Structural insights on the translation initiation complex: Ghosts of a universal initiation complex

Molecular Microbiology

Volumn 63, Issue 4, 2007, Pages 941-950

  Allen, Gregory S ^a   Frank, Joachim ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 1A; INITIATION FACTOR 5B; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; BACTERIUM; CRYOELECTRON MICROSCOPY; EUKARYOTE; GENOMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RIBOSOME; SHORT SURVEY; TRANSLATION INITIATION; X RAY;

BACTERIA; EUKARYOTIC INITIATION FACTORS; MULTIPROTEIN COMPLEXES; PEPTIDE INITIATION FACTORS; PROKARYOTIC INITIATION FACTOR-2; PROTEIN CONFORMATION;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 33846625924     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05574.x     Document Type: Short Survey

References (93)

1. Acker, M.G., Shin, B.S., Dever, T.E., and Lorsch, J.R. (2006) Interaction between eukaryotic initiation factors 1A and 5B is required for efficient ribosomal subunit joining. J Biol Chem 281: 8469-8475.
2. Algire, M.A., Maag, D., and Lorsch, J.R. (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.
3. Allen, G.S., Zavialov, A., Gursky, R., Ehrenberg, M., and Frank, J. (2005) The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121: 703-712.
4. Andreev, D.E., Terenin, I.M., Dunaevsky, Y.E., Dmitriev, S.E., and Shatsky, I.N. (2006) A leaderless mRNA can bind to mammalian 80S ribosomes and direct polypeptide synthesis in the absence of translation initiation factors. Mol Cell Biol 26: 3164-3169.
5. Antoun, A., Pavlov, M.Y., Andersson, K., Tenson, T., and Ehrenberg, M. (2003) The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis. EMBO J 22: 5593-5601.
6. Antoun, A., Pavlov, M.Y., Tenson, T., and Ehrenberg, M.M. (2004) Ribosome formation from subunits studied by stopped-flow and Rayleigh light scattering. Biol Proced Online 6: 35-54.
7. Antoun, A., Pavlov, M.Y., Lovmar, M., and Ehrenberg, M. (2006) How initiation factors tune the rate of initiation of protein synthesis in bacteria. EMBO J 25: 2539-2550.
8. Battiste, J.L., Pestova, T.V., Hellen, C.U., and Wagner, G. (2000) The eIF1A solution structure reveals a large RNA-binding surface important for scanning function. Mol Cell 5: 109-119.
9. Benner, S.A., Ellington, A.D., and Tauer, A. (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86: 7054-7058.
10. Blum, S., Schmid, S.R., Pause, A., Buser, P., Linder, P., Sonenberg, N., and Trachsel, H. (1992) ATP hydrolysis by initiation factor 4A is required for translation initiation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89: 7664-7668.
11. Caetano-Anolles, G. (2002) Tracing the evolution of RNA structure in ribosomes. Nucleic Acids Res 30: 2575-2587.
12. Carter, A.P., Clemons, W.M., Jr, Brodersen, D.E., Morgan-Warren, R.J., Hartsch, T., Wimberly, B.T., and Ramakrishnan, V. (2001) Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291: 498-501.
13. Caserta, E., Tomsic, J., Spurio, R., La Teana, A., Pon, C.L., and Gualerzi, C.O. (2006) Translation initiation factor IF2 interacts with the 30 S ribosomal subunit via two separate binding sites. J Mol Biol 362: 787-799.
14. Celano, B., Pawlik, R.T., and Gualerzi, C.O. (1988) Interaction of Escherichia coli translation-initiation factor IF-1 with ribosomes. Eur J Biochem 178: 351-355.
15. Chaires, J.B., Pande, C., and Wishnia, A. (1981) The effect of initiation factor IF-3 on Escherichia coli ribosomal subunit association kinetics. J Biol Chem 256: 6600-6607.
