Identification of intersubunit domain interactions within eukaryotic Initiation Factor (eIF) 2B, the nucleotide exchange factor for translation initiation

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8275-8285

  Reid, Peter J ^a   Mohammad Qureshi, Sarah S ^a   Pavitt, Graham D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CO-EXPRESSION; COMPLEX FORMATIONS; EUKARYOTIC INITIATION FACTOR; EUKARYOTIC TRANSLATION; G PROTEIN; GENETIC APPROACH; GUANINE NUCLEOTIDE EXCHANGE FACTORS; LEUKOENCEPHALOPATHY; NUCLEOTIDE EXCHANGE; NUCLEOTIDE-EXCHANGE FACTOR; PROTEIN SYNTHESIS; SUGAR NUCLEOTIDES; TERTIARY STRUCTURES;

PHOSPHORYLATION; PROGRAMMABLE LOGIC CONTROLLERS; SUGARS;

NUCLEOTIDES;

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR EPSILON; GUANINE NUCLEOTIDE EXCHANGE FACTOR GAMMA; PHOSPHOHEXOSE SUGAR NUCLEOTIDE PYROPHOSPHORYLASE; PHOSPHORYLASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; GENETIC ANALYSIS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TRANSLATION INITIATION;

CATALYTIC DOMAIN; EUKARYOTIC INITIATION FACTOR-2B; HUMANS; MULTIENZYME COMPLEXES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PEPTIDE MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 84858027453     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331645     Document Type: Article

References (48)

