Regulation of the G-protein regulatory-Gαi signaling complex by nonreceptor guanine nucleotide exchange factors

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3003-3015

  Oner, Sukru Sadik ^a   Maher, Ellen M ^a   Gabay, Meital ^b   Tall, Gregory G ^b   Blumer, Joe B ^a   Lanier, Stephen M ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX FORMATIONS; DYNAMIC INTERACTION; G PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; REGULATORY MECHANISM; SIGNALING COMPLEX; SUBCELLULAR LOCALIZATIONS;

NUCLEOTIDES; POSITIVE IONS;

PROTEINS;

AGS1 PROTEIN; AGS3 PROTEIN; AGS4 PROTEIN; GIV PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PERTUSSIS TOXIN; RIC 8A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CELL FRACTIONATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER TECHNIQUES; CELL FRACTIONATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; MICE; MUTANT PROTEINS; NEURONS; PERTUSSIS TOXIN; RAS PROTEINS; RECOMBINANT FUSION PROTEINS; RGS PROTEINS; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 84873324774     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.418467     Document Type: Article

References (80)

1. Cismowski, M. J., Takesono, A., Ma, C., Lizano, J. S., Xie, X., Fuernkranz, H., Lanier, S. M., and Duzic, E. (1999) Genetic screens in yeast to identify mammalian nonreceptor modulators of G-protein signaling. Nat. Biotechnol. 17, 878-883
2. Takesono, A., Cismowski, M. J., Ribas, C., Bernard, M., Chung, P., Hazard, S., 3rd, Duzic, E., and Lanier, S. M. (1999) Receptor-independent activators of heterotrimeric G-protein signaling pathways. J. Biol. Chem. 274, 33202-33205
3. Blumer, J. B., Smrcka, A. V., and Lanier, S. M. (2007) Mechanistic pathways and biological roles for receptor-independent activators of G-protein signaling. Pharmacol. Ther. 113, 488-506
4. De Vries, L., Fischer, T., Tronchère, H., Brothers, G. M., Strockbine, B., Siderovski, D. P., and Farquhar, M. G. (2000) Activator of G-protein signaling 3 is a guanine dissociation inhibitor for Gαi subunits. Proc. Natl. Acad. Sci. U. S. A. 97, 14364-14369
5. Du, Q., Stukenberg, P. T., and Macara, I. G. (2001) A mammalian Partner of inscuteable binds NuMA and regulates mitotic spindle organization. Nat. Cell Biol. 3, 1069-1075
6. Garcia-Marcos, M., Ghosh, P., and Farquhar, M. G. (2009) GIV is a non-receptor GEF for Gαi with a unique motif that regulates Akt signaling. Proc. Natl. Acad. Sci. U. S. A. 106, 3178-3183
7. Gotta, M., and Ahringer, J. (2001) Distinct roles for Gα and Gβγ in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat. Cell Biol. 3, 297-300
8. Lee, M. J., and Dohlman, H. G. (2008) Coactivation of G-protein signaling by cell-surface receptors and an intracellular exchange factor. Curr. Biol. 18, 211-215
9. Parmentier, M. L., Woods, D., Greig, S., Phan, P. G., Radovic, A., Bryant, P., and O'Kane, C. J. (2000) Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. 20, RC84
10. Sato, M., Blumer, J. B., Simon, V., and Lanier, S. M. (2006) Accessory proteins for G-proteins. Partners in signaling. Annu. Rev. Pharmacol. Toxicol. 46, 151-187
11. Schaefer, M., Shevchenko, A., Shevchenko, A., and Knoblich, J. A. (2000) A protein complex containing Inscuteable and the Gα-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10, 353-362
12. Tall, G. G., Krumins, A. M., and Gilman, A. G. (2003) Mammalian Ric-8A (synembryn) is a heterotrimeric Gα protein guanine nucleotide exchange factor. J. Biol. Chem. 278, 8356-8362
13. i3 binding to calnuc on Golgi membranes in living cells monitored by fluorescence resonance energy transfer of green fluorescent protein fusion proteins. Proc. Natl. Acad. Sci. U. S. A. 98, 14961-14966
