eIF2B promotes eIF5 dissociation from eIF2•GDP to facilitate guanine nucleotide exchange for translation initiation

Genes and Development

Volumn 27, Issue 24, 2013, Pages 2696-2707

  Jennings, Martin D ^a   Zhou, Yu ^a   Mohammad Qureshi, Sarah S ^a   Bennett, David ^a   Pavitt, Graham D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

G protein regulators; GDF; GDI; GEF; Protein synthesis initiation

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; INITIATION FACTOR 2B EPSILON; INITIATION FACTOR 2B GAMMA; INITIATION FACTOR 5; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG;

ARTICLE; DISSOCIATION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RNA TRANSLATION; TRANSLATION INITIATION;

G-PROTEIN REGULATORS; GDF; GDI; GEF; PROTEIN SYNTHESIS INITIATION;

EUKARYOTIC INITIATION FACTOR-2B; EUKARYOTIC INITIATION FACTORS; GUANINE; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; GUANOSINE DIPHOSPHATE; MUTATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84890605702     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.231514.113     Document Type: Article

References (54)

1. Algire M. A, Maag D, Lorsch JR. 2005. Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol Cell 20: 251-262.
2. Alone P. V, Dever TE. 2006. Direct binding of translation initiation factor eIF2γ-G domain to its GTPase-activating and GDP-GTP exchange factors eIF5 and eIF2Be. J Biol Chem 281: 12636-12644.
3. Amberg D. C, Burke D, Strathern JN, Laboratory CSH. 2005. Methods in yeast genetics: A Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Asano K., Krishnamoorthy T, Phan L, Pavitt GD, Hinnebusch AG. 1999. Conserved bipartite motifs in yeast eIF5 and eIF2Be, GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J 18: 1673-1688.
5. Baird T. D, Wek RC. 2012. Eukaryotic initiation factor 2 phosphorylation and translational control in metabolism. Adv Nutr 3: 307-321.
6. Bieniossek C., Schutz P, Bumann M, Limacher A, Uson I, Baumann U. 2006. The crystal structure of the carboxyterminal domain of human translation initiation factor eIF5. J Mol Biol 360: 457-465.
7. Boesen T., Mohammad SS, Pavitt GD, Andersen GR. 2004. Structure of the catalytic fragment of translation initiation factor 2B and identification of a critically important catalytic residue. J Biol Chem 279: 10584-10592.
8. Dever T. E, Yang W, Astrom S, Bystrom AS, Hinnebusch AG. 1995. Modulation of tRNAi Met, eIF-2 and eIF-2B expression shows that GCN4 translation is inversely coupled to the level of eIF-2_GTP_Met-tRNAi Met ternary complexes. Mol Cell Biol 15: 6351-6363.
9. Dirac-Svejstrup A. B, Sumizawa T, Pfeffer SR. 1997. Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI. EMBO J 16: 465-472.
10. Erickson F. L, Hannig EM. 1996. Ligand interactions with eukaryotic translation initiation factor 2: Role of the γ-subunit. EMBO J 15: 6311-6320.
11. Erickson F. L, Nika J, Rippel S, Hannig EM. 2001. Minimum requirements for the function of eukaryotic translation initiation factor 2. Genetics 158: 123-132.
12. Fogli A., Schiffmann R, Hugendubler L, Combes P, Bertini E, Rodriguez D., Kimball SR, Boespflug-Tanguy O. 2004. Decreased guanine nucleotide exchange factor activity in eIF2Bmutated patients. Eur J Hum Genet 12: 561-566.
13. Gietz R. D, Sugino A. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534.
14. Gietz R. D, Woods RA. 2006. Yeast transformation by the LiAc/SS Carrier D. NA/PEG method. Methods Mol Biol 313: 107-120.
