The β/Gcd7 subunit of eukaryotic translation initiation factor 2B (eIF2B), a guanine nucleotide exchange factor, is crucial for binding eIF2 in vivo

Molecular and Cellular Biology

Volumn 30, Issue 21, 2010, Pages 5218-5233

  Dev, Kamal ^a,b   Qiu, Hongfang ^a   Dong, Jinsheng ^a   Zhang, Fan ^a   Barthlme, Dominik ^a,c   Hinnebusch, Alan G ^a  

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

^b SHOOLINI UNIVERSITY   (India)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; INITIATION FACTOR 2; PROTEIN EIF 2 B; PROTEIN GCD 1; PROTEIN GCD 7; UNCLASSIFIED DRUG; FUNGAL RNA; GCD2 PROTEIN, S CEREVISIAE; GCD7 PROTEIN, S CEREVISIAE; METHIONINE TRANSFER RNA; PRIMER DNA; PROTEIN BINDING; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; FUNGAL GENE; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; BASE SEQUENCE; DNA PRIMERS; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-2B; GENES, FUNGAL; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; RNA, FUNGAL; RNA, TRANSFER, MET; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 77957825617     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00265-10     Document Type: Article

References (50)

1. Alone, P. V., C. Cao, and T. E. Dever. 2008. Translation initiation factor 2gamma mutant alters start codon selection independent of Met-tRNA binding. Mol. Cell. Biol. 28:6877-6888.
2. Anthony, T. G., J. R. Fabian, S. R. Kimball, and L. S. Jefferson. 2000. Identification of domains within the epsilon-subunit of the translation initiation factor eIF2B that are necessary for guanine nucleotide exchange activity and eIF2B holoprotein formation. Biochim. Biophys. Acta 1492:56-62.
3. Asano, K., T. Krishnamoorthy, L. Phan, G. D. Pavitt, and A. G. Hinnebusch. 1999. Conserved bipartite motifs in yeast eIF5 and eIF2Bε, GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J. 18:1673-1688.
4. Boeke, J. D., J. Trueheart, G. Natsoulis, and G. R. Fink. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154:164-175.
5. Bushman, J. L., A. I. Asuru, R. L. Matts, and A. G. Hinnebusch. 1993. 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.
6. Met functions in directing the scanning ribosome to the start site of translation. Science 242:93-97.
7. 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.
8. Craddock, B. L., and C. G. Proud. 1996. The α-subunit of the mammalian guanine nucleotide-exchange factor eIF-2B is essential for catalytic activity in vivo. Biochem. Biophys. Res. Commun. 220:843-847.
9. Cross, F. R. 1997. 'Marker swap' plasmids: convenient tools for budding yeast molecular genetics. Yeast 13:647-653.
10. Dar, A. C., T. E. Dever, and F. Sicheri. 2005. Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 122:887-900.
11. Dev, K., T. J. Santangelo, S. Rothenburg, D. Neculai, M. Dey, F. Sicheri, T. E. Dever, J. N. Reeve, and A. G. Hinnebusch. 2009. Archaeal aIF2B interacts with eukaryotic translation initiation factors eIF2alpha and eIF2Balpha: implications for aIF2B function and eIF2B regulation. J. Mol. Biol. 392:701-722.
12. Met ternary complexes. Mol. Cell. Biol. 15:6351-6363.
13. Dey, M., B. Trieselmann, E. G. Locke, J. Lu, C. Cao, A. C. Dar, T. Krishnamoorthy, J. Dong, F. Sicheri, and T. E. Dever. 2005. PKR and GCN2 kinases and guanine nucleotide exchange factor eukaryotic translation initiation factor 2B (eIF2B) recognize overlapping surfaces on eIF2alpha. Mol. Cell. Biol. 25:3063-3075.
14. Dohmen, R. J., P. Wu, and A. Varshavsky. 1994. Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science 263:1273-1276.
15. 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.
16. Erickson, F. L., J. Nika, S. Rippel, and E. M. Hannig. 2001. Minimum requirements for the function of eukaryotic translation initiation factor 2. Genetics 158:123-132.
17. 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.
18. 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.
19. Garcia-Barrio, M. T., T. Naranda, R. Cuesta, A. G. Hinnebusch, J. W. B. Hershey, and M. Tamame. 1995. GCD10, a translational repressor of GCN4, is the RNA-binding subunit of eukaryotic translation initiation factor-3. Genes Dev. 9:1781-1796.
20. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527-534.
21. Gietz, R. D., A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355-560.
22. Gomez, E., S. S. Mohammad, and G. D. Pavitt. 2002. Characterization of the minimal catalytic domain within eIF2B: the guanine-nucleotide exchange factor for translation initiation. EMBO J. 21:5292-5301.
23. Gomez, E., and G. D. Pavitt. 2000. Identification of domains and residues within the epsilon subunit of eukaryotic translation initiation factor 2B (eIF2β) required for guanine nucleotide exchange reveals a novel activation function promoted by eIF2B complex formation. Mol. Cell. Biol. 20:3965-3976.
