eIF2 independently binds two distinct eIF2b subcomplexes that catalyze and regulate guanine-nucleotide exchange

Genes and Development

Volumn 12, Issue 4, 1998, Pages 514-526

  Pavitt, Graham D ^a,d   Ramaiah, Kolluru V A ^a,c   Kimball, Scot R ^b   Hinnebusch, Alan G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF HYDERABAD   (India)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

eIF2; GEF; Phosphorylation; Translation initiation

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; INITIATION FACTOR 2; MUTANT PROTEIN; PROTEIN KINASE;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME SUBUNIT; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSLATION INITIATION; YEAST;

EID: 0032519585     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.4.514     Document Type: Article

References (48)

1. Boeke, J.D., F. LaCroute, and G.R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-Fluoro-orotic acid resistance. Mol. Gen. Genet. 197: 345-346.
2. Boguski, M.S. and F. McCormick. 1993. Proteins regulating Ras and its relatives. Nature 366: 643-654.
3. Bourne, H.R., D.A. Sanders, and F. McCormick. 1991. The GT-Pase superfamily: Conserved structure and molecular mechanism. Nature 349: 117-127.
4. Bushman, J.L., A.I. Asuru, R.L. Matts, and A.G. Hinnebusch. 1993a. Evidence that GCD6 and GCD7, translational regulators of GCN4, are subunits of the guanine nucleotide exchange factor for eIF-2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 1920-1932.
5. Bushman, J.L., M. Foiani, A.M. Cigan, C.J. Paddon, and A.G. Hinnebusch. 1993b. Guanine nucleotide exchange factor for eIF-2 in yeast: Genetic and biochemical analysis of interactions between essential subunits GCD2, GCD6 and GCD7 and regulatory subunit GCN3. Mol. Cell. Biol. 13: 4618-4631.
6. Christianson, T.W., R.S. Sikorski, M. Dante, J.H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
7. Cigan, A.M., E.K. Pabich, L. Feng, and T.F. Donahue. 1989. Yeast translation initiation suppressor sui2 encodes the alpha subunit of eukaryotic initiation factor 2 and shares identity with the human alpha subunit. Proc. Natl. Acad. Sci. 86: 2784-2788.
8. Cigan, A.M., M. Foiani, E.M. Hannig, and A.G. Hinnebusch. 1991. Complex formation by positive and negative translational regulators of GCN4. Mol. Cell. Biol. 11: 3217-3228.
9. Cigan, A.M., J.L. Bushman, T.R. Boal, and A.G. Hinnebusch. 1993. A protein complex of translational regulators of GCN4 is the guanine nucleotide exchange factor for eIF-2 in yeast. Proc. Natl. Acad. Sci. 90: 5350-5354.
10. Clemens, M.J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control. In Translational control (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 139-172. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. De Benedetti, A. and C. Baglioni. 1983. Phosphorylation of initiation factor eIF2α, binding of mRNA to 48S complexes, and its reutilization in initiation of protein synthesis. J. Biol. Chem. 258: 14556-14562.
12. Dever, T.E. 1997. Using GCN4 as a reporter of eIF2α phosphorylation and translational regulation in yeast. Methods 11: 403-417.
13. Dever, T.E., L. Feng, R.C. Wek, A.M. Cigan, T.D. Donahue, and A.G. Hinnebusch. 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585-596.
14. Dever, T.E., J.J. Chen, G.N. Barber, A.M. Cigan, L. Feng, T.F. Donahue, I.M. London, M.G. Katze, and A.G. Hinnebusch. 1993. Mammalian eukaryotic initiation factor 2α kinases functionally substitute for GCN2 in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. 90: 4616-4620.
15. Met ternary complexes. Mol. Cell. Biol. 15: 6351-6363.
16. Donahue, T.F., A.M. Cigan, E.K. Pabich, and B. Castilho-Valavicius. 1988. Mutations at a Zn(11) finger motif in the yeast elF-2β gene alter ribosomal start-site selection during the scanning process. Cell 54: 621-632.
17. Dorns, D.R., F.L. Erickson, and E.M. Hannig. 1995. Mutations in GCD11, the structural gene for eIF-2γ in yeast, alter translational regulation of GCN4 and the selection of the start site for protein synthesis. EMBO J. 14: 2239-2239.
18. Erickson, F.L. and E.M. Hannig. 1996. Ligand interactions with eukaryotic translation initiation factor 2: Role of the γ-subunit. EMBO J. 15: 6311-6320.
19. Fabian, J.R., S.R. Kimball, N.K. Heinzinger, and L.S. Jefferson. 1997, Subunit assembly and guanine nucleotide exchange activity of eukaryotic initiation factor-2B expressed in Sf9 cells. J. Biol. Chem. 272: 12359-12365.
20. Foiani, M., A.M. Cigan, C.J. Paddon, S. Harashima, and A.G. Hinnebusch. 1991. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 3203-3216.
21. Goss, D.J., L.J. Parkhurst, H.B. Mehta, C.L. Woodley, and A.J. Wahba. 1984. Studies on the role of eukaryotic nucleotide exchange factor in polypeptide chain initiation. J. Biol. Chem. 259: 7374-7377.