16. Chang, B., Halgamuge, S., and Tang, S.L. (2006) Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SD-led genes. Gene 373: 90-99.
17. Choi, S.K., Olsen, D.S., Roll-Mecak, A., Martung, A., Remo, K.L., Burley, S.K., et al. (2000) Physical and functional interaction between the eukaryotic orthologs of prokaryotic translation initiation factors IF1 and IF2. Mol Cell Biol 20: 7183-7191.
18. Choi, S.Y., Scherer, B.J., Schnier, J., Davies, M.V., Kaufman, R.J., and Hershey, J.W. (1992) Stimulation of protein synthesis in COS cells transfected with variants of the alpha-subunit of initiation factor eIF-2. J Biol Chem 267: 286-293.
19. Dallas, A., and Noller, H.F. (2001) Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol Cell 8: 855-864.
20. Dever, T.E. (1999) Translation initiation: adept at adapting. Trends Biochem Sci 24: 398-403.
21. Fekete, C.A., Applefield, D.J., Blakely, S.A., Shirokikh, N., Pestova, T., Lorsch, J.R., and Hinnebusch, A.G. (2005) The eIF1A C-terminal domain promotes initiation complex assembly, scanning and AUG selection in vivo. EMBO J 24: 3588-3601.
22. Gingras, A.C., Raught, B., and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963.
23. Grill, S., Gualerzi, C.O., Londei, P., and Blasi, U. (2000) Selective stimulation of translation of leaderless mRNA by initiation factor 2: evolutionary implications for translation. EMBO J 19: 4101-4110.
24. Grill, S., Moll, I., Giuliodori, A.M., Gualerzi, C.O., and Blasi, U. (2002) Temperature-dependent translation of leaderless and canonical mRNAs in Escherichia coli. FEMS Microbiol Lett 211: 161-167.
25. Grunberg-Manago, M., Dessen, P., Pantaloni, D., Godefroy-Colburn, T., Wolfe, A.D., and Dondon, J. (1975) Light-scattering studies showing the effect of initiation factors on the reversible dissociation of Escherichia coli ribosomes. J Mol Biol 94: 461-478.
26. Gualerzi, C.O., and Pon, C.L. (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29: 5881-5889.
27. Guenneugues, M., Caserta, E., Brandi, L., Spurio, R., Meunier, S., Pon, C.L., et al. (2000) Mapping the fMet-tRNA (f) (Met) binding site of initiation factor IF2. EMBO J 19: 5233-5240.
28. Guillon, L., Schmitt, E., Blanquet, S., and Mechulam, Y. (2005) Initiator tRNA binding by e/aIF5B, the eukaryotic/archaeal homologue of bacterial initiation factor IF2. Biochemistry 44: 15594-15601.
29. Harris, J.K., Kelley, S.T., Spiegelman, G.B., and Pace, N.R. (2003) The genetic core of the universal ancestor. Genome Res 13: 407-412.
30. Hartz, D., Binkley, J., Hollingsworth, T., and Gold, L. (1990) Domains of initiator tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3. Genes Dev 4: 1790-1800.
31. Hasenohrl, D., Benelli, D., Barbazza, A., Londei, P., and Blasi, U. (2006) Sulfolobus solfataricus translation initiation factor 1 stimulates translation initiation complex formation. RNA 12: 674-682.
32. Hirashima, A., and Kaji, A. (1972) Factor-dependent release of ribosomes from messenger RNA. Requirement for two heat-stable factors. J Mol Biol 65: 43-58.
33. Jivotovskaya, A.V., Valasek, L., Hinnebusch, A.G., and Nielsen, K.H. (2006) Eukaryotic translation initiation factor 3 (eIF3) and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol Cell Biol 26: 1355-1372.
34. Karimi, R., Pavlov, M.Y., Buckingham, R.H., and Ehrenberg, M. (1999) Novel roles for classical factors at the interface between translation termination and initiation. Mol Cell 3: 601-609.
