Molecular chaperoning function of Ric-8 is to fold nascent heterotrimeric G protein α subunits

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 10, 2013, Pages 3794-3799

  Chan, PuiYee ^a   Thomas, Celestine J ^b   Sprang, Stephen R ^b   Tall, Gregory G ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

Chaperone; GEF

Indexed keywords

CHOLINESTERASE INHIBITOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HETERODIMER; RESISTANCE TO INHIBITOR OF CHOLINESTERASE 8 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHOLINESTERASE INHIBITION; GEL FILTRATION; LYSIS; MOLECULAR CHAPERONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; RETICULOCYTE LYSATE; TRYPSINOLYSIS; WHEAT GERM;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; CATTLE; CELL-FREE SYSTEM; CHAPERONIN CONTAINING TCP-1; GTP-BINDING PROTEIN ALPHA SUBUNITS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; RABBITS; RECOMBINANT PROTEINS; RETICULOCYTES; TRITICUM;

EID: 84874604106     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220943110     Document Type: Article

References (42)

1. Dupré DJ, Robitaille M, Rebois RV, Hébert TE (2009) The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu Rev Pharmacol Toxicol 49:31-56.
2. Marrari Y, Crouthamel M, Irannejad R, Wedegaertner PB (2007) Assembly and trafficking of heterotrimeric G proteins. Biochemistry 46(26):7665-7677.
3. Michaelson D, Ahearn I, Bergo M, Young S, Philips M (2002) Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol Biol Cell 13(9):3294-3302.
4. Takida S, Wedegaertner PB (2003) Heterotrimer formation, together with isoprenylation, is required for plasma membrane targeting of Gbetagamma. J Biol Chem 278(19):17284-17290.
5. Lukov GL, et al. (2006) Mechanism of assembly of G protein betagamma subunits by protein kinase CK2-phosphorylated phosducin-like protein and the cytosolic chaperonin complex. J Biol Chem 281(31):22261-22274.
6. Lukov GL, Hu T, McLaughlin JN, Hamm HE, Willardson BM (2005) Phosducin-like protein acts as a molecular chaperone for G protein betagamma dimer assembly. EMBO J 24(11):1965-1975.
7. Wells CA, Dingus J, Hildebrandt JD (2006) Role of the chaperonin CCT/TRiC complex in G protein betagamma-dimer assembly. J Biol Chem 281(29):20221-20232.
8. Willardson BM, Howlett AC (2007) Function of phosducin-like proteins in G protein signaling and chaperone-assisted protein folding. Cell Signal 19(12):2417-2427.
9. Dupré DJ, et al. (2007) Dopamine receptor-interacting protein 78 acts as a molecular chaperone for Ggamma subunits before assembly with Gbeta. J Biol Chem 282(18): 13703-13715.
10. Farr GW, Scharl EC, Schumacher RJ, Sondek S, Horwich AL (1997) Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. Cell 89(6):927-937.
11. Waheed AA, Jones TL (2002) Hsp90 interactions and acylation target the G protein Galpha 12 but not Galpha 13 to lipid rafts. J Biol Chem 277(36):32409-32412.
12. Busconi L, Guan J, Denker BM (2000) Degradation of heterotrimeric Galpha(o) subunits via the proteosome pathway is induced by the hsp90-specific compound geldanamycin. J Biol Chem 275(3):1565-1569.
13. Vaiskunaite R, Kozasa T, Voyno-Yasenetskaya TA (2001) Interaction between the G alpha subunit of heterotrimeric G(12) protein and Hsp90 is required for G alpha(12) signaling. J Biol Chem 276(49):46088-46093.
14. Gabay M, et al. (2011) Ric-8 proteins are molecular chaperones that direct nascent G protein α subunit membrane association. Sci Signal 4(200):ra79.
15. 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(2):289-299.
16. Miller KG, Rand JB (2000) A role for RIC-8 (Synembryn) and GOA-1 (G(o)alpha) in regulating a subset of centrosome movements during early embryogenesis in Caenorhabditis elegans. Genetics 156(4):1649-1660.
17. Reynolds NK, Schade MA, Miller KG (2005) Convergent, RIC-8-dependent Galpha signaling pathways in the Caenorhabditis elegans synaptic signaling network. Genetics 169(2):651-670.
18. Schade MA, Reynolds NK, Dollins CM, Miller KG (2005) Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha(s) pathway and define a third major branch of the synaptic signaling network. Genetics 169(2):631-649.
