Molecular basis of a novel oncogenic mutation in GNAO1

Oncogene

Volumn 30, Issue 23, 2011, Pages 2691-2696

  Garcia Marcos, M ^a   Ghosh, P ^b   Farquhar, M G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

GAIP RGS19; heterotrimeric G protein; neoplasia; oncoprotein; somatic mutation; STAT3

Indexed keywords

GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NUCLEOTIDE; STAT3 PROTEIN;

ARTICLE; BINDING SITE; CELL TRANSFORMATION; ENZYME ACTIVITY; GENE ACTIVATION; GENE FUNCTION; GENE MUTATION; GNAO 1 R243H GENE; ONCOGENE; ONCOGENE SRC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARGININE; BINDING SITES; BIOCATALYSIS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTPASE-ACTIVATING PROTEINS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HISTIDINE; HUMANS; MICE; MODELS, MOLECULAR; MUTATION; NIH 3T3 CELLS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS PP60(C-SRC); SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 79958287784     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.645     Document Type: Article

References (41)

1. Barren B, Natochin M, Artemyev NO. (2006). Mutation R238E in transducin-alpha yields a GTPase and effector-deficient, but not dominant-negative, G-protein alpha-subunit. Mol Vis 12: 492-498.
2. Berman DM, Wilkie TM, Gilman AG. (1996). GAIP and RGS4 are GTPase-activating proteins for the Gi subfamily of G protein alpha subunits. Cell 86: 445-452. (Pubitemid 26272084)
3. Bourne HR. (1997). G proteins. The arginine finger strikes again. Nature 389: 673-674. (Pubitemid 27458937)
4. Casey PJ, Fong HK, Simon MI, Gilman AG. (1990). Gz, a guanine nucleotide-binding protein with unique biochemical properties. J Biol Chem 265: 2383-2390.
5. Coleman DE, Berghuis AM, Lee E, Linder ME, Gilman AG, Sprang SR. (1994). Structures of active conformations of Gi alpha 1 and the mechanism of GTP hydrolysis. Science 265: 1405-1412.
6. De Vries L, Mousli M, Wurmser A, Farquhar MG. (1995). GAIP, a protein that specifically interacts with the trimeric G protein G alpha i3, is a member of a protein family with a highly conserved core domain. Proc Natl Acad Sci USA 92: 11916-11920.
7. Doi M, Iwasaki K. (2002). Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33: 249-259. (Pubitemid 34127757)
8. Downward J. (2003). Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22. (Pubitemid 37328883)
9. Farfel Z, Bourne HR, Iiri T. (1999). The expanding spectrum of G protein diseases. N Engl J Med 340: 1012-1020. (Pubitemid 29157634)
10. Forbes SA, Bhamra G, Bamford S, Dawson E, Kok C, Clements J et al. (2008). The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr Protoc Hum Genet Chapter 10: Unit 10.11.
11. Garcia-Marcos M, Ghosh P, Farquhar MG. (2009). GIV is a nonreceptor GEF for G alpha i with a unique motif that regulates Akt signaling. Proc Natl Acad Sci USA 106: 3178-3183.
12. Garcia-Marcos M, Ghosh P, Ear J, Farquhar MG. (2010). A structural determinant that renders G alpha(i) sensitive to activation by GIV/girdin is required to promote cell migration. J Biol Chem 285: 12765-12777.
13. Ghosh P, Beas AO, Bornheimer SJ, Garcia-Marcos M, Forry EP, Johannson C et al. (2010). A G{alpha}i-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol Biol Cell 21: 2338-2354.
14. Ghosh P, Garcia-Marcos M, Bornheimer SJ, Farquhar MG. (2008). Activation of Galphai3 triggers cell migration via regulation of GIV. J Cell Biol 182: 381-393.
15. Grishina G, Berlot CH. (1998). Mutations at the domain interface of GSalpha impair receptor-mediated activation by altering receptor and guanine nucleotide binding. J Biol Chem 273: 15053-15060. (Pubitemid 28272800)
16. Higashijima T, Ferguson KM, Smigel MD, Gilman AG. (1987). The effect of GTP and Mg2+ on the GTPase activity and the fluorescent properties of Go. J Biol Chem 262: 757-761. (Pubitemid 17005249)
17. Iiri T, Farfel Z, Bourne HR. (1998). G-protein diseases furnish a model for the turn-on switch. Nature 394: 35-38. (Pubitemid 28321792)
18. Johnston CA, Taylor JP, Gao Y, Kimple AJ, Grigston JC, Chen JG et al. (2007). GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proc Natl Acad Sci USA 104: 17317-17322. (Pubitemid 350219840)
19. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM et al. (2010). Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466: 869-873.
20. Kleuss C, Raw AS, Lee E, Sprang SR, Gilman AG. (1994). Mechanism of GTP hydrolysis by G-protein alpha subunits. Proc Natl Acad Sci USA 91: 9828-9831. (Pubitemid 24311901)
21. Kroll SD, Chen J, De Vivo M, Carty DJ, Buku A, Premont RT et al. (1992). The Q205LGo-alpha subunit expressed in NIH-3T3 cells induces transformation. J Biol Chem 267: 23183-23188.
22. Lamba S, Felicioni L, Buttitta F, Bleeker FE, Malatesta S, Corbo V et al. (2009). Mutational profile of GNAQQ209 in human tumors. PLoS One 4: e6833.
23. Landis CA, Masters SB, Spada A, Pace AM, Bourne HR, Vallar L. (1989). GTPase inhibiting mutations activate the alpha chain of Gs and stimulate adenylyl cyclase in human pituitary tumours. Nature 340: 692-696. (Pubitemid 19214389)
24. Linder ME, Ewald DA, Miller RJ, Gilman AG. (1990). Purification and characterization of Go alpha and three types of Gi alpha after expression in Escherichia coli. J Biol Chem 265: 8243-8251.
25. Lyons J, Landis CA, Harsh G, Vallar L, Grunewald K, Feichtinger H et al. (1990). Two G protein oncogenes in human endocrine tumors. Science 249: 655-659. (Pubitemid 20259082)
26. Makita N, Sato J, Rondard P, Fukamachi H, Yuasa Y, Aldred MA et al. (2007). Human G(salpha) mutant causes pseudohypopar-athyroidism type Ia/neonatal diarrhea, a potential cell-specific role of the palmitoylation cycle. Proc Natl Acad Sci USA 104: 17424-17429. (Pubitemid 350219854)
27. Marinissen MJ, Gutkind JS. (2001). G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol Sci 22: 368-376. (Pubitemid 32592476)
28. Mukhopadhyay S, Ross EM. (2002). Quench-flow kinetic measurement of individual reactions of G-protein-catalyzed GTPase cycle. Methods Enzymol 344: 350-369. (Pubitemid 34193362)
29. Pereira R, Cerione RA. (2005). A switch 3 point mutation in the alpha subunit of transducin yields a unique dominant-negative inhibitor. J Biol Chem 280: 35696-35703. (Pubitemid 41532762)
30. Radhika V, Dhanasekaran N. (2001). Transforming G proteins. Oncogene 20: 1607-1614. (Pubitemid 32336849)
31. Ram PT, Horvath CM, Iyengar R. (2000). Stat3-mediated transformation of NIH-3T3 cells by the constitutively active Q205L Galphao protein. Science 287: 142-144. (Pubitemid 30033239)
32. Sprang SR. (1997). G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66: 639-678. (Pubitemid 27274670)
33. Sternweis PC, Robishaw JD. (1984). Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem 259: 13806-13813. (Pubitemid 15224957)
34. Van Raamsdonk CD, Bezrookove V, Green G, Bauer J, Gaugler L, O'Brien JM et al. (2009). Frequent somatic mutations of GNAQ in uveal melanoma and blue naevi. Nature 457: 599-602.
35. Vara Prasad MV, Shore SK, Dhanasekaran N. (1994). Activated mutant of G alpha 13 induces Egr-1, c-fos, and transformation in NIH 3T3 cells. Oncogene 9: 2425-2429.
36. Voyno-Yasenetskaya TA, Pace AM, Bourne HR. (1994). Mutant alpha subunits of G12 and G13 proteins induce neoplastic transformation of Rat-1 fibroblasts. Oncogene 9: 2559-2565. (Pubitemid 24254031)
37. Warner DR, Weinstein LS. (1999). A mutation in the heterotrimeric stimulatory guanine nucleotide binding protein alpha-subunit with impaired receptor-mediated activation because of elevated GTPase activity. Proc Natl Acad Sci USA 96: 4268-4272. (Pubitemid 29190325)
38. Wong YH, Chan JS, Yung LY, Bourne HR. (1995). Mutant alpha subunit of Gz transforms Swiss 3T3 cells. Oncogene 10: 1927-1933.
39. Xu N, Bradley L, Ambdukar I, Gutkind JS. (1993). A mutant alpha subunit of G12 potentiates the eicosanoid pathway and is highly oncogenic in NIH 3T3 cells. Proc Natl Acad Sci USA 90: 6741-6745. (Pubitemid 23207289)
40. Xu N, Voyno-Yasenetskaya T, Gutkind JS. (1994). Potent transforming activity of the G13 alpha subunit defines a novel family of oncogenes. Biochem Biophys Res Commun 201: 603-609.
41. Zurita AR, Birnbaumer L. (2008). The same mutation in Gsalpha and transducin alpha reveals behavioral differences between these highly homologous G protein alpha-subunits. Proc Natl Acad Sci USA 105: 2363-2368. (Pubitemid 351520519)