35. Kolakofsky, D., Ohta, T., and Thach, R.E. (1968) Junction of the 50S ribosomal subunit with the 30S initiation complex. Nature 220: 244-247.
36. Kozak, M. (1989) The scanning model for translation: an update. J Cell Biol 108: 229-241.
37. Kozak, M. (2005) Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361: 13-37.
38. Krafft, C., Diehl, A., Laettig, S., Behlke, J., Heinemann, U., Pon, C.L., et al. (2000) Interaction of fMet-tRNA (fMet) with the C-terminal domain of translational initiation factor IF2 from Bacillus stearothermophilus. FEBS Lett 471: 128-132.
39. Kyrpides, N.C., and Woese, C.R. (1998) Universally conserved translation initiation factors. Proc Natl Acad Sci USA 95: 224-228.
40. Laursen, B.S., Mortensen, K.K., Sperling-Petersen, H.U., and Hoffman, D.W. (2003) A conserved structural motif at the N terminus of bacterial translation initiation factor IF2. J Biol Chem 278: 16320-16328.
41. Laursen, B.S., Kjaergaard, A.C., Mortensen, K.K., Hoffman, D.W., and Sperling-Petersen, H.U. (2004) The N-terminal domain (IF2N) of bacterial translation initiation factor IF2 is connected to the conserved C-terminal domains by a flexible linker. Protein Sci 13: 230-239.
42. Laursen, B.S., Sorensen, H.P., Mortensen, K.K., and Sperling-Petersen, H.U. (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69: 101-123.
43. Lee, J.H., Pestova, T.V., Shin, B.S., Cao, C., Choi, S.K., and Dever, T.E. (2002) Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation. Proc Natl Acad Sci USA 99: 16689-16694.
44. Li, W., and Hoffman, D.W. (2001) Structure and dynamics of translation initiation factor aIF-1A from the archaeon Methanococcus jannaschii determined by NMR spectroscopy. Protein Sci 10: 2426-2438.
45. Lockwood, A.H., Chakraborty, P.R., and Maitra, U. (1971) A complex between initiation factor IF2, guanosine triphosphate, and fMet-tRNA: an intermediate in initiation complex formation. Proc Natl Acad Sci USA 68: 3122-3126.
46. Lomakin, I.B., Kolupaeva, V.G., Marintchev, A., Wagner, G., and Pestova, T.V. (2003) Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes Dev 17: 2786-2797.
47. Lomakin, I.B., Shirokikh, N.E., Yusupov, M.M., Hellen, C.U., and Pestova, T.V. (2006) The fidelity of translation initiation: reciprocal activities of eIF1, IF3 and YciH. EMBO J 25: 196-210.
48. Londei, P. (2005) Evolution of translational initiation: new insights from the archaea. FEMS Microbiol Rev 29: 185-200.
49. Luchin, S., Putzer, H., Hershey, J.W., Cenatiempo, Y., Grunberg-Manago, M., and Laalami, S. (1999) In vitro study of two dominant inhibitory GTPase mutants of Escherichia coli translation initiation factor IF2. Direct evidence that GTP hydrolysis is necessary for factor recycling. J Biol Chem 274: 6074-6079.
50. Maag, D., and Lorsch, J.R. (2003) Communication between eukaryotic translation initiation factors 1 and 1A on the yeast small ribosomal subunit. J Mol Biol 330: 917-924.
51. 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.
52. Majumdar, R., Bandyopadhyay, A., and Maitra, U. (2003) Mammalian translation initiation factor eIF1 functions with eIF1A and eIF3 in the formation of a stable 40 S preinitiation complex. J Biol Chem 278: 6580-6587.
53. Marck, C., and Grosjean, H. (2002) tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8: 1189-1232.
54. Marintchev, A., and Wagner, G. (2004) Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 37: 197-284.
55. Marintchev, A., Kolupaeva, V.G., Pestova, T.V., and Wagner, G. (2003) Mapping the binding interface between human eukaryotic initiation factors 1A and 5B: a new interaction between old partners. Proc Natl Acad Sci USA 100: 1535-1540.