14. Willard, F. S., Kimple, R. J., and Siderovski, D. P. (2004) Return of the GDI. The GoLoco motif in cell division. Annu. Rev. Biochem. 73, 925-951
15. Yu, F., Morin, X., Cai, Y., Yang, X., and Chia, W. (2000) Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100, 399-409
16. Blumer, J. B., Sadik Oner, S., and Lanier, S. M. (2011) Group II activators of G-protein signalling and proteins containing a G-protein regulatory motif. Acta Physiol. 204, 202-218
17. Blumer, J. B., Lord, K., Saunders, T. L., Pacchioni, A., Black, C., Lazartigues, E., Varner, K. J., Gettys, T. W., and Lanier, S. M. (2008) Activator of G-protein signaling 3 null mice. I. Unexpected alterations in metabolic and cardiovascular function. Endocrinology 149, 3842-3849
18. Bowers, M. S., Hopf, F. W., Chou, J. K., Guillory, A. M., Chang, S. J., Janak, P. H., Bonci, A., and Diamond, I. (2008) Nucleus accumbens AGS3 expression drives ethanol seeking throughGβγ. Proc. Natl. Acad. Sci. U. S. A. 105, 12533-12538
19. Bowers, M. S., McFarland, K., Lake, R. W., Peterson, Y. K., Lapish, C. C., Gregory, M. L., Lanier, S. M., and Kalivas, P. W. (2004) Activator of Gprotein signaling 3. A gatekeeper of cocaine sensitization and drug seeking. Neuron 42, 269-281
20. Groves, B., Gong, Q., Xu, Z., Huntsman, C., Nguyen, C., Li, D., and Ma, D. (2007) A specific role of AGS3 in the surface expression of plasma membrane proteins. Proc. Natl. Acad. Sci. U. S. A. 104, 18103-18108
21. Lee, S. E., Simons, S. B., Heldt, S. A., Zhao, M., Schroeder, J. P., Vellano, C. P., Cowan, D. P., Ramineni, S., Yates, C. K., Feng, Y., Smith, Y., Sweatt, J. D., Weinshenker, D., Ressler, K. J., Dudek, S. M., and Hepler, J. R. (2010) RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc. Natl. Acad. Sci. U. S. A. 107, 16994-16998
22. Nadella, R., Blumer, J. B., Jia, G., Kwon, M., Akbulut, T., Qian, F., Sedlic, F., Wakatsuki, T., Sweeney, W. E., Jr., Wilson, P. D., Lanier, S. M., and Park, F. (2010) Activator of G-protein signaling 3 promotes epithelial cell proliferation in PKD. J. Am. Soc. Nephrol. 21, 1275-1280
23. Pattingre, S., De Vries, L., Bauvy, C., Chantret, I., Cluzeaud, F., Ogier-Denis, E., Vandewalle, A., and Codogno, P. (2003) The G-protein regulator AGS3 controls an early event during macroautophagy in human intestinal HT-29 cells. J. Biol. Chem. 278, 20995-21002
24. Regner, K. R., Nozu, K., Lanier, S. M., Blumer, J. B., Avner, E. D., Sweeney, W. E., Jr., and Park, F. (2011) Loss of activator of G-protein signaling 3 impairs renal tubular regeneration following acute kidney injury in rodents. FASEB J. 25, 1844-1855
25. Sans, N., Wang, P. Y., Du, Q., Petralia, R. S., Wang, Y. X., Nakka, S., Blumer, J. B., Macara, I. G., and Wenthold, R. J. (2005) mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell Biol. 7, 1079-1090
26. Walsh, T., Shahin, H., Elkan-Miller, T., Lee, M. K., Thornton, A. M., Roeb, W., Abu Rayyan, A., Loulus, S., Avraham, K. B., King, M. C., and Kanaan, M. (2010) Whole exome sequencing and homozygosity mapping identify mutation in the cell polarity protein GPSM2 as the cause of nonsyndromic hearing loss DFNB82. Am. J. Hum. Genet. 87, 90-94
27. Wiser, O., Qian, X., Ehlers, M., Ja, W. W., Roberts, R. W., Reuveny, E., Jan, Y. N., and Jan, L. Y. (2006) Modulation of basal and receptor-induced GIRK potassium channel activity and neuronal excitability by the mammalian PINS homolog LGN. Neuron 50, 561-573
28. Yao, L., McFarland, K., Fan, P., Jiang, Z., Inoue, Y., and Diamond, I. (2005) Activator of G-protein signaling 3 regulates opiate activation of protein kinase A signaling and relapse of heroin-seeking behavior. Proc. Natl. Acad. Sci. U. S. A. 102, 8746-8751