1. Hinnebusch, A. G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434-467
2. Schmitt, E., Naveau, M., and Mechulam, Y. (2010) Eukaryotic and archaeal translation initiation factor 2: a heterotrimeric tRNA carrier. FEBS Lett. 584, 405-412
3. Jennings, M. D., and Pavitt, G. D. (2010) eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation. Nature 465, 378-381
4. Pavitt, G. D. (2005) eIF2B, a mediator of general and gene-specific translational control. Biochem. Soc. Trans. 33, 1487-1492
5. Pavitt, G. D., Ramaiah, K. V., Kimball, S. R., and Hinnebusch, A. G. (1998) eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange. Genes Dev. 12, 514-526 (Pubitemid 28101014)
6. Jackson, R. J., Hellen, C. U., and Pestova, T. V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113-127
7. Pavitt, G. D., and Proud, C. G. (2009) Protein synthesis and its control in neuronal cells with a focus on vanishing white matter disease. Biochem. Soc. Trans. 37, 1298-1310
8. Horzinski, L., Huyghe, A., Cardoso, M. C., Gonthier, C., Ouchchane, L., Schiffmann, R., Blanc, P., Boespflug-Tanguy, O., and Fogli, A. (2009) Eukaryotic initiation factor 2B (eIF2B) GEF activity as a diagnostic tool for EIF2B-related disorders. PLoS One 4, e8318
9. Yang, W., and Hinnebusch, A. G. (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 (Pubitemid 26361019)
10. Pavitt, G. D., Yang, W., and Hinnebusch, A. G. (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 (Pubitemid 27097359)
11. Krishnamoorthy, T., Pavitt, G. D., Zhang, F., Dever, T. E., and Hinnebusch, A. G. (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 (Pubitemid 32656399)
12. Kimball, S. R., Fabian, J. R., Pavitt, G. D., Hinnebusch, A. G., and Jefferson, L. S. (1998) Regulation of guanine nucleotide exchange through phosphorylation of eukaryotic initiation factor eIF2α. Role of the α and δ subunits of eiF2b. J. Biol. Chem. 273, 12841-12845 (Pubitemid 28246840)
13. Gomez, E., Mohammad, S. S., and Pavitt, G. D. (2002) Characterization of the minimal catalytic domain within eIF2B: the guanine-nucleotide exchange factor for translation initiation. EMBO J. 21, 5292-5301
14. Mohammad-Qureshi, S. S., Haddad, R., Hemingway, E. J., Richardson, J. P., and Pavitt, G. D. (2007) Critical contacts between the eukaryotic initiation factor 2B (eIF2B) catalytic domain and both eIF2β and eIF2γmediate guanine nucleotide exchange. Mol. Cell Biol. 27, 5225-5234 (Pubitemid 47068295)
15. Fabian, J. R., Kimball, S. R., Heinzinger, N. K., and Jefferson, L. S. (1997) Subunit assembly and guanine nucleotide exchange activity of eukaryotic initiation factor-2B expressed in Sf9 cells. J. Biol. Chem. 272, 12359-12365 (Pubitemid 27203321)
16. Williams, D. D., Pavitt, G. D., and Proud, C. G. (2001) Characterization of the initiation factor eIF2B and its regulation in Drosophila melanogaster. J. Biol. Chem. 276, 3733-3742
17. Bushman, J. L., Asuru, A. I., Matts, R. L., and Hinnebusch, A. G. (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 (Pubitemid 23068132)
18. Koonin, E. V. (1995) Multidomain organization of eukaryotic guanine nucleotide exchange translation initiation factor eIF-2B subunits revealed by analysis of conserved sequence motifs. Protein Sci. 4, 1608-1617
19. Jin, X., Ballicora, M. A., Preiss, J., and Geiger, J. H. (2005) Crystal structure of potato tuber ADP-glucose pyrophosphorylase. EMBO J. 24, 694-704 (Pubitemid 40396100)
20. Brown, K., Pompeo, F., Dixon, S., Mengin-Lecreulx, D., Cambillau, C., and Bourne, Y. (1999) Crystal structure of the bifunctional N-acetylglucosamine 1-phosphate uridyltransferase from Escherichia coli: a paradigm for the related pyrophosphorylase superfamily. EMBO J. 18, 4096-4107 (Pubitemid 29364113)
21. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-392
22. Pieper, U., Webb, B. M., Barkan, D. T., Schneidman-Duhovny, D., Schlessinger, A., Braberg, H., Yang, Z., Meng, E. C., Pettersen, E. F., Huang, C. C., Datta, R. S., Sampathkumar, P., Madhusudhan, M. S., Sjölander, K., Ferrin, T. E., Burley, S. K., and Sali, A. (2011) ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 39, D465-474
23. Guthrie, C., and Fink, G. R. (eds). (1991) Guide to Yeast Genetics and Molecular Biology, Vol. 194, Academic Press Inc, San Diego, CA
24. Gietz, R. D., and Woods, R. A. (2006) Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol. Biol. 313, 107-120
25. Asano, K., Krishnamoorthy, T., Phan, L., Pavitt, G. D., and Hinnebusch, A. G. (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 (Pubitemid 29127079)