19. Chan P, Gabay M, Wright FA, Tall GG (2011) Ric-8B is a GTP-dependent G protein alphas guanine nucleotide exchange factor. J Biol Chem 286(22):19932-19942.
20. Tall GG, Krumins AM, Gilman AG (2003) Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J Biol Chem 278(10): 8356-8362.
21. Afshar K, Willard FS, Colombo K, Siderovski DP, Gönczy P (2005) Cortical localization of the Galpha protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division. Development 132(20):4449-4459.
22. David NB, 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(11):1083-1090.
23. Hampoelz B, Hoeller O, Bowman SK, Dunican D, Knoblich JA (2005) Drosophila Ric-8 is essential for plasma-membrane localization of heterotrimeric G proteins. Nat Cell Biol 7(11):1099-1105.
24. Wang H, et al. (2005) Ric-8 controls Drosophila neural progenitor asymmetric division by regulating heterotrimeric G proteins. Nat Cell Biol 7(11):1091-1098.
25. Wright SJ, Inchausti R, Eaton CJ, Krystofova S, Borkovich KA (2011) RIC8 is a guaninenucleotide exchange factor for Galpha subunits that regulates growth and development in Neurospora crassa. Genetics 189(1):165-176.
26. Chan P, et al. (2011) Purification of heterotrimeric G protein alpha subunits by GSTRic- 8 association: Primary characterization of purified G alpha(olf). J Biol Chem 286(4): 2625-2635.
27. Kerr DS, Von Dannecker LE, Davalos M, Michaloski JS, Malnic B (2008) Ric-8B interacts with G alpha olf and G gamma 13 and co-localizes with G alpha olf, G beta 1 and G gamma 13 in the cilia of olfactory sensory neurons. Mol Cell Neurosci 38(3):341-348.
28. Nagai Y, Nishimura A, Tago K, Mizuno N, Itoh H (2010) Ric-8B stabilizes the α subunit of stimulatory G protein by inhibiting its ubiquitination. J Biol Chem 285(15): 11114-11120.
29. Malik S, Ghosh M, Bonacci TM, Tall GG, Smrcka AV (2005) Ric-8 enhances G protein betagamma-dependent signaling in response to betagamma-binding peptides in intact cells. Mol Pharmacol 68(1):129-136.
30. Fung BK, Nash CR (1983) Characterization of transducin from bovine retinal rod outer segments. II. Evidence for distinct binding sites and conformational changes revealed by limited proteolysis with trypsin. J Biol Chem 258(17):10503-10510.
31. Hurley JB, Simon MI, Teplow DB, Robishaw JD, Gilman AG (1984) Homologies between signal transducing G proteins and ras gene products. Science 226(4676): 860-862.
32. Sternweis PC, Robishaw JD (1984) Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem 259(22): 13806-13813.
33. Tall GG, Gilman AG (2004) Purification and Functional Analysis of Ric-8A: A Guanine Nucleotide Exchange Factor for G-Protein α Subunits Methods in Enzymology. ed Siderovski DP (Academic, New York), Vol 390, pp 377-388.
34. Wilkie TM, Kinch L (2005) New roles for Galpha and RGS proteins: Communication continues despite pulling sisters apart. Curr Biol 15(20):R843-R854.
35. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796-815.
36. Neer EJ, Denker BM, Thomas TC, Schmidt CJ (1994) Analysis of G-protein α and βγ subunits by in vitro translation. Methods in Enzymology. ed Ravi I (Academic, New York) Vol 237, pp. 226-239.
37. Kubota S, Kubota H, Nagata K (2006) Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic β-strands. Proc Natl Acad Sci USA 103(22):8360-8365.
38. Lee E, Linder ME, Gilman AG (1994) Expression of G-protein α subunits in Escherichia coli. Methods Enzymol 237:146-164.
39. Hepler JR, et al. (1993) Purification from Sf9 cells and characterization of recombinant Gq α and G11 α. Activation of purified phospholipase C isozymes by G α subunits. J Biol Chem 268(19):14367-14375.
40. Thomas CJ, et al. (2011) The nucleotide exchange factor Ric-8A is a chaperone for the conformationally dynamic nucleotide-free state of Gαi1. PLoS ONE 6(8):e23197.
41. Itzen A, Pylypenko O, Goody RS, Alexandrov K, Rak A (2006) Nucleotide exchange via local protein unfolding-structure of Rab8 in complex with MSS4. EMBO J 25(7): 1445-1455.
42. Kozasa T (1999) Purification of Recombinant G Protein α and βγ Subunits from Sf9 cells, ed Manning DR (CRC Press, Boca Raton, FL).