29. Yao, L., McFarland, K., Fan, P., Jiang, Z., Ueda, T., and Diamond, I. (2006) Adenosine A2a blockade prevents synergy between μ-opiate and cannabinoid CB1 receptors and eliminates heroin-seeking behavior in addicted rats. Proc. Natl. Acad. Sci. U. S. A. 103, 7877-7882
30. Ponting, C. P. (1999) Raf-like Ras/Rap-binding domains in RGS12-and still-life-like signalling proteins. J. Mol. Med. 77, 695-698
31. Siderovski, D. P., Diversé-Pierluissi Ma, and De Vries, L. (1999) The GoLoco motif. A Gαi/o binding motif and potential guanine-nucleotide exchange factor. Trends Biochem. Sci. 24, 340-341
32. An, N., Blumer, J. B., Bernard, M. L., and Lanier, S. M. (2008) The PDZ and band 4.1 containing protein Frmpd1 regulates the subcellular location of activator of G-protein signaling 3 and its interaction with G-proteins. J. Biol. Chem. 283, 24718-24728
33. Blumer, J. B., Bernard, M. L., Peterson, Y. K., Nezu, J., Chung, P., Dunican, D. J., Knoblich, J. A., and Lanier, S. M. (2003) Interaction of activator of G-protein signaling 3 (AGS3) with LKB1, a serine/threonine kinase involved in cell polarity and cell cycle progression. Phosphorylation of the G-protein regulatory (GPR) motif as a regulatory mechanism for the interaction of GPR motifs with Giα. J. Biol. Chem. 278, 23217-23220
34. Bowman, S. K., Neumüller, R. A., Novatchkova, M., Du, Q., and Knoblich, J. A. (2006) The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell 10, 731-742
35. Du, Q., and Macara, I. G. (2004) Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G-proteins. Cell 119, 503-516
36. Garcia-Marcos, M., Ear, J., Farquhar, M. G., and Ghosh, P. (2011) A GDI (AGS3) and a GEF (GIV) regulate autophagy by balancing G-protein activity and growth factor signals. Mol. Biol. Cell 22, 673-686
37. Johnston, C. A., Hirono, K., Prehoda, K. E., and Doe, C. Q. (2009) Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell 138, 1150-1163
38. o-mediated G-protein-coupled receptor signaling. Mol. Biol. Cell 20, 3865-3877
39. i-GDP complexes. Proc. Natl. Acad. Sci. U. S. A. 102, 16584-16589
40. Thomas, C. J., Tall, G. G., Adhikari, A., and Sprang, S. R. (2008) Ric-8A catalyzes guanine nucleotide exchange on Gαi1 bound to the GPR/GoLoco exchange inhibitor AGS3. J. Biol. Chem. 283, 23150-23160
41. Vellano, C. P., Shu, F. J., Ramineni, S., Yates, C. K., Tall, G. G., and Hepler, J. R. (2011) Activation of the regulator of G-protein signaling 14-Gαi1-GDP signaling complex is regulated by resistance to inhibitors of cholinesterase-8A. Biochemistry 50, 752-762
42. Oner, S. S., An, N., Vural, A., Breton, B., Bouvier, M., Blumer, J. B., and Lanier, S. M. (2010) Regulation of the AGS3αGαi signaling complex by a seven-transmembrane span receptor. J. Biol. Chem. 285, 33949-33958
43. Oner, S. S., Maher, E. M., Breton, B., Bouvier, M., and Blumer, J. B. (2010) Receptor-regulated interaction of activator of G-protein signaling-4 and Gαi. J. Biol. Chem. 285, 20588-20594
44. Cismowski, M. J., Ma, C., Ribas, C., Xie, X., Spruyt, M., Lizano, J. S., Lanier, S. M., and Duzic, E. (2000) Activation of heterotrimeric G-protein signaling by a Ras-related protein. Implications for signal integration. J. Biol. Chem. 275, 23421-23424
45. Hiskens, R., Vatish, M., Hill, C., Davey, J., and Ladds, G. (2005) Specific in vivo binding of activator of G-protein signalling 1 to the Gβ1 subunit. Biochem. Biophys. Res. Commun. 337, 1038-1046
46. i1 complex in live cells. J. Biol. Chem. 286, 38659-38669
47. i-coupled formyl peptide receptor to Erk-1/2 MAP kinases. J. Biol. Chem. 277, 10876-10882
