Probing Gα i1 protein activation at single-amino acid resolution

Nature Structural and Molecular Biology

Volumn 22, Issue 9, 2015, Pages 686-694

  Sun, Dawei ^a,b   Flock, Tilman ^c   Deupi, Xavier ^a   Maeda, Shoji ^a,e   Matkovic, Milos ^a,b   Mendieta, Sandro ^a   Mayer, Daniel ^a,b   Dawson, Roger J P ^d   Schertler, Gebhard F X ^a,b   Babu, M Madan ^c   Veprintsev, Dmitry B ^a,b  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANOSINE TRIPHOSPHATASE; RHODOPSIN; DNA; PROTEIN BINDING;

ALPHA HELIX; ARTICLE; CONFORMATIONAL TRANSITION; MOLECULAR PROBE; MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RECEPTOR BINDING; SIGNAL TRANSDUCTION; THERMOSTABILITY; CHEMICAL STRUCTURE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; HUMAN; METABOLISM; PROTEIN CONFORMATION;

AMINO ACIDS; DNA; DNA MUTATIONAL ANALYSIS; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; RHODOPSIN;

EID: 84941026002     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3070     Document Type: Article

References (46)

1. Gilman, A.G. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649 (1987).
2. Wall, M.A. et al. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83, 1047-1058 (1995).
3. Sprang, S.R. G proteins, effectors and GAPs: structure and mechanism. Curr. Opin. Struct. Biol. 7, 849-856 (1997).
4. Oldham, W.M., Van Eps, N., Preininger, A.M., Hubbell, W.L. & Hamm, H.E. Mechanism of the receptor-catalyzed activation of heterotrimeric G proteins. Nat Struct. Mol. Biol. 13, 772-777 (2006).
5. Oldham, W.M. & Hamm, H.E. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9, 60-71 (2008).
6. Marin, E.P., Krishna, A.G. & Sakmar, T.P. Rapid activation of transducin by mutations distant from the nucleotide-binding site: evidence for a mechanistic model of receptor-catalyzed nucleotide exchange by G proteins. J. Biol. Chem. 276, 27400-27405 (2001).
7. Marin, E.P., Krishna, A.G. & Sakmar, T.P. Disruption of the alpha5 helix of transducin impairs rhodopsin-catalyzed nucleotide exchange. Biochemistry 41, 6988-6994 (2002).
8. Garcia, P.D., Onrust, R., Bell, S.M., Sakmar, T.P. & Bourne, H.R. Transducin-alpha C-terminal mutations prevent activation by rhodopsin: a new assay using recombinant proteins expressed in cultured cells. EMBO J. 14, 4460-4469 (1995).
9. Onrust, R. et al. Receptor and betagamma binding sites in the alpha subunit of the retinal G protein transducin. Science 275, 381-384 (1997).
10. Coleman, D.E. et al. Structures of active conformations of Gi alpha 1 and the mechanism of GTP hydrolysis. Science 265, 1405-1412 (1994).
11. Mixon, M.B. et al. Tertiary and quaternary structural changes in Gi alpha 1 induced by GTP hydrolysis. Science 270, 954-960 (1995).
12. Chen, Z., Singer, W.D., Danesh, S.M., Sternweis, P.C. & Sprang, S.R. Recognition of the activated states of Galpha13 by the rgRGS domain of PDZRhoGEF. Structure 16, 1532-1543 (2008).
13. Noel, J.P., Hamm, H.E. & Sigler, P.B. The 2.2 A crystal structure of transducin-a complexed with GTPyS. Nature 366, 654-663 (1993).
14. Lambright, D.G., Noel, J.P., Hamm, H.E. & Sigler, P.B. Structural determinants for activation of the a-subunit of a heterotrimeric G protein. Nature 369, 621-628 (1994).
15. Lambright, D.G. et al. The 2.0 A crystal structure of a heterotrimeric G protein. Nature 379, 311-319 (1996).
16. Rasmussen, S.G. et al. Crystal structure of the p2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011).
17. Van Eps, N. et al. Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc. Natl. Acad. Sci. USA 108, 9420-9424 (2011).
18. Westfeld, G.H. et al. Structural fexibility of the G alpha s alpha-helical domain in the beta2-adrenoceptor Gs complex. Proc. Natl. Acad. Sci. USA 108, 16086-16091 (2011).
19. Galés, C. et al. Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes. Nat. Struct. Mol. Biol. 13, 778-786 (2006).
