Ribosomal localization of translation initiation factor IF2

RNA

Volumn 9, Issue 8, 2003, Pages 958-969

  Marzi, Stefano ^a,b   Knight, William ^b   Brandi, Letizia ^a,b   Caserta, Enrico ^a   Soboleva, Natalia ^a   Hill, Walter E ^b   Gualerzi, Claudio O ^a   Lodmell, J Stephen ^b  

^a UNIVERSITY OF CAMERINO   (Italy)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

BABE; fMet tRNA; IF2; Phenanthroline; Ribosome topography; Tethered nuclease; Translation initiation

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; INITIATION FACTOR 2; TRANSFER RNA;

ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; COMPUTER MODEL; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RNA STRUCTURE; TOPOGRAPHY; TRANSLATION INITIATION;

BACILLUS STEAROTHERMOPHILUS; BASE SEQUENCE; COMPUTER SIMULATION; CYSTEINE; HYDROLYSIS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROKARYOTIC INITIATION FACTOR-2; RIBOSOMES; RNA, RIBOSOMAL;

BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0041806480     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2116303     Document Type: Article

References (86)

1. Abel, K., Yoder, M.D., Hilgenfeld, R., and Jurnak, F. 1996. An α to β conformational switch in EF-Tu. Structure 4: 1153-1159.
2. Ævarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., al-Karadaghi, S., Svensson, L.A., and Liljas, A. 1994. Three-dimensional structure of the ribosomal translocase: Elongation factor G from Thermus thermophilus. EMBO J. 13: 3669-3677.
3. Agrawal, R.K., Penczek, P., Grassucci, R.A., and Frank, J. 1998. Visualization of elongation factor G on the Escherichia coli 70S ribosome: The mechanism of translocation. Proc. Natl. Acad. Sci. 95: 6134-6138.
4. Agrawal, R.K., Heagle, A.B., Penczek, P., Grassucci, R.A., and Frank, J. 1999. EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat. Struct. Biol. 6: 643-647.
5. al-Karadaghi, S., Aevarsson, A., Garber, M., Zheltonosova, J., and Liljas, A. 1996. The structure of elongation factor G in complex with GDP: Conformational flexibility and nucleotide exchange. Structure 4: 555-565.
6. Ban, N., Nissen, P., Hansen, J., Capel, M., Moore, P.B., and Steitz, T.A. 1999. Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit. Nature 400: 841-847.
7. Ban, N., Nissen, P., Hansen, J., Moore, P.B., and Steitz, T.A. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
8. Berchtold, H., Reshetnikova, L., Reiser, C.O., Schirmer, N.K., Sprinzl, M., and Hilgenfeld, R. 1993. Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365: 126-132.
9. 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.
10. Boelens, R. and Gualerzi, C.O. 2002. Stucture and function of bacterial initiation factors. Curr. Prot. Pep. Sci. 3: 107-119.
11. Boileau, G., Butler, P., Hershey, J.W., and Traut, R.R. 1983. Direct cross-links between initiation factors 1, 2, and 3 and ribosomal proteins promoted by 2-iminothiolane. Biochemistry 22: 3162-3170.
12. Bollen, A., Heimark, R.L., Cozzone, A., Traut, R.R., and Hershey, J.W. 1975. Cross-linking of initiation factor IF-2 to Escherichia coli 30 S ribosomal proteins with dimethylsuberimidate. J. Biol. Chem. 250: 4310-4314.
13. Bowen, W.S., Hill, W.E., and Lodmell, J.S. 2001, Comparison of rRNA cleavage by complementary 1,10-phenanthroline-Cu(II)- and EDTA-Fe(II)-derivatized oligonucleotides. Methods 25: 344-350.
14. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
15. Brock, S., Szkaradkiewicz, K., and Sprinzl, M. 1998. Initiation factors of protein biosynthesis in bacteria and their structural relationship to elongation and termination factors. Mol. Microbiol. 29: 409-417.
16. Brombach, M., Gualerzi, C.O., Nakamura, Y., and Pon, C.L. 1986. Molecular cloning and sequence of the Bacillus stearothermophilus translational initiation factor IF2 gene. Mol. Gen. Genet. 205: 97-102.
17. Cameron, D.M., Thompson, J., March, P.E., and Dahlberg, A.E. 2002. Initiation factor IF2, thiostrepton and micrococcin prevent the binding of elongation factor G to the Escherichia coli ribosome. J. Mol. Biol. 319: 27-35.
18. Carter, A.P., Clemons, W.M., Brodersen, D.E., Morgan-Warren, R.J., Wimberly, B.T., and Ramakrishnan, V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407: 340-348.
