Structure of the eukaryotic initiation factor (eIF) 5 reveals a fold common to several translation factors

Biochemistry

Volumn 45, Issue 14, 2006, Pages 4550-4558

  Conte, Maria R ^a,b   Kelly, Geoff ^c   Babon, Jeff ^d   Sanfelice, Domenico ^a,b   Youell, James ^a,b   Smerdon, Stephen J ^c   Proud, Christopher G ^e,f  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CONFORMATIONS; ENZYME KINETICS; ENZYMES; HYDROLYSIS;

ACTIVATION SIGNAL; N-TERMINAL SUBDOMAIN; TRANSLATION INITIATION;

PROTEINS;

ARGININE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 1; INITIATION FACTOR 2; INITIATION FACTOR 5; NUCLEIC ACID;

ALPHA CHAIN; AMINO TERMINAL SEQUENCE; ARTICLE; BETA CHAIN; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; HYDROLYSIS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; START CODON; TRANSLATION INITIATION;

EUKARYOTIC INITIATION FACTOR-1; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-5; EUKARYOTIC INITIATION FACTORS; GTPASE-ACTIVATING PROTEINS; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

ARCHAEA; EUKARYOTA;

EID: 33645677012     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052387u     Document Type: Article

References (60)

1. Dever, T. E. (2002) Gene-specific regulation by general translation factors, Cell 108, 545-556.
2. Kapp, L. D., and Lorsch, J. R. (2004) The molecular mechanics of eukaryotic translation, Annu. Rev. Biochem. 73, 657-704.
3. Sonenberg, N., and Dever, T. E. (2003) Eukaryotic translation initiation factors and regulators, Curr. Opin. Struct. Biol. 13, 56-63.
4. Paulin, F. E., Campbell, L. E., O'Brien, K., Loughlin, J., and Proud, C. G. (2001) Eukaryotic translation initiation factor 5 (eIF5) acts as a classical GTPase-activator protein, Curr. Biol. 11, 55-59.
5. Das, S., Ghosh, R., and Maitra, U. (2001) Eukaryotic translation initiation factor 5 functions as a GTPase-activating protein, J. Biol. Chem. 276, 6720-6726.
6. 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.
7. Maag, D., Fekete, C. A., Gryczynski, Z., and Lorsch, J. R. (2005) A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon, Mol. Cell 17, 265-275.
8. Majumdar, R., and Maitra, U. (2005) Regulation of GTP hydrolysis prior to ribosomal AUG selection during eukaryotic translation initiation, EMBO J. 24, 3737-3746.
9. Valasek, L., Nielsen, K. H., Zhang, F., Fekete, C. A., and Hinnebusch, A. G. (2004) Interactions of eukaryotic translation initiation factor 3 (eIF3) subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection, Mol. Cell. Biol. 24, 9437-9455.
10. Unbehaun, A., Borukhov, S. I., Hellen, C. U., and Pestova, T. V. (2004) Release of initiation factors from 48S complexes during ribosomal subunit joining and the link between establishment of codon-anticodon base-pairing and hydrolysis of eIF2-bound GTP, Genes Dev. 18, 3078-3093.
11. i release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation, Mol. Cell 20, 251-262.
12. Huang, H. K., Yoon, H., Hannig, E. M., and Donahue, T. F. (1997) GTP hydrolysis controls stringent selection of the AUG start codon during translation initiation in Saccharomyces cerevisiae, Genes Dev. 11, 2396-2413.
13. Yoon, H. J., and Donahue, T. F. (1992) The suil suppressor locus in Saccharomyces cerevisiae encodes a translation factor that functions during tRNA(iMet) recognition of the start codon, Mol. Cell. Biol. 12, 248-260.
14. Cui, Y., Dinman, J. D., Kinzy, T. G., and Peltz, S. W. (1998) The Mof2/Sui1 protein is a general monitor of translational accuracy, Mol. Cell. Biol. 18, 1506-1516.
15. Scheffzek, K., Ahmadian, M. R., and Wittinghofer, A. (1998) GTPase-activating proteins: Helping hands to complement an active site, Trends Biochem. Sci. 23, 257-262.
16. Ribera, I. L., Ruiz-Avila, L., and Puigdomenech, P. (1997) The eukaryotic translation initiation factor 5, eIF-5, a protein from Zea mays, containing a zinc-finger structure, binds nucleic acids in a zinc-dependent manner, Biochem. Biophys. Res. Commun. 236, 510-516.