26. Gomez, E., and Pavitt, G. D. (2000) Identification of domains and residues within the ε subunit of eukaryotic translation initiation factor 2B (eIF2Bε) required for guanine nucleotide exchange reveals a novel activation function promoted by eIF2B complex formation. Mol. Cell Biol. 20, 3965-3976 (Pubitemid 30314495)
27. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (Pubitemid 28022245)
28. Boesen, T., Mohammad, S. S., Pavitt, G. D., and Andersen, G. R. (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 (Pubitemid 38372670)
29. Mohammad-Qureshi, S. S., Jennings, M. D., and Pavitt, G. D. (2008) Clues to the mechanism of action of eIF2B, the guanine nucleotide exchange factor for translation initiation. Biochem. Soc. Trans. 36, 658-664
30. Mitchell, D. A., Marshall, T. K., and Deschenes, R. J. (1993) Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast 9, 715-722 (Pubitemid 23228871)
31. Miller, C. A., 3rd, Martinat, M. A., and Hyman, L. E. (1998) Assessment of aryl hydrocarbon receptor complex interactions using pBEVY plasmids: expression vectors with bidirectional promoters for use in Saccharomyces cerevisiae. Nucleic Acids Res. 26, 3577-3583 (Pubitemid 28347232)
32. Mohammad-Qureshi, S. S., Haddad, R., Palmer, K. S., Richardson, J. P., Gomez, E., and Pavitt, G. D. (2007) Purification of FLAG-tagged eukaryotic initiation factor 2B complexes, subcomplexes, and fragments from Saccharomyces cerevisiae. Methods Enzymol. 431, 1-13
33. Manchester, K. L. (1997) Catalysis of guanine nucleotide exchange on eIF-2 by eIF-2B: is it a sequential or substituted enzyme mechanism? Biochem. Biophys. Res. Commun. 239, 223-227
34. Nika, J., Yang, W., Pavitt, G. D., Hinnebusch, A. G., and Hannig, E. M. (2000) Purification and kinetic analysis of eIF2B from Saccharomyces cerevisiae. J. Biol. Chem. 275, 26011-26017
35. Richardson, J. P., Mohammad, S. S., and Pavitt, G. D. (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 (Pubitemid 38325992)
36. Sprang, S. R., and Coleman, D. E. (1998) Invasion of the nucleotide snatchers: structural insights into the mechanism of G protein GEFs. Cell 95, 155-158 (Pubitemid 28473776)
37. Siderovski, D. P., and Willard, F. S. (2005) The GAPs, GEFs, and GDIs of heterotrimeric G protein α subunits. Int. J. Biol. Sci. 1, 51-66
38. Manchester, K. L. (2001) Catalysis of guanine nucleotide exchange on eIF2 by eIF2B: can it be both a substituted enzyme and a sequential mechanism? Biochem. Biophys. Res. Commun. 289, 643-646
39. Price, N., and Proud, C. (1994) The guanine nucleotide exchange factor, eIF-2B. Biochimie 76, 748-760
40. Hiyama, T. B., Ito, T., Imataka, H., and Yokoyama, S. (2009) Crystal structure of the α subunit of human translation initiation factor 2B. J. Mol. Biol. 392, 937-951
41. Dev, K., Santangelo, T. J., Rothenburg, S., Neculai, D., Dey, M., Sicheri, F., Dever, T. E., Reeve, J. N., and Hinnebusch, A. G. (2009) Archaeal aIF2B interacts with eukaryotic translation initiation factors eIF2α and eIF2Bα: implications for aIF2B function and eIF2B regulation. J. Mol. Biol. 392, 701-722
42. Liu, A. R., van der Lei, H. D., Wang, X., Wortham, N. C., Tang, H., van Berkel, C. G., Mufunde, T. A., Huang, W., van der Knaap, M. S., Scheper, G. C., and Proud, C. G. (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
43. Dev, K., Qiu, H., Dong, J., Zhang, F., Barthlme, D., and Hinnebusch, A. G. (2010) The β/Gcd7 subunit of eukaryotic translation initiation factor 2B (eIF2B), a guanine nucleotide exchange factor, is crucial for binding eIF2 in vivo. Mol. Cell Biol. 30, 5218-5233
44. Li, W., Wang, X., Van Der Knaap, M. S., and Proud, C. G. (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 (Pubitemid 38452074)
45. Anthony, T. G., Fabian, J. R., Kimball, S. R., and Jefferson, L. S. (2000) Identification of domains within the ε 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 (Pubitemid 30349180)
46. Bushman, J. L., Foiani, M., Cigan, A. M., Paddon, C. J., and Hinnebusch, A. G. (1993) Guanine nucleotide exchange factor for eukaryotic translation initiation factor 2 in Saccharomyces cerevisiae: interactions between the essential subunits GCD2, GCD6, and GCD7 and the regulatory subunit GCN3. Mol. Cell Biol. 13, 4618-4631 (Pubitemid 23220369)
47. Met ternary complexes. Mol. Cell Biol. 15, 6351-6363
48. Wang, X., Wortham, N. C., Liu, R., and Proud, C. G. (January 11, 2012) Identification of residues that underpin interactions within the eukaryotic initiation factor (eIF2) 2B complex. J. Biol. Chem. 287, 8263-8274