EIF2B: Recent structural and functional insights into a key regulator of translation

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 1234-1240

  Wortham, Noel C ^a,b   Proud, Christopher G ^a,c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b Trafalgar School   (United Kingdom)

^c SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Eukaryotic initiation factor 2B (eIF2B); Integrated stress response; Integrated stress response inhibitor (ISRIB); Protein synthesis; Vanishing white matter

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN SUBUNIT;

ARTICLE; GENE MUTATION; LEUKOENCEPHALOPATHY; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; STRESS; VANISHING WHITE MATTER; WHITE MATTER; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; MUTATION; PROTEIN CONFORMATION; PROTEIN SUBUNIT; PROTEIN SYNTHESIS;

ANIMALS; EUKARYOTIC INITIATION FACTOR-2B; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LEUKOENCEPHALOPATHIES; MODELS, MOLECULAR; MUTATION; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 84969377017     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150164     Document Type: Article

References (38)

1. 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 CrossRef PubMed
2. Pavitt, G.D. (2005) eIF2B, a mediator of general and gene-specific translational control. Biochem. Soc. Trans. 33, 1487-1492 CrossRef PubMed
3. 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 CrossRef PubMed
4. Price, N.T., Mellor, H., Craddock, B.L., Flowers, K.M., Kimball, S.R., Wilmer, T., Jefferson, L.S. and Proud, C.G. (1996) eIF2B, the guanine nucleotide-exchange factor for eukaryotic initiation factor 2. sequence conservation between the alpha, beta and delta subunits of eIF2B from mammals and yeast. Biochem. J. 318 Pt 2, 637-643 CrossRef PubMed
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 CrossRef PubMed
6. Wang, X., Wortham, N.C., Liu, R. and Proud, C.G. (2012) Identification of residues that underpin interactions within the eukaryotic initiation factor (eIF2) 2B complex. J. Biol. Chem. 287, 8263-8274 CrossRef PubMed
7. Hiyama, T.B., Ito, T., Imataka, H. and Yokoyama, S. (2009) Crystal structure of the alpha subunit of human translation initiation factor 2B. J. Mol. Biol. 392, 937-951 CrossRef PubMed
8. 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 CrossRef PubMed
9. Liu, 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 CrossRef PubMed
10. Pronk, J.C., van, K.B., Scheper, G.C. and van der Knaap, M.S. (2006) Vanishing white matter disease: a review with focus on its genetics. Ment. Retard. Dev. Disabil. Res. Rev. 12, 123-128 CrossRef PubMed
11. 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 CrossRef PubMed
12. Matsukawa, T., Wang, X., Liu, R., Wortham, N.C., Onuki, Y., Kubota, A., Hida, A., Kowa, H., Fukuda, Y., Ishiura, H. et al. (2011) Adult-onset leukoencephalopathies with vanishing white matter with novel missense mutations in EIF2B2, EIF2B3, and EIF2B5. Neurogenetics 12, 259-261 CrossRef PubMed
13. Fogli, A., Schiffmann, R., Hugendubler, L., Combes, P., Bertini, E., Rodriguez, D., Kimball, S.R. and Boespflug-Tanguy, O. (2004) Decreased guanine nucleotide exchange factor activity in eIF2B-mutated patients. Eur. J. Hum. Genet. 12, 561-566 CrossRef PubMed
14. 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 CrossRef PubMed
15. Wang, X., Paulin, F.E., Campbell, L.E., Gomez, E., O'Brien, K., Morrice, N. and Proud, C.G. (2001) Eukaryotic initiation factor 2B: identification of multiple phosphorylation sites in the epsilon-subunit and their functions in vivo. EMBO J. 20, 4349-4359 CrossRef PubMed
16. Welsh, G.I., Miller, C.M., Loughlin, A.J., Price, N.T. and Proud, C.G. (1998) Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in response to insulin. FEBS Lett. 421, 125-130 CrossRef PubMed
17. Woods, Y.L., Cohen, P., Becker, W., Jakes, R., Goedert, M., Wang, X. and Proud, C.G. (2001) The kinase DYRK phosphorylates protein-synthesis initiation factor eIF2Bepsilon at Ser539 and the microtubule-associated protein tau at Thr212: potential role for DYRK as a glycogen synthase kinase 3-priming kinase. Biochem. J. 355, 609-615 CrossRef PubMed
