Signal activation and inactivation by the Gα helical domain: A long-neglected partner in G protein signaling

Science Signaling

Volumn 5, Issue 226, 2012, Pages

  Dohlman, Henrik G ^a   Jones, Janice C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; RAS PROTEIN; PROTEIN P21;

ALPHA HELIX; CRYSTAL STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; ENZYME ACTIVATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; ENZYME ACTIVATION; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; ONCOGENE PROTEIN P21(RAS); PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84861760053     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003013     Document Type: Review

References (46)

1. G. H. Biddlecome, G. Berstein, E. M. Ross, Regulation of phospholipase C-β1 by Gq and m1 muscarinic cholinergic receptor. Steady-state balance of receptor-mediated activation and GTPase-activating protein-promoted deactivation. J. Biol. Chem. 271, 7999-8007 (1996) [published erratum appears in J. Biol. Chem. 271, 33705 (1996)].
2. G. L. Waldo, T. K. Ricks, S. N. Hicks, M. L. Cheever, T. Kawano, K. Tsuboi, X. Wang, C. Montell, T. Kozasa, J. Sondek, T. K. Harden, Kinetic scaffolding mediated by a phospholipase C-β and Gq signaling complex. Science 330, 974-980 (2010).
3. S. R. Sprang, G protein mechanisms: Insights from structural analysis. Annu. Rev. Biochem. 66, 639-678 (1997).
4. W. Liu, W. A. Clark, P. Sharma, J. K. Northup, Mechanism of allosteric regulation of the rod cGMP phosphodiesterase activity by the helical domain of transducin α subunit. J. Biol. Chem. 273, 34284-34292 (1998).
5. W. Liu, J. K. Northup, The helical domain of a G protein α subunit is a regulator of its effector. Proc. Natl. Acad. Sci. U.S.A. 95, 12878-12883 (1998).
6. D. W. Markby, R. Onrust, H. R. Bourne, Separate GTP binding and GTPase activating domains of a Gα subunit. Science 262, 1895-1901 (1993).
7. T. Higashijima, K. M. Ferguson, P. C. Sternweis, M. D. Smigel, A. G. Gilman, Effects of Mg2+ and the β γ-subunit complex on the interactions of guanine nucleotides with G proteins. J. Biol. Chem. 262, 762-766 (1987).
8. D. E. Coleman, S. R. Sprang, Crystal structures of the G protein Gi α 1 complexed with GDP and Mg2+: A crystallographic titration experiment. Biochemistry 37, 14376-14385 (1998).
9. C. A. Johnston, J. P. Taylor, Y. Gao, A. J. Kimple, J. C. Grigston, J. G. Chen, D. P. Siderovski, A. M. Jones, F. S. Willard, GTPase acceleration as the rate-limiting step in Arabidopsis G proteincoupled sugar signaling. Proc. Natl. Acad. Sci. U.S.A. 104, 17317-17322 (2007).
10. J. C. Jones, J. W. Duffy, M. Machius, B. R. Temple, H. G. Dohlman, A. M. Jones, The crystal structure of a self-activating G protein α subunit reveals its distinct mechanism of signal initiation. Sci. Signal. 4, ra8 (2011).
11. S. G. Rasmussen, B. T. DeVree, Y. Zou, A. C. Kruse, K. Y. Chung, T. S. Kobilka, F. S. Thian, P. S. Chae, E. Pardon, D. Calinski, J. M. Mathiesen, S. T. Shah, J. A. Lyons, M. Caffrey, S. H. Gellman, J. Steyaert, G. Skiniotis, W. I. Weis, R. K. Sunahara, B. K. Kobilka, Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011).
12. B. R. Conklin, H. R. Bourne, Structural elements of G alpha subunits that interact with G β γ, receptors, and effectors. Cell 73, 631-641 (1993).
13. W. M. Oldham, H. E. Hamm, Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9, 60-71 (2008).