56. Marzi, S., Knight, W., Brandi, L., Caserta, E., Soboleva, N., Hill, W.E., et al. (2003) Ribosomal localization of translation initiation factor IF2. RNA 9: 958-969.
57. Mears, J.A., Cannone, J.J., Stagg, S.M., Gutell, R.R., Agrawal, R.K., and Harvey, S.C. (2002) Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol 321: 215-234.
58. Meinnel, T., Sacerdot, C., Graffe, M., Blanquet, S., and Springer, M. (1999) Discrimination by Escherichia coli initiation factor IF3 against initiation on non-canonical codons relies on complementarity rules. J Mol Biol 290: 825-837.
59. Moll, I., Grill, S., Gualerzi, C.O., and Blasi, U. (2002) Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43: 239-246.
60. Moll, I., Hirokawa, G., Kiel, M.C., Kaji, A., and Blasi, U. (2004) Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res 32: 3354-3363.
61. Myasnikov, A.G., Marzi, S., Simonetti, A., Giuliodori, A.M., Gualerzi, C.O., Yusupova, G., et al. (2005) Conformational transition of initiation factor 2 from the GTP- to GDP-bound state visualized on the ribosome. Nat Struct Mol Biol 12: 1145-1149.
62. O'Donnell, S.M., and Janssen, G.R. (2002) Leaderless mRNAs bind 70S ribosomes more strongly than 30S ribosomal subunits in Escherichia coli. J Bacteriol 184: 6730-6733.
63. Ogawa, K., and Kaji, A. (1975) Requirement for ribosome-releasing factor for the release of ribosomes at the termination codon. Eur J Biochem 58: 411-419.
64. Olsen, D.S., Savner, E.M., Mathew, A., Zhang, F., Krishnamoorthy, T., Phan, L., and Hinnebusch, A.G. (2003) Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J 22: 193-204.
65. Pedulla, N., Palermo, R., Hasenohrl, D., Blasi, U., Cammarano, P., and Londei, P. (2005) The archaeal eIF2 homologue: functional properties of an ancient translation initiation factor. Nucleic Acids Res 33: 1804-1812.
66. Peske, F., Rodnina, M.V., and Wintermeyer, W. (2005) Sequence of steps in ribosome recycling as defined by kinetic analysis. Mol Cell 18: 403-412.
67. Pestova, T.V., and Hellen, C.U. (2001) Functions of eukaryotic factors in initiation of translation. Cold Spring Harb Symp Quant Biol 66: 389-396.
68. 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.
69. Pestova, T.V., Lomakin, I.B., Lee, J.H., Choi, S.K., Dever, T.E., and Hellen, C.U. (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403: 332-335.
70. Petrelli, D., LaTeana, A., Garofalo, C., Spurio, R., Pon, C.L., and Gualerzi, C.O. (2001) Translation initiation factor IF3: two domains, five functions, one mechanism? EMBO J 20: 4560-4569.
71. Pisarev, A.V., Kolupaeva, V.G., Pisareva, V.P., Merrick, W.C., Hellen, C.U., and Pestova, T.V. (2006) Specific functional interactions of nucleotides at key -3 and +4 positions flanking the initiation codon with components of the mammalian 48S translation initiation complex. Genes Dev 20: 624-636.
72. Poyry, T.A., Kaminski, A., and Jackson, R.J. (2004) What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev 18: 62-75.
73. Rich, A. (1962) On the problems of evolution and biochemical information transfer. In Horizons in Biochemistry. Kasha, M., and Pullmann, B. (eds). New York: Academic Press, pp. 103-126.
74. Rodnina, M.V., Stark, H., Savelsbergh, A., Wieden, H.J., Mohr, D., Matassova, N.B., et al. (2000) GTPases mechanisms and functions of translation factors on the ribosome. Biol Chem 381: 377-387.