48. Nguyen, C. H., and Watts, V. J. (2005) Dexras1 blocks receptor-mediated heterologous sensitization of adenylyl cyclase 1. Biochem. Biophys. Res. Commun. 332, 913-920
49. Vaidyanathan, G., Cismowski, M. J., Wang, G., Vincent, T. S., Brown, K. D., and Lanier, S. M. (2004) The Ras-related protein AGS1/RASD1 suppresses cell growth. Oncogene 23, 5858-5863
50. Baniwal, S. K., Khalid, O., Gabet, Y., Shah, R. R., Purcell, D. J., Mav, D., Kohn-Gabet, A. E., Shi, Y., Coetzee, G. A., and Frenkel, B. (2010) Runx2 transcriptome of prostate cancer cells. Insights into invasiveness and bone metastasis. Mol. Cancer 9, 258
51. Dalgin, G. S., Holloway, D. T., Liou, L. S., and De Lisi, C. (2007) Identification and characterization of renal cell carcinoma gene markers. Cancer Inform. 3, 65-92
52. de Souza Rocha Simonini, P., Breiling, A., Gupta, N., Malekpour, M., Youns, M., Omranipour, R., Malekpour, F., Volinia, S., Croce, C. M., Najmabadi, H., Diederichs, S., Sahin, O., Mayer, D., Lyko, F., Hoheisel, J. D., and Riazalhosseini, Y. (2010) Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor α in breast cancer cells. Cancer Res. 70, 9175-9184
53. Nojima, M., Maruyama, R., Yasui, H., Suzuki, H., Maruyama, Y., Tarasawa, I., Sasaki, Y., Asaoku, H., Sakai, H., Hayashi, T., Mori, M., Imai, K., Tokino, T., Ishida, T., Toyota, M., and Shinomura, Y. (2009) Genomic screening for genes silenced by DNA methylation revealed an association between RASD1 inactivation and dexamethasone resistance in multiple myeloma. Clin. Cancer Res. 15, 4356-4364
54. Shaw, E. J., Haylock, B., Husband, D., du Plessis, D., Sibson, D. R., Warnke, P. C., and Walker, C. (2011) Gene expression in oligodendroglial tumors. Cell Oncol. 34, 355-367
55. Ghosh, P., Beas, A. O., Bornheimer, S. J., Garcia-Marcos, M., Forry, E. P., Johannson, C., Ear, J., Jung, B. H., Cabrera, B., Carethers, J. M., and Farquhar, M. G. (2010) A Gαi-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol. Biol. Cell 21, 2338-2354
56. Garcia-Marcos, M., Jung, B. H., Ear, J., Cabrera, B., Carethers, J. M., and Ghosh, P. (2011) Expression of GIV/Girdin, a metastasis-related protein, predicts patient survival in colon cancer. FASEB J. 25, 590-599
57. Afshar, K., Willard, F. S., Colombo, K., Johnston, C. A., McCudden, C. R., Siderovski, D. P., and Gönczy, P. (2004) RIC-8 is required for GPR-1/2-dependentGα function during asymmetric division of C. elegans embryos. Cell 119, 219-230
58. Couwenbergs, C., Spilker, A. C., and Gotta, M. (2004) Control of embryonic spindle positioning and Gα activity by C. elegans RIC-8. Curr. Biol. 14, 1871-1876
59. i-dependent planar orientation of the mitotic spindle during asymmetric cell division. Nat. Cell Biol. 7, 1083-1090
60. Hampoelz, B., Hoeller, O., Bowman, S. K., Dunican, D., and Knoblich, J. A. (2005) Drosophila Ric-8 is essential for plasma-membrane localization of heterotrimeric G-proteins. Nat. Cell Biol. 7, 1099-1105
61. Hess, H. A., Röper, J. C., Grill, S. W., and Koelle, M. R. (2004) RGS-7 completes a receptor-independent heterotrimeric G-protein cycle to asymmetrically regulate mitotic spindle positioning in C. elegans. Cell 119, 209-218
62. qα signaling in the C. elegans nervous system. Neuron 27, 289-299
63. Miller, K. G., and Rand, J. B. (2000) A role for RIC-8 (Synembryn) and GOA-1 (Goα) in regulating a subset of centrosome movements during early embryogenesis in Caenorhabditis elegans. Genetics 156, 1649-1660
64. Wang, H., Ng, K. H., Qian, H., Siderovski, D. P., Chia, W., and Yu, F. (2005) Ric-8 controls Drosophila neural progenitor asymmetric division by regulating heterotrimeric G-proteins. Nat. Cell Biol. 7, 1091-1098
