EIF2B is a decameric guanine nucleotide exchange factor with a γ2 ε

Nature Communications

Volumn 5, Issue , 2014, Pages

  Gordiyenko, Yuliya ^a,b   Schmidt, Carla ^a   Jennings, Martin D ^c   Matak Vinkovic, Dijana ^b   Pavitt, Graham D ^c   Robinson, Carol V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; CROSS LINKING REAGENT; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 2; PROTEIN BINDING; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE PROTEIN; SOLVENT;

EUKARYOTE; HOMOLOGY; MASS SPECTROMETRY; NUCLEIC ACID; PROTEIN; STOICHIOMETRY;

ARTICLE; CATALYST; COMPLEX FORMATION; CROSS LINKING; MASS SPECTROMETRY; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; STOICHIOMETRY; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURAL HOMOLOGY;

CROSS-LINKING REAGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-2B; GUANOSINE TRIPHOSPHATE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SOLVENTS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84901452168     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4902     Document Type: Article

References (55)

1. Sonenberg, N. & Hinnebusch, A. G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745 (2009).
2. Maag, D., Fekete, C. A., Gryczynski, Z. & Lorsch, J. R. A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol. Cell 17, 265-275 (2005).
3. Singh, C. R. et al. An eIF5/eIF2 complex antagonizes guanine nucleotide exchange by eIF2B during translation initiation. EMBO J. 25, 4537-4546 (2006).
4. Jennings, M. D. & Pavitt, G. D. eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation. Nature 465, 378-381 (2010).
5. Jennings, M. D., Zhou, Y., Mohammad-Qureshi, S. S., Bennett, D. & Pavitt, G. D. eIF2B promotes eIF5 dissociation from eIF2*GDP to facilitate guanine nucleotide exchange for translation initiation. Genes Dev. 27, 2696-2707 (2013).
6. Nika, J., Rippel, S. & Hannig, E. M. Biochemical analysis of the eIF2beta gamma complex reveals a structural function for eIF2alpha in catalyzed nucleotide exchange. J. Biol. Chem. 276, 1051-1056 (2001).
7. Naveau, M. et al. Roles of yeast eIF2alpha and eIF2beta subunits in the binding of the initiator methionyl-tRNA. Nucleic Acids Res. 41, 1047-1057 (2013).
8. Hinnebusch, A. G. Gene-specific translational control of the yeast GCN4 gene by phosphorylation of eukaryotic initiation factor 2. Mol. Microbiol. 10, 215-223 (1993).
9. Krishnamoorthy, T., Pavitt, G. D., Zhang, F., Dever, T. E. & Hinnebusch, A. G. 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 (2001).
10. Sudhakar, A. et al. Phosphorylation of serine 51 in initiation factor 2 alpha (eIF2 alpha) promotes complex formation between eIF2 alpha(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39, 12929-12938 (2000).
11. Borck, G. et al. eIF2gamma mutation that disrupts eIF2 complex integrity links intellectual disability to impaired translation initiation. Mol. Cell. 48, 641-646 (2012).
12. van der Knaap, M. S. et al. Mutations in each of the five subunits of translation initiation factor eIF2B can cause leukoencephalopathy with vanishing white matter. Ann. Neurol. 51, 264-270 (2002).
13. Yatime, L., Mechulam, Y., Blanquet, S. & Schmitt, E. Structure of an archaeal heterotrimeric initiation factor 2 reveals a nucleotide state between the GTP and the GDP states. Proc. Natl Acad. Sci. USA 104, 18445-18450 (2007).
14. Ito, T., Marintchev, A. & Wagner, G. Solution structure of human initiation factor eIF2alpha reveals homology to the elongation factor eEF1B. Structure 12, 1693-1704 (2004).
15. Nonato, M. C., Widom, J. & Clardy, J. Crystal structure of the N-terminal segment of human eukaryotic translation initiation factor 2alpha. J. Biol. Chem. 277, 17057-17061 (2002).
16. Dhaliwal, S. & Hoffman, D. W. The crystal structure of the N-terminal region of the alpha subunit of translation initiation factor 2 (eIF2alpha) from Saccharomyces cerevisiae provides a view of the loop containing serine 51, the target of the eIF2alpha-specific kinases. J. Mol. Biol. 334, 187-195 (2003).
17. Hiyama, T. B., Ito, T., Imataka, H. & Yokoyama, S. Crystal structure of the alpha subunit of human translation initiation factor 2B. J. Mol. Biol. 392, 937-951 (2009).
18. Boesen, T., Mohammad, S. S., Pavitt, G. D. & Andersen, G. R. Structure of the catalytic fragment of translation initiation factor 2B and identification of a critically important catalytic residue. J. Biol. Chem. 279, 10584-10592 (2004).
19. Pavitt, G. D., Ramaiah, K. V., Kimball, S. R. & Hinnebusch, A. G. eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange. Genes Dev. 12, 514-526 (1998).
20. Pavitt, G. D., Yang, W. & Hinnebusch, A. G. 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 (1997).
21. Dev, K. et al. 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 (2010).
22. Pavitt, G. D. eIF2B, a mediator of general and gene-specific translational control. Biochem. Soc. Trans. 33, 1487-1492 (2005).
23. Gomez, E., Mohammad, S. S. & Pavitt, G. D. Characterization of the minimal catalytic domain within eIF2B: the guanine-nucleotide exchange factor for translation initiation. EMBO J. 21, 5292-5301 (2002).