17. Donahue, T. F., Cigan, A. M., Pabich, E. K., and Valavicius, B. C. (1988) Mutations at a Zn(II) finger motif in the yeast eIF-2β gene alter ribosomal start-site selection during the scanning process, Cell 54, 621-632.
18. Chantalat, L., Leroy, D., Filhol, O., Nueda, A., Benitez, M. J., Chambaz, E. M., Cochet, C., and Dideberg, O. (1999) Crystal structure of the human protein kinase CK2 regulatory subunit reveals its zinc finger-mediated dimerization, EMBO J. 18, 2930-2940.
19. Asano, K., Clayton, J., Shalev, A., and Hinnebusch, A. G. (2000) A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA(Met) is an important translation initiation intermediate in vivo, Genes Dev. 14, 2534-2546.
20. Asano, K., Shalev, A., Phan, L., Nielsen, K., Clayton, J., Valasek, L., Donahue, T. F., and Hinnebusch, A. G. (2001) Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation, EMBO J. 20, 2326-2337.
21. Bandyopadhyay, A., and Maitra, U. (1999) Cloning and characterization of the p42 subunit of mammalian translation initiation factor 3 (eIF3): Demonstration that eIF3 interacts with eIF5 in mammalian cells, Nucleic Acids Res. 27, 1331-1337.
22. Yamamoto, Y., Singh, C. R., Marintchev, A., Hall, N. S., Hannig, E. M., Wagner, G., and Asano, K. (2005) The eukaryotic initiation factor (eIF) 5 HEAT domain mediates multifactor assembly and scanning with distinct interfaces to eIF1, eIF2, eIF3, and eIF4G, Proc. Natl. Acad. Sci. U.S.A.
23. Asano, K., Krishnamoorthy, T., Phan, L., Pavitt, G. D., and Hinnebusch, A. G. (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.
24. Valasek, L., Mathew, A. A., Shin, B. S., Nielsen, K. H., Szamecz, B., and Hinnebusch, A. G. (2003) The yeast eIF3 subunits TIF32/a, NIP1/c, and eIF5 make critical connections with the 40S ribosome in vivo, Genes Dev. 17, 786-799.
25. Valasek, L., Nielsen, K. H., and Hinnebusch, A. G. (2002) Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo, EMBO J. 21, 5886-5898.
26. Phan, L., Zhang, X., Asano, K., Anderson, J., Vornlocher, H. P., Greenberg, J. R., Qin, J., and Hinnebusch, A. G. (1998) Identification of a translation initiation factor 3 (eIF3) core complex, conserved in yeast and mammals, that interacts with eIF5, Mol. Cell. Biol. 18, 4935-4946.
27. Pestova, T. V., and Kolupaeva, V. G. (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection, Genes Dev. 16, 2906-2922.
28. He, H., von der Haar, T., Singh, C. R., Ii, M., Li, B., Hinnebusch, A. G., McCarthy, J. E., and Asano, K. (2003) The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection, Mol. Cell. Biol. 23, 5431-5445.
29. Alfano, C., Sanfelice, D., Babon, J., Kelly, G., Jacks, A., Curry, S., and Conte, M. R. (2004) Structural analysis of cooperative RNA binding by the La motif and central RRM domain of human La protein, Nat. Struct. Mol. Biol. 11, 323-329.
30. Alfano, C., Babon, J., Kelly, G., Curry, S., and Conte, M. R. (2003) Resonance assignment and secondary structure of an N-terminal fragment of the human La protein, J. Biomol. NMR 27, 93-94.
31. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
32. Bartels, C., Xia, T., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer supported NMR spectral-analysis of biological macromolecules, J. Biomol. NMR 6, 1-10.
33. Fesik, S. W., and Zuiderweg, E. R. P. (1988) Heteronuclear 3-dimensional NMR spectroscopy. A strategy for the simplification of homo-nuclear two-dimensional NMR spectra, J. Magn. Reson. 78, 588-593.
34. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
35. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease, Biochemistry 28, 8972-8979.
36. Brünger, A. T. (1993) Yale University, New Haven, CT.
37. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55, 29-32.
38. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
39. Rückert, M., and Otting, G. (2000) Alignment of biological macromolecules in novel non-ionic liquid crystalline media for NMR experiments, J. Am. Chem. Soc. 122, 7793-7797.
40. Hansen, M. R., Mueller, L., and Pardi, A. (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions, Nat. Struct. Biol. 5, 1065-1074.