15. Gomez E., Pavitt GD. 2000. Identification of domains and residues within the e subunit of eukaryotic translation initiation factor 2B (eIF2Be) required for guanine nucleotide exchange reveals a novel activation function promoted by eIF2B complex formation. Mol Cell Biol 20: 3965-3976.
16. Gomez E., Mohammad SS, Pavitt GD. 2002. Characterization of the minimal catalytic domain within eIF2B: The guaninenucleotide exchange factor for translation initiation. EMBO J 21: 5292-5301.
17. Grant C. M, Miller PF, Hinnebusch AG. 1994. Requirements for intercistronic distance and level of eukaryotic initiation factor 2 activity in reinitiation on GCN4 mRNA vary with the downstream cistron. Mol Cell Biol 14: 2616-2628.
18. Harashima S., Hinnebusch AG. 1986. Multiple GCD genes required for repression of GCN4, a transcriptional activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol Cell Biol 6: 3990-3998.
19. Harashima S., Hannig EM, Hinnebusch AG. 1987. Interactions between positive and negative regulators of GCN4 controlling gene expression and entry into the yeast cell cycle. Genetics 117: 409-419.
20. Hinnebusch A. G, Lorsch JR. 2012. The mechanism of eukaryotic translation initiation: New insights and challenges. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a011544.
21. Horzinski L., Huyghe A, Cardoso MC, Gonthier C, Ouchchane L, Schiffmann R, Blanc P, Boespflug-Tanguy O, Fogli A. 2009. Eukaryotic initiation factor 2B (eIF2B) GEF activity as a diagnostic tool for EIF2B-related disorders. PLoS ONE 4: e8318.
22. Jackson R. J, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
23. Jennings M. D, Pavitt GD. 2010a. eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation. Nature 465: 378-381.
24. Jennings M. D, Pavitt GD. 2010b. eIF5 is a dual function GAP and GDI for eukaryotic translational control. Small GTPases 1: 118-123.
25. Krishnamoorthy T., Pavitt GD, Zhang F, Dever TE, Hinnebusch AG. 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.
26. Li W., Wang X, Van Der Knaap MS, Proud CG. 2004. Mutations linked to leukoencephalopathy with vanishing white matter impair the function of the eukaryotic initiation factor 2B complex in diverse ways. Mol Cell Biol 24: 3295-3306.
27. Liu R., van der Lei HD, Wang X, Wortham NC, Tang H, van Berkel C. G, Mufunde TA, Huang W, van der Knaap MS, Scheper G. C, et al. 2011. Severity of vanishing white matter disease does not correlate with deficits in eIF2B activity or the integrity of eIF2B complexes. Hum Mutat 32: 1036-1045.
28. Luna R. E, Arthanari H, Hiraishi H, Nanda J, Martin-Marcos P, Markus M. A, Akabayov B, Milbradt AG, Luna LE, Seo HC, et al. 2012. The C-terminal domain of eukaryotic initiation factor 5 promotes start codon recognition by its dynamic interplay with eIF1 and eIF2β. Cell Rep 1: 689-702.
29. Machner M. P, Isberg RR. 2007. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318: 974-977.
30. Matsukawa T., Wang X, Liu R, Wortham NC, Onuki Y, Kubota A, Hida A, Kowa H, Fukuda Y, Ishiura H, et al. 2011. Adultonset leukoencephalopathies with vanishing white matter with novel missense mutations in EIF2B2, EIF2B3, and EIF2B5. Neurogenetics 12: 259-261.
31. Mohammad-Qureshi S. S, Haddad R, Hemingway EJ, Richardson JP, Pavitt GD. 2007a. Critical contacts between the eukaryotic initiation factor 2B (eIF2B) catalytic domain and both eIF2β and-2γ mediate guanine nucleotide exchange. Mol Cell Biol 27: 5225-5234.
32. Mohammad-Qureshi S. S, Haddad R, Palmer KS, Richardson JP, Gomez E., Pavitt GD. 2007b. Purification of Flag-tagged eukaryotic initiation factor 2B complexes, subcomplexes, and fragments from Saccharomyces cerevisiae. Methods Enzymol 431: 1-13.