24. Asano, K., Krishnamoorthy, T., Phan, L., Pavitt, G. D. & Hinnebusch, A. G. Conserved bipartite motifs in yeast eIF5 and eIF2Bepsilon, GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J. 18, 1673-1688 (1999).
25. Alone, P. V. & Dever, T. E. Direct binding of translation initiation factor eIF2gamma-G domain to its GTPase-activating and GDP-GTP exchange factors eIF5 and eIF2B epsilon. J. Biol. Chem. 281, 12636-12644 (2006).
26. Mohammad-Qureshi, S. S., Haddad, R., Hemingway, E. J., Richardson, J. P. & Pavitt, G. D. 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 (2007).
27. Reid, P. J., Mohammad-Qureshi, S. S. & Pavitt, G. D. Identification of intersubunit domain interactions within eukaryotic initiation factor (eIF) 2B, the nucleotide exchange factor for translation initiation. J. Biol. Chem. 287, 8275-8285 (2012).
28. Wang, X.,Wortham, N. C., Liu, R. & Proud, C. G. Identification of residues that underpin interactions within the eukaryotic initiation factor (eIF2) 2B complex. J. Biol. Chem. 287, 8263-8274 (2012).
29. Hernandez, H. & Robinson, C. V. Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2, 715-726 (2007).
30. Taverner, T. et al. Subunit architecture of intact protein complexes from mass spectrometry and homology modeling. Acc. Chem. Res. 41, 617-627 (2008).
31. Cigan, A. M., Bushman, J. L., Boal, T. R. & Hinnebusch, A. G. A protein complex of translational regulators of GCN4 mRNA is the guanine nucleotideexchange factor for translation initiation factor 2 in yeast. Proc. Natl Acad. Sci. USA 90, 5350-5354 (1993).
32. Hall, Z., Politis, A. & Robinson, C. V. Structural modeling of heteromeric protein complexes from disassembly pathways and ion mobility-mass spectrometry. Structure 20, 1596-1609 (2012).
33. Mohammad-Qureshi, S. S. et al. Purification of FLAG-tagged eukaryotic initiation factor 2B complexes, subcomplexes, and fragments from Saccharomyces cerevisiae. Methods Enzymol. 431, 1-13 (2007).
34. Nika, J., Yang, W., Pavitt, G. D., Hinnebusch, A. G. & Hannig, E. M. Purification and kinetic analysis of eIF2B from Saccharomyces cerevisiae. J. Biol. Chem. 275, 26011-26017 (2000).
35. Tahara, M., Ohsawa, A., Saito, S. & Kimura, M. In vitro phosphorylation of initiation factor 2 alpha (aIF2 alpha) from hyperthermophilic archaeon Pyrococcus horikoshii OT3. J. Biochem. 135, 479-485 (2004).
36. Schwanhäusser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
37. Eswar, N. et al. Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 31, 3375-3380 (2003).
38. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006).
39. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 27-38 (1996).
40. Stolboushkina, E. et al. Crystal structure of the intact archaeal translation initiation factor 2 demonstrates very high conformational flexibility in the alpha-and beta-subunits. J. Mol. Biol. 382, 680-691 (2008).
41. Yang, W. & Hinnebusch, A. G. Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2. Mol. Cell Biol. 16, 6603-6616 (1996).
42. Wortham, N. C., Martinez, M., Gordiyenko, Y., Robinson, C. V. & Proud, C. G. Analysis of the subunit organization of the eIF2B complex reveals new insights into its structure and regulation. FASEB J. 28, 2225-2237 (2014).
43. Panniers, R., Rowlands, A. G. & Henshaw, E. C. 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 (1988).
44. Manchester, K. L. 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 (1997).
45. Kimball, S. R., Fabian, J. R., Pavitt, G. D., Hinnebusch, A. G. & Jefferson, L. S. Regulation of guanine nucleotide exchange through phosphorylation of eukaryotic initiation factor eIF2a. Role of the alpha-and delta-subunits of eIF2B. J. Biol. Chem. 273, 12841-12845 (1998).
46. Sobott, F., Hernandez, H., McCammon, M. G., Tito, M. A. & Robinson, C. V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74, 1402-1407 (2002).
47. Chernushevich, I. V. & Thomson, B. A. Collisional cooling of large ions in electrospray mass spectrometry. Anal. Chem. 76, 1754-1760 (2004).
48. Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
49. Olsen, J. V. et al. Parts per million mass accuracy on an orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (2005).
50. Xu, H. & Freitas, M. A. A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data. BMC Bioinformatics 8, 133 (2007).
51. Xu, H. & Freitas, M. A. Monte carlo simulation-based algorithms for analysis of shotgun proteomic data. J. Proteome Res. 7, 2605-2615 (2008).
52. Xu, H., Zhang, L. & Freitas, M. A. Identification and characterization of disulfide bonds in proteins and peptides from tandem MS data by use of the MassMatrix MS/MS search engine. J. Proteome Res. 7, 138-144 (2008).
53. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
54. Schwanhausser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
55. Mendoza, V. L. & Vachet, R. W. Protein surface mapping using diethylpyrocarbonate with mass spectrometric detection. Anal. Chem. 80, 2895-2904 (2008).