24. Hannig, E. H., N. P. Williams, R. C. Wek, and A. G. Hinnebusch. 1990. The translational activator GCN3 functions downstream from GCN1 and GCN2 in the regulatory pathway that couples GCN4 expression to amino acid availability in Saccharomyces cerevisiae. Genetics 126:549-562.
25. Hinnebusch, A. G. 1996. Translational control of GCN4: gene-specific regulation by phosphorylation of eIF2, p. 199-244. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Hinnebusch, A. G. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59:407-450.
27. Hoffman, C. S., and F. Winston. 1987. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267-272.
28. Jivotovskaya, A. V., L. Valasek, A. G. Hinnebusch, and K. H. Nielsen. 2006. Eukaryotic translation initiation factor 3 (eIF3) and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol. Cell. Biol. 26:1355-1372.
29. Kapp, L. D., and J. R. Lorsch. 2004. GTP-dependent recognition of the methionine moiety on initiator tRNA by translation factor eIF2. J. Mol. Biol. 335:923-936.
30. Kawagishi-Kobayashi, M., J. B. Silverman, T. L. Ung, and T. E. Dever. 1997. Regulation of the protein kinase PKR by the vaccinia virus pseudosubstrate inhibitor K3L is dependent on residues conserved between the K3L protein and the PKR substrate eIF2α. Mol. Cell. Biol. 17:4146-4158.
31. Kimball, S. R., J. R. Fabian, G. D. Pavitt, A. G. Hinnebusch, and L. S. Jefferson. 1998. Regulation of guanine nucleotide exchange through phosphorylation of eukaryotic initiation factor eIF2α. J. Biol. Chem. 273:12841-12845.
32. Krishnamoorthy, T., G. D. Pavitt, F. Zhang, T. E. Dever, and A. G. Hinnebusch. 2001. Tight binding of the phosphorylated α subunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell. Biol. 21:5018-5030.
33. Labib, K., J. A. Tercero, and J. F. Diffley. 2000. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288:1643-1647.
34. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
35. Lu, J., E. B. O'Hara, B. A. Trieselmann, P. R. Romano, and T. E. Dever. 1999. The interferon-induced double-stranded RNA-activated protein kinase PKR will phosphorylate serine, threonine, or tyrosine at residue 51 in eukaryotic initiation factor 2alpha. J. Biol. Chem. 274:32198-32203.
36. Mohammad-Qureshi, S. S., R. Haddad, E. J. Hemingway, J. P. Richardson, and G. D. Pavitt. 2007. Critical contacts between the eukaryotic initiation factor 2B (eIF2B) catalytic domain and both eIF2beta and -2gamma mediate guanine nucleotide exchange. Mol. Cell. Biol. 27:5225-5234.
37. Pavitt, G. D., K. V. A. Ramaiah, S. R. Kimball, and A. G. Hinnebusch. 1998. eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange. Genes Dev. 12:514-526.
38. 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.
39. Proud, C. G. 1992. Protein phosphorylation in translational control. Curr. Top. Cell. Regul. 32:243-369.
40. Ramirez, M., R. C. Wek, C. R. Vazquez de Aldana, B. M. Jackson, B. Freeman, and A. G. Hinnebusch. 1992. Mutations activating the yeast eIF-2α kinase GCN2: isolation of alleles altering the domain related to histidyltRNA synthetases. Mol. Cell. Biol. 12:5801-5815.
41. Reid, G. A., and G. Schatz. 1982. Import of proteins into mitochondria. Yeast cells grown in the presence of carbonyl cyanide m-chlorophenylhydrazone accumulate massive amounts of some mitochondrial precursor polypeptides. J. Biol. Chem. 257:13056-13061.
42. Richardson, J. P., S. S. Mohammad, and G. D. Pavitt. 2004. Mutations causing childhood ataxia with central nervous system hypomyelination reduce eukaryotic initiation factor 2B complex formation and activity. Mol. Cell. Biol. 24:2352-2363.
43. Sherman, F., G. R. Fink, and C. W. Lawrence. 1974. Methods in yeast genetics, p. 61-64. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
44. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
45. Singh, C. R., T. Udagawa, B. Lee, S. Wassink, H. He, Y. Yamamoto, J. T. Anderson, G. D. Pavitt, and K. Asano. 2007. Change in nutritional status modulates the abundance of critical pre-initiation intermediate complexes during translation initiation in vivo. J. Mol. Biol. 370:315-330.
46. Vazquez de Aldana, C. R., T. E. Dever, and A. G. Hinnebusch. 1993. Mutations in the α subunit of eukaryotic translation initiation factor 2 (eIF-2α) that overcome the inhibitory effects of eIF-2α phosphorylation on translation initiation. Proc. Natl. Acad. Sci. U. S. A. 90:7215-7219.
47. 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.
48. Vazquez de Aldana, C. R., R. C. Wek, P. San Segundo, A. G. Truesdell, and A. G. Hinnebusch. 1994. Multicopy tRNA genes functionally suppress mutations in yeast eIF-2α kinase GCN2: evidence for separate pathways coupling GCN4 expression to uncharged tRNA. Mol. Cell. Biol. 14:7920-7932.
49. Williams, D. D., N. T. Price, A. J. Loughlin, and C. G. Proud. 2001. Characterization of the mammalian initiation factor eIF2B complex as a GDP dissociation stimulator protein. J. Biol. Chem. 276:24697-24703.
50. 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.