14. K. M. Ferguson, T. Higashijima, M. D. Smigel, A. G. Gilman, The influence of bound GDP on the kinetics of guanine nucleotide binding to G proteins. J. Biol. Chem. 261, 7393-7399 (1986).
15. N. Van Eps, A. M. Preininger, N. Alexander, A. I. Kaya, S. Meier, J. Meiler, H. E. Hamm, W. L. Hubbell, Interaction of a G protein with an activated receptor opens the interdomain interface in the α subunit. Proc. Natl. Acad. Sci. U.S.A. 108, 9420-9424 (2011).
16. K. Y. Chung, S. G. Rasmussen, T. Liu, S. Li, B. T. DeVree, P. S. Chae, D. Calinski, B. K. Kobilka, V. L. Woods Jr., R. K. Sunahara, Conformational changes in the G protein Gs induced by the β2 adrenergic receptor. Nature 477, 611-615 (2011).
17. G. H. Westfield, S. G. Rasmussen, M. Su, S. Dutta, B. T. DeVree, K. Y. Chung, D. Calinski, G. Velez-Ruiz, A. N. Oleskie, E. Pardon, P. S. Chae, T. Liu, S. Li, V. L. Woods, Jr, J. Steyaert, B. K. Kobilka, R. K. Sunahara, G. Skiniotis, Structural flexibility of the G α s α-helical domain in the β2- adrenoceptor Gs complex. Proc. Natl. Acad. Sci. U.S.A. 108, 16086-16091 (2011).
18. R. K. Sunahara, J. J. Tesmer, A. G. Gilman, S. R. Sprang, Crystal structure of the adenylyl cyclase activator Gsα. Science 278, 1943-1947 (1997).
19. 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 Gi β 1 α 1 γ 2. Cell 83, 1047-1058 (1995).
20. C. Janetopoulos, T. Jin, P. Devreotes, Receptormediated activation of heterotrimeric G-proteins in living cells. Science 291, 2408-2411 (2001).
21. T. M. Yi, H. Kitano, M. I. Simon, A quantitative characterization of the yeast heterotrimeric G protein cycle. Proc. Natl. Acad. Sci. U.S.A. 100, 10764-10769 (2003).
22. C. Galés, J. J. Van Durm, S. Schaak, S. Pontier, Y. Percherancier, M. Audet, H. Paris, M. Bouvier, Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes. Nat. Struct. Mol. Biol. 13, 778-786 (2006).
23. C. J. Thomas, K. Briknarová, J. K. Hilmer, N. Movahed, B. Bothner, J. P. Sumida, G. G. Tall, S. R. Sprang, The nucleotide exchange factor Ric-8A is a chaperone for the conformationally dynamic nucleotide-free state of Gαi1. PLoS ONE 6, e23197 (2011).
24. V. N. Uversky, A. K. Dunker, Understanding protein non-folding. Biochim. Biophys. Acta 1804, 1231-1264 (2010).
25. J. Gsponer, M. E. Futschik, S. A. Teichmann, M. M. Babu, Tight regulation of unstructured proteins: From transcript synthesis to protein degradation. Science 322, 1365-1368 (2008).
26. W. P. Hausdorff, J. A. Pitcher, D. K. Luttrell, M. E. Linder, H. Kurose, S. J. Parsons, M. G. Caron, R. J. Lefkowitz, Tyrosine phosphorylation of G protein α subunits by pp60c-src. Proc. Natl. Acad. Sci. U.S.A. 89, 5720-5724 (1992).
27. M. W. Bell, N. Desai, X. X. Guo, A. J. Ghalayini, Tyrosine phosphorylation of the α subunit of transducin and its association with Src in photoreceptor rod outer segments. J. Neurochem. 75, 2006-2019 (2000).
28. M. Y. Chen, P. N. Devreotes, R. E. Gundersen, Serine 113 is the site of receptor-mediated phosphorylation of the Dictyostelium G protein α-subunit G α 2. J. Biol. Chem. 269, 20925-20930 (1994).
29. M. P. Torres, M. J. Lee, F. Ding, C. Purbeck, B. Kuhlman, N. V. Dokholyan, H. G. Dohlman, G protein mono-ubiquitination by the Rsp5 ubiquitin ligase. J. Biol. Chem. 284, 8940-8950 (2009).
30. S. D. Cappell, R. Baker, D. Skowyra, H. G. Dohlman, Systematic analysis of essential genes reveals important regulators of G protein signaling. Mol. Cell 38, 746-757 (2010).
