The nucleotide exchange factor Ric-8a is a chaperone for the conformationally dynamic nucleotide-free state of gαi1

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Thomas, Celestine J ^a   Briknarová, Klára ^a   Hilmer, Jonathan K ^b   Movahed, Navid ^b   Bothner, Brian ^b   Sumida, John P ^c   Tall, Gregory G ^d   Sprang, Stephen R ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; MONOMER; RIC 8A PROTEIN; UNCLASSIFIED DRUG; GNAI1 PROTEIN, RAT; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; NUCLEAR PROTEIN; NUCLEOTIDE; PROTON; RIC8A PROTEIN, RAT; TRYPSIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; DIFFERENTIAL SCANNING CALORIMETRY; MASS SPECTROMETRY; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN UNFOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; ANIMAL; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN DENATURATION; PROTEIN SECONDARY STRUCTURE; THERMODYNAMICS;

MAMMALIA;

ANIMALS; DEUTERIUM EXCHANGE MEASUREMENT; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CHAPERONES; NUCLEAR PROTEINS; NUCLEOTIDES; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTONS; RATS; THERMODYNAMICS; TRYPSIN;

EID: 80051655842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023197     Document Type: Article

References (51)

1. Sprang SR, (1997) G protein mechanisms: Insights from structural analysis. Annu Rev Biochem 66: 639-678.
2. Cherfils J, Chardin P, (1999) GEFs: structural basis for their activation of small GTP-binding proteins. Trends Biochem Sci 24: 306-311.
3. Pierce KL, Premont RT, Lefkowitz RJ, (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3: 639-650.
4. Tall GG, Krumins AM, Gilman AG, (2003) Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J Biol Chem 278: 8356-8362.
5. Afshar K, Willard FS, Colombo K, Johnston CA, McCudden CR, et al. (2004) RIC-8 Is Required for GPR-1/2-Dependent Galpha Function during Asymmetric Division of C. elegans Embryos. Cell 119: 219-230.
6. Miller KG, Emerson MD, McManus JR, Rand JB, (2000) RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system. Neuron 27: 289-299.
7. David NB, Martin CA, Segalen M, Rosenfeld F, Schweisguth F, et al. (2005) Drosophila Ric-8 regulates Galphai cortical localization to promote Galphai-dependent planar orientation of the mitotic spindle during asymmetric cell division. Nat Cell Biol 7: 1083-1090.
8. Woodard GE, Huang NN, Cho H, Miki T, Tall GG, et al. Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol Cell Biol 30: 3519-3530.
9. Figueroa M, Hinrichs MV, Bunster M, Babbitt P, Martinez-Oyanedel J, et al. (2009) Biophysical studies support a predicted superhelical structure with armadillo repeats for Ric-8. Protein Sci 18: 1139-1145.
10. Oldham WM, Hamm HE, (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol 9: 60-71.
11. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, et al. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455: 497-502.
12. Thomas CJ, Tall GG, Adhikari A, Sprang SR, (2008) Ric-8A catalyzes guanine nucleotide exchange on G alphai1 bound to the GPR/GoLoco exchange inhibitor AGS3. J Biol Chem 283: 23150-23160.
13. Zelent B, Veklich Y, Murray J, Parkes JH, Gibson S, et al. (2001) Rapid irreversible G protein alpha subunit misfolding due to intramolecular kinetic bottleneck that precedes Mg2+ "lock" after GTP/GDP exchange. Biochemistry 40: 9647-9656.
14. Coleman DE, Berghuis AM, Lee E, Linder ME, Gilman AG, et al. (1994) Structures of active conformations of Gi alpha 1 and the mechanism of GTP hydrolysis. Science 265: 1405-1412.
15. Pervushin K, Riek R, Wider G, Wüthrich K, (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proceedings of the National Academy of Sciences of the United States of America 94: 12366-12371.
16. Abdulaev NG, Zhang C, Dinh A, Ngo T, Bryan PN, et al. (2005) Bacterial expression and one-step purification of an isotope-labeled heterotrimeric G-protein alpha-subunit. J Biomol NMR 32: 31-40.
17. Hoofnagle AN, Resing KA, Ahn NG, (2003) Protein analysis by hydrogen exchange mass spectrometry. Annu Rev Biophys Biomol Struct 32: 1-25.
18. Englander SW, Downer NW, Teitelbaum H, (1972) Hydrogen exchange. Annual Review of Biochemistry 41: 903-924.
19. Privalov PL, Potekhin SA, (1986) Scanning microcalorimetry in studying temperature-induced changes in proteins. Methods in Enzymology 131: 4-51.
20. Privalov PL, Khechinashvili NN, (1974) A thermodynamic approach to the problem of stabilization of globular protein structure: A calorimetric study. J Mol Biol 86: 665-684.
21. Privalov PL, Gill SJ, (1988) Stability of protein structure and hydrophobic interaction. Advances in Protein Chemistry 39: 191-234.
22. Prabhu NV, Sharp KA, (2005) Heat capacity in proteins. Annu Rev Phys Chem 56: 521-548.
23. Griko YV, Privalov PL, (1994) Thermodynamic puzzle of apomyoglobin unfolding. J Mol Biol 235: 1318-1325.