33. Mueller P. P, Jackson BM, Miller PF, Hinnebusch AG. 1988. The first and fourth upstream open reading frames in GCN4 mRNA have similar initiation efficiencies but respond differently in translational control to change in length and sequence. Mol Cell Biol 8: 5439-5447.
34. Nika J., Yang W, Pavitt GD, Hinnebusch AG, Hannig EM. 2000. Purification and kinetic analysis of eIF2B from Saccharomyces cerevisiae. J Biol Chem 275: 26011-26017.
35. Panniers R., Rowlands AG, Henshaw EC. 1988. The effect of Mg2+ and guanine nucleotide exchange factor on the binding of guanine nucleotides to eukaryotic initiation factor 2. J Biol Chem 263: 5519-5525.
36. Pavitt G.D. 2005. eIF2B, a mediator of general and gene-specific translational control. Biochem Soc Trans 33: 1487-1492.
37. Pavitt G. D, Proud CG. 2009. Protein synthesis and its control in neuronal cells with a focus on vanishing white matter disease. Biochem Soc Trans 37: 1298-1310.
38. Pavitt G. D, Yang W, Hinnebusch AG. 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. Pavitt G. D, Ramaiah KV, Kimball SR, Hinnebusch AG. 1998. eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange. Genes Dev 12: 514-526.
40. Pfeffer S.R. 1994. Rab GTPases: Master regulators of membrane trafficking. Curr Opin Cell Biol 6: 522-526.
41. Reid P. J, Mohammad-Qureshi SS, Pavitt GD. 2012. Identification of intersubunit domain interactions within eukaryotic initiation factor (eIF) 2B, the nucleotide exchange factor for translation initiation. J Biol Chem 287: 8275-8285.
42. Rhee H. S, Pugh BF. 2011. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147: 1408-1419.
43. Richardson J. P, Mohammad SS, Pavitt GD. 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.
44. Rowlands A. G, Panniers R, Henshaw EC. 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.
45. Shapiro A. D, Pfeffer SR. 1995. Quantitative analysis of the interactions between prenyl Rab9, GDP dissociation inhibitor-α, and guanine nucleotides. J Biol Chem 270: 11085-11090.
46. Singh C. R, Lee B, Udagawa T, Mohammad-Qureshi SS, Yamamoto Y, Pavitt GD, Asano K. 2006. An eIF5/eIF2 complex antago-nizes guanine nucleotide exchange by eIF2B during translation initiation. EMBO J 25: 4537-4546.
47. Singh C. R, Udagawa T, Lee B, Wassink S, He H, Yamamoto Y, Anderson J. T, Pavitt GD, Asano K. 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.
48. Sivars U., Aivazian D, Pfeffer SR. 2003. Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425: 856-859.
49. Suh H. Y, Lee DW, Lee KH, Ku B, Choi SJ, Woo JS, Kim YG, Oh BH. 2010. Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA. EMBO J 29: 496-504.
50. van der Knaap MS, Leegwater PA, Konst AA, Visser A, Naidu S, Oudejans C. B, Schutgens RB, Pronk JC. 2002. Mutations in each of the five subunits of translation initiation factor eIF2B can cause leukoencephalopathy with vanishing white matter. Ann Neurol 51: 264-270.
51. Wei Z., Xue Y, Xu H, Gong W. 2006. Crystal structure of the C-terminal domain of S. cerevisiae eIF5. J Mol Biol 359: 1-9.
52. Wolfner M., Yep D, Messenguy F, Fink GR. 1975. Integration of amino acid biosynthesis into the cell cycle of Saccharomyces cerevisiae. J Mol Biol 96: 273-290.
53. Yang W., Hinnebusch AG. 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.
54. Yoshimura S., Gerondopoulos A, Linford A, Rigden DJ, Barr FA. 2010. Family-wide characterization of the DENN domain Rab G. DP-GTP exchange factors. J Cell Biol 191: 367-381.