31. Y. Wang, L. A. Marotti Jr., M. J. Lee, H. G. Dohlman, Differential regulation of G protein α subunit trafficking by mono- and polyubiquitination. J. Biol. Chem. 280, 284-291 (2005).
32. M. P. Torres, S. T. Clement, S. D. Cappell, H. G. Dohlman, Cell cycle-dependent phosphorylation and ubiquitination of a G protein α subunit. J. Biol. Chem. 286, 20208-20216 (2011).
33. L. A. Marotti Jr., R. Newitt, Y. Wang, R. Aebersold, H. G. Dohlman, Direct identification of a G protein ubiquitination site by mass spectrometry. Biochemistry 41, 5067-5074 (2002).
34. o and the structural basis for RGS16-mediated deactivation. Proc. Natl. Acad. Sci. U.S.A. 105, 6243-6248 (2008).
35. M. Soundararajan, F. S. Willard, A. J. Kimple, A. P. Turnbull, L. J. Ball, G. A. Schoch, C. Gileadi, O. Y. Fedorov, E. F. Dowler, V. A. Higman, S. Q. Hutsell, M. Sundström, D. A. Doyle, D. P. Siderovski, Structural diversity in the RGS domain and its interaction with heterotrimeric G protein α-subunits. Proc. Natl. Acad. Sci. U.S.A. 105, 6457-6462 (2008).
36. N. P. Skiba, C. S. Yang, T. Huang, H. Bae, H. E. Hamm, The α-helical domain of Gαt determines specific interaction with regulator of G protein signaling 9. J. Biol. Chem. 274, 8770-8778 (1999).
37. C. V. Carman, J. L. Parent, P. W. Day, A. N. Pronin, P. M. Sternweis, P. B. Wedegaertner, A. G. Gilman, J. L. Benovic, T. Kozasa, Selective regulation of Gα(q/11) by an RGS domain in the G protein-coupled receptor kinase, GRK2. J. Biol. Chem. 274, 34483-34492 (1999).
38. P. W. Day, C. V. Carman, R. Sterne-Marr, J. L. Benovic, P. B. Wedegaertner, Differential interaction of GRK2 with members of the Gαq family. Biochemistry 42, 9176-9184 (2003).
39. P. W. Day, J. J. Tesmer, R. Sterne-Marr, L. C. Freeman, J. L. Benovic, P. B. Wedegaertner, Characterization of the GRK2 binding site of Gαq. J. Biol. Chem. 279, 53643-53652 (2004).
40. R. J. Kimple, M. E. Kimple, L. Betts, J. Sondek, D. P. Siderovski, Structural determinants for GoLoco-induced inhibition of nucleotide release by Gαsubunits. Nature 416, 878-881 (2002).
41. N. Hajicek, M. Kukimoto-Niino, C. Mishima-Tsumagari, C. R. Chow, M. Shirouzu, T. Terada, M. Patel, S. Yokoyama, T. Kozasa, Identification of critical residues in Gα13 for stimulation of p115RhoGEF activity and the structure of the Gα13-p115RhoGEF regulator of G protein signaling homology (RH) domain complex. J. Biol. Chem. 286, 20625-20636 (2011).
42. Z. Chen, W. D. Singer, P. C. Sternweis, S. R. Sprang, Structure of the p115RhoGEF rgRGS domain-Gα13/i1 chimera complex suggests convergent evolution of a GTPase activator. Nat. Struct. Mol. Biol. 12, 191-197 (2005).
43. 13. Science 280, 2109-2111 (1998).
44. M. J. Hart, X. Jiang, T. Kozasa, W. Roscoe, W. D. Singer, A. G. Gilman, P. C. Sternweis, G. Bollag, Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Gα13. Science 280, 2112-2114 (1998).
45. M. B. Mixon, E. Lee, D. E. Coleman, A. M. Berghuis, A. G. Gilman, S. R. Sprang, Tertiary and quaternary structural changes in Giα1 induced by GTP hydrolysis. Science 270, 954-960 (1995) [see comments].
46. J. C. Jones, A. M. Jones, B. R. Temple, H. G. Dohlman, Differences in intradomain and interdomain motion confer distinct activation properties to structurally similar Gα proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 7275-7279 (2012).