20. Chung, K.Y. et al. Conformational changes in the G protein Gs induced by the p2 adrenergic receptor. Nature 477, 611-615 (2011).
21. Alexander, N.S. et al. Energetic analysis of the rhodopsin-G-protein complex links the a5 helix to GDP release. Nat. Struct. Mol. Biol. 21, 56-63 (2014).
22. Kaya, A.I. et al. A conserved phenylalanine as a relay between the alpha5 helix and the GDP binding region of heterotrimeric Gi protein alpha subunit. J. Biol. Chem. 289, 24475-24487 (2014).
23. Maeda, S. et al. Crystallization scale preparation of a stable GPCR signaling complex between constitutively active rhodopsin and G-protein. PLoS ONE 9, e98714 (2014).
24. Matouschek, A., Kellis, J.T. Jr., Serrano, L. & Fersht, A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 340, 122-126 (1989).
25. Flock, T. et al. Universal allosteric mechanism for Gα activation by GPCRs. Nature doi:10.1038/nature14663 (6 July 2015).
26. Hamm, H.E. et al. Site of G protein binding to rhodopsin mapped with synthetic peptides from the alpha subunit. Science 241, 832-835 (1988).
27. Osawa, S. & Weiss, E.R. The effect of carboxyl-terminal mutagenesis of Gt alpha on rhodopsin and guanine nucleotide binding. J. Biol. Chem. 270, 31052-31058 (1995).
28. Standfuss, J. et al. The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660 (2011).
29. Dratz, E.A. et al. NMR structure of a receptor-bound G-protein peptide. Nature 363, 276-281 (1993).
30. Van Eps, N. et al. Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc. Natl. Acad. Sci. USA 108, 9420-9424 (2011).
31. Liu, W. & Northup, J.K. The helical domain of a G protein alpha subunit is a regulator of its effector. Proc. Natl. Acad. Sci. USA 95, 12878-12883 (1998).
32. Jones, J.C. et al. The crystal structure of a self-activating G protein alpha subunit reveals its distinct mechanism of signal initiation. Sci. Signal. 4, ra8 (2011).
33. Urano, D., Chen, J.G., Botella, J.R. & Jones, A.M. Heterotrimeric G protein signalling in the plant kingdom. Open Biol. 3, 120186 (2013).
34. Raw, A.S., Coleman, D.E., Gilman, A.G. & Sprang, S.R. Structural and biochemical characterization of the GTPgammaS-, GDP.Pi-, and GDP-bound forms of a GTPase-defcient Gly42 → Val mutant of Gialpha1. Biochemistry 36, 15660-15669 (1997).
35. Dror, R.O. et al. Signal transduction: structural basis for nucleotide exchange in heterotrimeric G proteins. Science 348, 1361-1365 (2015).
36. Sun, D. et al. AAscan, PCRdesign and MutantChecker: a suite of programs for primer design and sequence analysis for high-throughput scanning mutagenesis. PLoS ONE 8, e78878 (2013).
37. Iwata, S. Methods and Results in Crystallization of Membrane Proteins (International University Line, La Jolla, California, USA, 2003).
38. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
39. Pettersen, E.F. et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
40. Webb, B. & Sali, A. Comparative protein structure modeling using MODELLER. Curr. Protoc. Bioinformatics 47, 5.6 (2014).
41. Liu, W. et al. Structural basis for allosteric regulation of GPCRs by sodium ions. Science 337, 232-236 (2012).
42. Mahalingam, M., Martinez-Mayorga, K., Brown, M.F. & Vogel, R. Two protonation switches control rhodopsin activation in membranes. Proc. Natl. Acad. Sci. USA 105, 17795-17800 (2008).
43. Tajkhorshid, E., Baudry, J., Schulten, K. & Suhai, S. Molecular dynamics study of the nature and origin of retinal's twisted structure in bacteriorhodopsin. Biophys. J. 78, 683-693 (2000).
44. Nina, M., Roux, B. & Smith, J.C. Functional interactions in bacteriorhodopsin: a theoretical analysis of retinal hydrogen bonding with water. Biophys. J. 68, 25-39 (1995).
45. Phillips, J.C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
46. MacKerell, A.D. et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (1998).