golgi network. Mol. Biol. Cell 21, 3041-3053
89. Dugani, C. B., and Klip, A. (2005) Glucose transporter 4: cycling, compartments and controversies. EMBO Rep. 6, 1137-1142
90. Wieman, H. L., Wofford, J. A., and Rathmell, J. C. (2007) Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell 18, 1437-1446
91. Jaén, C., and Doupnik, C. A. (2006) RGS3 and RGS4 differentially associate with G protein-coupled receptor-Kir3 channel signaling complexes revealing two modes of RGS modulation. Precoupling and collision coupling. J. Biol. Chem. 281, 34549-34560
92. Zhang, Q., Pacheco, M. A., and Doupnik, C. A. (2002) Gating properties of GIRK channels activated by G-(o)-and G-(i)-coupled muscarinic m2 receptors in Xenopus oocytes: the role of receptor precoupling in RGS modulation. J. Physiol. 545, 355-373
93. Chen, Y., Liu, Y., Cottingham, C., McMahon, L., Jiao, K., Greengard, P., and Wang, Q. (2012) Neurabin scaffolding of adenosine receptor and RGS4 regulates anti-seizure effect of endogenous adenosine. J. Neurosci. 32, 2683-2695
94. Schwendt, M., Sigmon, S. A., and McGinty, J. F. (2012) RGS4 overexpression in the rat dorsal striatum modulates mGluR5-and amphetaminemediated behavior and signaling. Psychopharmacology 221, 621-635
95. Harris, I. S., Treskov, I., Rowley, M. W., Heximer, S., Kaltenbronn, K., Finck, B. N., Gross, R. W., Kelly, D. P., Blumer, K. J., and Muslin, A. J. (2004) G-protein signaling participates in the development of diabetic cardiomyopathy. Diabetes 53, 3082-3090