18. Wang, X. and Proud, C.G. (2008) A novel mechanism for the control of translation initiation by amino acids, mediated by phosphorylation of eukaryotic initiation factor 2B. Mol. Cell. Biol. 28, 1429-1442 CrossRef PubMed
19. Wek, R.C., Jiang, H.Y. and Anthony, T.G. (2006) Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11 CrossRef PubMed
20. Bi, M., Naczki, C., Koritzinsky, M., Fels, D., Blais, J., Hu, N., Harding, H., Novoa, I., Varia, M. and Raleigh, J. (2005) ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24, 3470-3481 CrossRef PubMed
21. Krishnamoorthy, T., Pavitt, G.D., Zhang, F., Dever, T.E. and Hinnebusch, A.G. (2001) Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell. Biol. 21, 5018-5030 CrossRef PubMed
22. Dev, K., Qiu, H., Dong, J., Zhang, F., Barthlme, D. and Hinnebusch, A.G. (2010) The beta/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 CrossRef PubMed
23. Vazquez de Aldana, C.R. and Hinnebusch, A.G. (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 PubMed
24. Elsby, R., Heiber, J.F., Reid, P., Kimball, S.R., Pavitt, G.D. and Barber, G.N. (2011) The alpha subunit of eukaryotic initiation factor 2B (eIF2B) is required for eIF2-mediated translational suppression of vesicular stomatitis virus. J. Virol. 85, 9716-9725 CrossRef PubMed
25. 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 PubMed
26. Wortham, N.C. and Proud, C.G. (2015) Biochemical effects of mutations in the gene encoding the alpha subunit of eukaryotic initiation factor (eIF) 2B associated with vanishing white matter disease. BMC Med. Genet. 16, 64 CrossRef
27. Sidrauski, C., Acosta-Alvear, D., Khoutorsky, A., Vedantham, P., Hearn, B.R., Li, H., Gamache, K., Gallagher, C.M., Ang, K.K., Wilson, C. et al. (2013) Pharmacological brake-release of mRNA translation enhances cognitive memory. Elife 2, e00498 CrossRef PubMed
28. Sidrauski, C., Tsai, J.C., Kampmann, M., Hearn, B.R., Vedantham, P., Jaishankar, P., Sokabe, M., Mendez, A.S., Newton, B.W., Tang, E.L. et al. (2015) Pharmacological dimerization and activation of the exchange factor eIF2B antagonizes the integrated stress response. Elife 4, e07314 PubMed
29. Wortham, N.C., Martinez, M., Gordiyenko, Y., Robinson, C.V. and Proud, C.G. (2014) Analysis of the subunit organization of the eIF2B complex reveals new insights into its structure and regulation. FASEB J. 28, 2225-2237 CrossRef PubMed
30. Martin, L., Kimball, S.R. and Gardner, L.B. (2010) Regulation of the unfolded protein response by eif2Bdelta isoforms. J. Biol. Chem. 285, 31944-31953 CrossRef PubMed
31. Bogorad, A.M., Xia, B., Sandor, D.G., Mamonov, A.B., Cafarella, T.R., Jehle, S., Vajda, S., Kozakov, D. and Marintchev, A. (2014) Insights into the architecture of the eIF2Balpha/beta/delta regulatory subcomplex. Biochemistry 53, 3432-3445 CrossRef PubMed
32. Gordiyenko, Y., Schmidt, C., Jennings, M.D., Matak-Vinkovic, D., Pavitt, G.D. and Robinson, C.V. (2014) eIF2B is a decameric guanine nucleotide exchange factor with a gamma2epsilon2 tetrameric core. Nat. Commun. 5, 3902 CrossRef PubMed
33. Sekine, Y., Zyryanova, A., Crespillo-Casado, A., Fischer, P.M., Harding, H.P. and Ron, D. (2015) Stress responses. mutations in a translation initiation factor identify the target of a memory-enhancing compound. Science 348, 1027-1030 CrossRef PubMed
34. Jennings, M.D. and Pavitt, G.D. (2014) A new function and complexity for protein translation initiation factor eIF2B. Cell Cycle 13, 2660-2665 CrossRef PubMed
35. Jennings, M.D., Zhou, Y., Mohammad-Qureshi, S.S., Bennett, D. and Pavitt, G.D. (2013) eIF2B promotes eIF5 dissociation from eIF2-GDP to facilitate guanine nucleotide exchange for translation initiation. Genes Dev. 27, 2696-2707 CrossRef PubMed
36. Jennings, M.D. and Pavitt, G.D. (2010) eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation. Nature 465, 378-381 CrossRef PubMed
37. Singh, C.R., Lee, B., Udagawa, T., Mohammad-Qureshi, S.S., Yamamoto, Y., Pavitt, G.D. and Asano, K. (2006) An eIF5/eIF2 complex antagonizes guanine nucleotide exchange by eIF2B during translation initiation. EMBO J. 25, 4537-4546 CrossRef PubMed
38. Schmitt, E., Naveau, M. and Mechulam, Y. (2010) Eukaryotic and archaeal translation initiation factor 2: a heterotrimeric tRNA carrier. FEBS Lett. 584, 405-412 CrossRef PubMed