65. Woodard, G. E., Huang, N. N., Cho, H., Miki, T., Tall, G. G., and Kehrl, J. H. (2010) Ric-8A and Giα recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol. Cell. Biol. 30, 3519-3530
66. Gabay, M., Pinter, M. E., Wright, F. A., Chan, P., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., and Tall, G. G. (2011) Ric-8 proteins are molecular chaperones that direct nascent G-protein α subunit membrane association. Sci. Signal. 4, ra79
67. Audet, N., Galés, C., Archer-Lahlou, E., Vallières, M., Schiller, P. W., Bouvier, M., and Pineyro, G. (2008) Bioluminescence resonance energy transfer assays reveal ligand-specific conformational changes within preformed signaling complexes containing α-opioid receptors and heterotrimeric Gproteins. J. Biol. Chem. 283, 15078-15088
68. Galés, C., Rebois, R. V., Hogue, M., Trieu, P., Breit, A., Hébert, T. E., and Bouvier, M. (2005) Real-time monitoring of receptor and G-protein interactions in living cells. Nat. Methods 2, 177-184
69. Galés, C., Van Durm, J. J., Schaak, S., Pontier, S., Percherancier, Y., Audet, M., Paris, H., and Bouvier, M. (2006) Probing the activation-promoted structural rearrangements in preassembled receptor-G-protein complexes. Nat. Struct. Mol. Biol. 13, 778-786
70. i selectively blocks GoLoco motif binding. Direct evidence for Gα·GoLoco complexes in mitotic spindle dynamics. J. Biol. Chem. 283, 36698-36710
71. Chauhan, S., Jelen, F., Sharina, I., and Martin, E. (2012) The G-protein regulator LGN modulates the activity of the NO receptor soluble guanylate cyclase. Biochem. J. 446, 445-453
72. Groves, B., Abrahamsen, H., Clingan, H., Frantz, M., Mavor, L., Bailey, J., and Ma, D. (2010) An inhibitory role of the G-protein regulator AGS3 in mTOR-dependent macroautophagy. PLoS ONE 5, e8877
73. Hofler, C., and Koelle, M. R. (2011) AGS-3 alters Caenorhabditis elegans behavior after food deprivation via RIC-8 activation of the neural G-protein Gαo. J. Neurosci. 31, 11553-11562
74. Doherty, D., Chudley, A. E., Coghlan, G., Ishak, G. E., Innes, A. M., Lemire, E. G., Rogers, R. C., Mhanni, A. A., Phelps, I. G., Jones, S. J., Zhan, S. H., Fejes, A. P., Shahin, H., Kanaan, M., Akay, H., Tekin, M., FORGE Canada Consortium, Triggs-Raine, B., and Zelinski, T. (2012) GPSM2 mutations cause the brain malformations and hearing loss in Chudley-McCullough syndrome. Am. J. Hum. Genet. 90, 1088-1093
75. olf. J. Biol. Chem. 286, 2625-2635
76. Casey, P. J., Graziano, M. P., and Gilman, A. G. (1989) G-protein βγ subunits from bovine brain and retina: equivalent catalytic support of ADP-ribosylation of α subunits by pertussis toxin but differential interactions with Gsα. Biochemistry 28, 611-616
77. Bodenstein, J., Sunahara, R. K., and Neubig, R. R. (2007) N-terminal residues control proteasomal degradation of RGS2, RGS4, and RGS5 in human embryonic kidney 293 cells. Mol. Pharmacol. 71, 1040-1050
78. Thomas, C. J., Briknarová, K., Hilmer, J. K., Movahed, N., Bothner, B., Sumida, J. P., Tall, G. G., and Sprang, S. R. (2011) The nucleotide exchange factor Ric-8A is a chaperone for the conformationally dynamic nucleotidefree state of Gαi1. PLoS ONE 6, e23197
79. Figueroa, M., Hinrichs, M. V., Bunster, M., Babbitt, P., Martinez-Oyanedel, J., and Olate, J. (2009) Biophysical studies support a predicted superhelical structure with armadillo repeats for Ric-8. Protein Sci. 18, 1139-1145
80. Vural, A., Oner, S., An, N., Simon, V., Ma, D., Blumer, J. B., and Lanier, S. M. (2010) Distribution of activator of G-protein signaling 3 within the aggresomal pathway. Role of specific residues in the tetratricopeptide repeat domain and differential regulation by the AGS3 binding partners Gi (α) and mammalian inscuteable. Mol. Cell. Biol. 30, 1528-1540