24. Anderson LL, Marshall GR, Baranski TJ, (2005) Expressed protein ligation to study protein interactions: semi-synthesis of the G-protein alpha subunit. Protein Pept Lett 12: 783-787.
25. Vellano CP, Shu FJ, Ramineni S, Yates CK, Tall GG, et al. (2011) Activation of the regulator of G protein signaling 14-Galphai1-GDP signaling complex is regulated by resistance to inhibitors of cholinesterase-8A. Biochemistry 50: 752-762.
26. Horwich AL, Apetri AC, Fenton WA, (2009) The GroEL/GroES cis cavity as a passive anti-aggregation device. FEBS Lett 583: 2654-2662.
27. Sauer RT, Bolon DN, Burton BM, Burton RE, Flynn JM, et al. (2004) Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119: 9-18.
28. Oldham WM, Van Eps N, Preininger AM, Hubbell WL, Hamm HE, (2007) Mapping allosteric connections from the receptor to the nucleotide-binding pocket of heterotrimeric G proteins. Proc Natl Acad Sci U S A 104: 7927-7932.
29. Kapoor N, Menon ST, Chauhan R, Sachdev P, Sakmar TP, (2009) Structural evidence for a sequential release mechanism for activation of heterotrimeric G proteins. J Mol Biol 393: 882-897.
30. Peterson YK, Bernard ML, Ma H, Hazard S 3rd, Graber SG, et al. (2000) Stabilization of the GDP-bound conformation of Gialpha by a peptide derived from the G-protein regulatory motif of AGS3. J Biol Chem 275: 33193-33196.
31. Siderovski DP, Diverse-Pierluissi M, De Vries L, (1999) The GoLoco motif: a Galphai/o binding motif and potential guanine- nucleotide exchange factor. Trends Biochem Sci 24: 340-341.
32. Kimple RJ, Kimple ME, Betts L, Sondek J, Siderovski DP, (2002) Structural determinants for GoLoco-induced inhibition of nucleotide release by Galpha subunits. Nature 416: 878-881.
33. Oldham WM, Van Eps N, Preininger AM, Hubbell WL, Hamm HE, (2006) Mechanism of the receptor-catalyzed activation of heterotrimeric G proteins. Nat Struct Mol Biol 13: 772-777.
34. Lonhienne TG, Forwood JK, Marfori M, Robin G, Kobe B, et al. (2009) Importin-beta is a GDP-to-GTP exchange factor of Ran: implications for the mechanism of nuclear import. J Biol Chem 284: 22549-22558.
35. Forwood JK, Lonhienne TG, Marfori M, Robin G, Meng W, et al. (2008) Kap95p binding induces the switch loops of RanGDP to adopt the GTP-bound conformation: implications for nuclear import complex assembly dynamics. J Mol Biol 383: 772-782.
36. Abdulaev NG, Ngo T, Ramon E, Brabazon DM, Marino JP, et al. (2006) The receptor-bound "empty pocket" state of the heterotrimeric G-protein alpha-subunit is conformationally dynamic. Biochemistry 45: 12986-12997.
37. Abdulaev NG, Ngo T, Zhang C, Dinh A, Brabazon DM, et al. (2005) Heterotrimeric G-protein alpha-subunit adopts a "preactivated" conformation when associated with betagamma-subunits. J Biol Chem 280: 38071-38080.
38. Van Eps N, Preininger AM, Alexander N, Kaya AI, Meier S, et al. (2011) Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc Natl Acad Sci U S A 108: 9420-9424.
39. Anderson LL, Marshall GR, Crocker E, Smith SO, Baranski TJ, (2005) Motion of carboxyl terminus of Galpha is restricted upon G protein activation. A solution NMR study using semisynthetic Galpha subunits. J Biol Chem 280: 31019-31026.
40. Ferguson KM, Higashijima T, (1991) Preparation of guanine nucleotide-free G proteins. Methods Enzymol 195: 188-192.
41. Coleman DE, Lee E, Mixon MB, Linder ME, Berghuis A, et al. (1994) Crystallization and preliminary crystallographic studies of Gia1 and mutants of Gia1 in the GTP and GDP-bound states. J Mol Biol 238: 630-634.
42. Holdeman TC, Gardner KH, (2001) 1H, 13C and 15N chemical shift assignments of the N-terminal PAS domain of mNPAS2. J Biomol NMR 21: 383-384.
43. Sugita S, Hata Y, Südhof TC, (1996) Distinct Ca2+-dependent properties of the first and second C2-domains of synaptotagmin I. J Biol Chem 271: 1262-1265.
44. Vojtek AB, Hollenberg SM, Cooper JA, (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74: 205-214.
45. Fabian JR, Vojtek AB, Cooper JA, Morrison DK, (1994) A single amino acid change in Raf1 inhibits Ras binding and alters Raf-1 function. Proceedings of the National Academy of Sciences USA 91: 5982-5986.
46. Sternweis P, Robishaw J, (1984) Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem 259: 13806-13813.
47. Higashijima T, Ferguson KM, (1991) Tryptophan fluorescence of G proteins: analysis of guanine nucleotide binding and hydrolysis. Methods in Enzymology 195: 321-328.
48. Perez-Iratxeta C, Andrade-Navarro MA, (2008) K2D2: estimation of protein secondary structure from circular dichroism spectra. BMC Structural Biology 8: 25.
49. Weigelt J, (1998) Single Scan, Sensitivity- and Gradient-Enhanced TROSY for Multidimensional NMR Experiments. J Am Chem Soc 120: 10778-10779.
50. Cooper, Nutley, Wadwood, (2000) Differential Scanning Microcalorimetry; In: Harding SE, Chowdry BZ, editors. Oxford, New York Oxford University Press.
51. Cole C, Barber JD, Barton GJ, (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res pp. w197-201.