22. Gross, M., M. Wing, C. Rundquist, and M.S. Rubino. 1987. Evidence that phosphorylation of the eIF-2α prevents the eIF-2B-mediated dissociation of eIF-2 · GDP from the 60S subunit of complete initiation complexes. J. Biol. Chem. 262: 6899-6907.
23. Hannig, E.M., A.M. Cigan, B.A. Freeman, and T.G. Kinzy. 1993. GCD11, a negative regulator of GCN4 expression, encodes the gamma subunit of eIF-2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 506-520.
24. Hannig, E.M. and A.G. Hinnebusch. 1988. Molecular analysis of GCN3, a translational activator of GCN4: Evidence for post-translational control of GCN3 regulatory function. Mol Cell. Biol. 8: 4808-4820.
25. Harrison, C.J., M. Hayer-Hartl, M. Di Liberto, F.U. Hartl, and J. Kuriyan. 1997. Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276: 431-435.
26. Hinnebusch, A.G. 1994. Translational control of GCN4: An in vivo barometer of initiation factor activity. Trends Biochem. Sci. 19: 409-414.
27. _. 1996. Translational control of GCN4: Gene-specific regulation by phosphorylation of eIF2. In Translational control, (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 199-244. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Hinnebusch, A.G. and G.R. Fink. 1983. Positive regulation in the general amino acid control of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 80: 5374-5378.
29. Ito, H., Y. Fukada, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153: 163-168.
30. Jackson, R.J. and T. Hunt. 1985. A novel approach to the isolation of rabbit reticulocyte heam-controlled eIF-2α protein kinase. Biochem. Biophys. Acta. 826: 224-228.
31. Jones, E.W. 1991. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194: 428-453.
32. Merrick W.C. 1992. Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56: 291-315.
33. Moehle, C.M. and A.G. Hinnebusch. 1991. Association of RAP1 binding sites with stringent control of ribosomal protein gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 2723-2735.
34. Paddon, C.J. and A.G. Hinnebusch. 1989. gcd12 mutations are gcn3-dependent alleles of GCD2, a negative regulator of GCN4 in the general amino acid control of Saccharomcyes cerevisiae. Genetics 122: 543-550.
35. Paddon, C.J., E.M. Hannig, and A.G. Hinnebusch. 1989. Amino acid sequence similarity between GCN3 and GCD2, positive and negative translational regulators of GCN4: Evidence for antagonism by competition. Genetics 122: 551-559.
36. Pavitt, G.D., W. Yang, and A.G. Hinnebusch. 1997. Homologous segments in three subunits of the guanine nucleotide exchange factor eIF2B mediate translational regulation by phosphorylation of eIF2. Mol. Cell. Biol. 17: 1298-1313.
37. Phizicky, E.M. and S. Fields. 1995. Protein-protein interactions. Methods for detection and analysis. Microbiol. Rev. 59: 94-123.
38. Price, N.T., S.R. Kimball, L.S. Jefferson, and C.G. Proud. 1996a. Cloning of cDNA for the γ-subunit of mammalian translation initiation factor 2B, the guanine nucleotide-exchange factor for eukaryotic initiation factor 2. Biochem. J. 318: 631-636.
39. Price, N.T., H. Mellor, B.L. Craddock, K.M. Flowers, S.R. Kimball, T. Wilmer, L.S. Jefferson, and C.G. Proud. 1996b. eIF2B, the guanine nucleotide-exchange factor for eukaryotic initiation factor 2. Biochem. J. 318: 637-643.
40. Ramaiah, K.V.A., R.S. Dhindsa, J.-J. Chen, I.M. London, and D. Levin. 1992. Recycling and phosphorylation of eukaryotic initiation factor 2 on 60S subunits of 80S initiation complexes and polysomes. Proc. Natl. Acad. Sci. 89: 12063-12067.
41. Rowlands, A.G., R. Panniers, and E.C. Henshaw. 1988. The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J. Biol. Chem. 263: 5526-5533.
42. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Sherman, F., G.R. Fink, and C.W. Lawrence. 1974. Methods of yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
44. Thomas, N.S.B., R.L. Matts, D.H. Levin, and I.M. London. 1985. The 60S ribosomal subunit as a carrier of eukaryotic initiation factor 2 and the site of reversing factor activity during protein synthesis. J. Biol. Chem. 260: 9860-9866.
45. Trachsel, H. 1996. Binding of initiator methionyl-tRNA to ribosomes. In Translational control, (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 113-138. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Vazquez de Aldana, C.R. and A.G. Hinnebusch. 1994. Mutations in the GCD7 subunit of yeast guanine nucleotide exchange factor eIF-2B overcome the inhibitory effects of phosphorylated eIF-2 on translation initiation. Mol. Cell. Biol. 14: 3208-3222.
47. Wek, R.C., M. Ramirez, B.M. Jackson, and A.G. Hinnebusch. 1990. Identification of positive-acting domains in GCN2 protein kinase required for translational activation of GCN4 expression. Mol. Cell. Biol. 10: 2820-2831.
48. Yang, W. and A.G. Hinnebusch. 1996. Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2. Mol. Cell. Biol. 16: 6603-6616.