41. Ishii, Y., Markus, M. A., and Tycko, R. (2001) Controlling residual dipolar couplings in high-resolution NMR of proteins by strain induced alignment in a gel, J. Biomol. NMR 21, 141-151.
42. Sass, H. J., Musco, G., Stahl, S. J., Wingfield, P. T., and Grzesiek, S. (2000) Solution NMR of proteins within polyacrylamide gels: Diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes, J. Biomol. NMR 18, 303-309.
43. Gutierrez, P., Osborne, M. J., Siddiqui, N., Trempe, J. F., Arrowsmith, C., and Gehring, K. (2004) Structure of the archaeal translation initiation factor aIF2β from Methanobacterium thermoautotrophicum: Implications for translation initiation, Protein Sci. 13, 659-667.
44. Cho, S., and Hoffman, D. W. (2002) Structure of the β subunit of translation initiation factor 2 from the archaeon Methanococcus jannaschii: A representative of the eIF2β/eIF5 family of proteins, Biochemistry 41, 5730-5742.
45. Yao, J., Chung, J., Eliezer, D., Wright, P. E., and Dyson, H. J. (2001) NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding, Biochemistry 40, 3561-3571.
46. Thompson, G. M., Pacheco, E., Melo, E. O., and Castilho, B. A. (2000) Conserved sequences in the beta subunit of archaeal and eukaryal translation initiation factor 2 (eIF2), absent from eIF5, mediate interaction with eIF2γ, Biochem. J. 347 (part 3), 703-709.
47. Gamblin, S. J., and Smerdon, S. J. (1998) GTPase-activating proteins and their complexes, Curr. Opin. Struct. Biol. 8, 195-201.
48. Rittinger, K., Taylor, W. R., Smerdon, S. J., and Gamblin, S. J. (1998) Support for shared ancestry of GAPs, Nature 392, 448-449.
49. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2256-2268.
50. Jaravine, V. A., Nolde, D. E., Reibarkh, M. J., Korolkova, Y. V., Kozlov, S. A., Pluzhnikov, K. A., Grishin, E. V., and Arseniev, A. S. (1997) Three-dimensional structure of toxin OSK1 from Orthochirus scrobiculosus scorpion venom, Biochemistry 36, 1223-1232.
51. van Duyne, G. D., Ghosh, G., Maas, W. K., and Sigler, P. B. (1996) Structure of the oligomerization and L-arginine binding domain of the arginine repressor of Escherichia coli, J. Mol. Biol. 256, 377-391.
52. Musco, G., Kharrat, A., Stier, G., Fraternali, F., Gibson, T. J., Nilges, M., and Pastore, A. (1997) The solution structure of the first KH domain of FMR1, the protein responsible for the fragile X syndrome, Nat. Struct. Biol. 4, 712-716.
53. Fletcher, C. M., Pestova, T. V., Hellen, C. U., and Wagner, G. (1999) Structure and interactions of the translation initiation factor eIF1, EMBO J. 18, 2631-2637.
54. Qian, X., Gozani, S. N., Yoon, H., Jeon, C. J., Agarwal, K., and Weiss, M. A. (1993) Novel zinc finger motif in the basal transcriptional machinery: Three-dimensional NMR studies of the nucleic acid binding domain of transcriptional elongation factor TFIIS, Biochemistry 32, 9944-9959.
55. Hard, T., Rak, A., Allard, P., Kloo, L., and Garber, M. (2000) The solution structure of ribosomal protein L36 from Thermus thermophilus reveals a zinc-ribbon-like fold, J. Mol. Biol. 296, 169-180.
56. Zhu, W., Zeng, Q., Colangelo, C. M., Lewis, M., Summers, M. F., and Scott, R. A. (1996) The N-terminal domain of TFIIB from Pyrococcus furiosus forms a zinc ribbon, Nat. Struct. Biol. 3, 122-124.
57. Aravind, L., Anantharaman, V., Balaji, S., Babu, M. M., and Iyer, L. M. (2005) The many faces of the helix-turn-helix domain: Transcription regulation and beyond, FEMS Microbiol. Rev. 29, 231-262.
58. Biou, V., Shu, F., and Ramakrishnan, V. (1995) X-ray crystallography shows that translational initiation factor IF3 consists of two compact α/β domains linked by an α-helix, EMBO J. 14, 4056-4064.
59. Gross, J. D., Moerke, N. J., von der Haar, T., Lugovskoy, A. A., Sachs, A. B., McCarthy, J. E., and Wagner, G. (2003) Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E, Cell 115, 739-750.
60. Canagarajah, B., Leskow, F. C., Ho, J. Y., Mischak, H., Saidi, L. F., Kazanietz, M. G., and Hurley, J. H. (2004) Structural mechanism for lipid activation of the Rac-specific GAP, β2-chimaerin, Cell 119, 407-418.