75. Roll-Mecak, A., Cao, C., Dever, T.E., and Burley, S.K. (2000) X-Ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103: 781-792.
76. Roll-Mecak, A., Shin, B.S., Dever, T.E., and Burley, S.K. (2001) Engaging the ribosome: universal IFs of translation. Trends Biochem Sci 26: 705-709.
77. Sacerdot, C., Vachon, G., Laalami, S., Morel-Deville, F., Cenatiempo, Y., and Grunberg-Manago, M. (1992) Both forms of translational initiation factor IF2 (alpha and beta) are required for maximal growth of Escherichia coli. Evidence for two translational initiation codons for IF2 beta. J Mol Biol 225: 67-80.
78. Seshadri, A., and Varshney, U. (2006) Mechanism of recycling of post-termination ribosomal complexes in eubacteria: a new role of initiation factor 3. J Biosci 31: 281-289.
79. Sette, M., van Tilborg, P., Spurio, R., Kaptein, R., Paci, M., Gualerzi, C.O., and Boelens, R. (1997) The structure of the translational initiation factor IF1 from E. coli contains an oligomer-binding motif. EMBO J 16: 1436-1443.
80. She, Q., Singh, R.K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M.J., et al. (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA 98: 7835-7840.
81. Shin, B.S., Maag, D., Roll-Mecak, A., Arefin, M.S., Burley, S.K., Lorsch, J.R., and Dever, T.E. (2002) Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell 111: 1015-1025.
82. Slupska, M.M., King, A.G., Fitz-Gibbon, S., Besemer, J., Borodovsky, M., and Miller, J.H. (2001) Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. J Mol Biol 309: 347-360.
83. Sokabe, M., Yao, M., Sakai, N., Toya, S., and Tanaka, I. (2006) Structure of archaeal translational initiation factor 2 betagamma-GDP reveals significant conformational change of the beta-subunit and switch 1 region. Proc Natl Acad Sci USA 103: 13016-13021.
84. Studer, S.M., and Joseph, S. (2006) Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol Cell 22: 105-115.
85. Sussman, J.K., Simons, E.L., and Simons, R.W. (1996) Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Mol Microbiol 21: 347-360.
86. Tahara, M., Ohsawa, A., Saito, S., and Kimura, M. (2004) In vitro phosphorylation of initiation factor 2 alpha (aIF2 alpha) from hyperthermophilic archaeon Pyrococcus horikoshii OT3. J Biochem (Tokyo) 135: 479-485.
87. Tolstrup, N., Sensen, C.W., Garrett, R.A., and Clausen, I.G. (2000) Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus. Extremophiles 4: 175-179.
88. Udagawa, T., Shimizu, Y., and Ueda, T. (2004) Evidence for the translation initiation of leaderless mRNAs by the intact 70 S ribosome without its dissociation into subunits in eubacteria. J Biol Chem 279: 8539-8546.
89. 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.
90. Weiel, J., and Hershey, J.W. (1982) The binding of fluorescein-labeled protein synthesis initiation factor 2 to Escherichia coli 30 S ribosomal subunits determined by fluorescence polarization. J Biol Chem 257: 1215-1220.
91. Wintermeyer, W., and Gualerzi, C. (1983) Effect of Escherichia coli initiation factors on the kinetics of N-Acphe-tRNAPhe binding to 30S ribosomal subunits. A fluorescence stopped-flow study. Biochemistry 22: 690-694.
92. Zavialov, A.V., Hauryliuk, V.V., and Ehrenberg, M. (2005) Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G. Mol Cell 18: 675-686.
93. Zucker, F.H., and Hershey, J.W. (1986) Binding of Escherichia coli protein synthesis initiation factor IF1-30S ribosomal subunits measured by fluorescence polarization. Biochemistry 25: 3682-3690.