19. Carter, A.P., Clemons Jr., W.M., 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.
20. Cenatiempo, Y., Deville, F., Dondon, J., Grunberg-Manago, M., Sacerdot, C., Hershey, J.W., Hansen, H.F., Petersen, H.U., Clark, B.F., Kjeldgaard, M., et al. 1987. The protein synthesis initiation factor 2 G-domain. Study of a functionally active C-terminal 65-kilodalton fragment of IF2 from Escherichia coli. Biochemistry 26: 5070-5076.
21. Chen, C.B., Gorin, M.B., and Sigman, D.S. 1993. Sequence-specific scission of DNA by the chemical nuclease activity of 1,10-phenanthroline-copper(I) targeted by RNA. Proc. Natl. Acad. Sci. 90: 4206-4210.
22. Culver, G.M., Heilek, G.M., and Noller, H.F. 1999. Probing the rRNA environment of ribosomal protein S5 across the subunit interface and inside the 30 S subunit using tethered Fe(II). J. Mol. Biol. 286: 355-364.
23. Czworkowski, J., Wang, J., Steitz, T.A., and Moore, P.B. 1994. The crystal structure of elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J. 13: 3661-3668.
24. Dallas, A. and Noller, H.F. 2001. Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol. Cell 8: 855-864.
25. Garcia, C., Fortier, P.L., Blanquet, S., Lallemand, J.Y., and Dardel, F. 1995a. 1H and 15N resonance assignments and structure of the N-terminal domain of Escherichia coli initiation factor 3. Eur. J. Biochem. 228: 395-402.
26. -. 1995b. Solution structure of the ribosome-binding domain of E. coli translation initiation factor IF3. Homology with the U1A protein of the eukaryotic spliceosome. J. Mol. Biol. 254: 247-259.
27. 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.
28. Gualerzi, C.O., Severini, M., Spurio, R., La Teana, A., and Pon, C.L. 1991. Molecular dissection of translation initiation factor IF2. Evidence for two structural and functional domains. J. Biol. Chem. 266: 16356-16362.
29. Gualerzi, C.O., Brandi, L., Caserta, E., La Teana, A., Spurio, R., Tomsic, J., and Pon, C.L. 2000. Translation initiation in bacteria. In The ribosome: Structure, function, antibiotics, and cellular interactions (eds. R.A. Garrett et al.), pp. 477-494. ASM Press, Washington, D.C.
30. Gualerzi, C.O., Brandi, L., Caserta, E., Garofolo, C., Lammi, M., La Teana, A., Petrelli, D., Spurio, R., Tomsic, J., and Pon, C.L. 2001. Initiation factors in the early events of mRNA translation in bactera. Cold Spring Harbor Symp. Quant. Biol. 66: 363-376.
31. Guenneugues, M., Caserta, E., Brandi, L., Spurio, R., Meunier, S., Pon, C.L., Boelens, R., and Gualerzi, C.O. 2000. Mapping the fMet-tRNA(f)(Met) binding site of initiation factor IF2. EMBO J. 19: 5233-5240.
32. Guex, N and Peitsch, M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
33. Hall, K.B. and Fox, R.O. 1999. Directed cleavage of RNA with protein-tethered EDTA-Fe. Methods 18: 78-84.
34. Heilek, G.M. and Noller, H.F. 1996. Site-directed hydroxyl radical probing of the rRNA neighborhood of ribosomal protein S5. Science 272: 1659-1662.
35. Heilek, G.M., Marusak, R., Meares, C.F., and Noller, H.F. 1995. Directed hydroxyl radical probing of 16S rRNA using Fe(II) tethered to ribosomal protein S4. Proc. Natl. Acad. Sci. 92: 1113-1116.
36. Heimark, R.L., Kahan, L., Johnston, K., Hershey, J.W., and Traut, R.R. 1976. Cross-linking of initiation factor IF3 to proteins of the Escherichia coli 30 S ribosomal subunit. J. Mol. Biol. 105: 219-230.
37. Imlay, J.A. and Linn, S. 1988. DNA damage and oxygen radical toxicity. Science 240: 1302-1309.
38. Johnson, G.R.A. and Nazhat, N.B. 1987. Kinetics and mechanism of the reaction of the Bis(1,10-phenanthroline)copper(I) Ion with hydrogen peroxide in aqueous solution. J. Am. Chem. Soc. 109: 1990-1994.
39. Kawashima, T., Berthet-Colominas, C., Wulff, M., Cusack, S., and Leberman, R. 1996. The structure of the Escherichia coli EF-Tu.EF-Ts complex at 2.5 Å resolution. Nature 379: 511-518.
40. Kjeldgaard, M. and Nyborg, J. 1992. Refined structure of elongation factor EF-Tu from Escherichia coli. J. Mol. Biol. 223: 721-742.
41. Kjeldgaard, M., Nissen, P., Thirup, S., and Nyborg, J. 1993. The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1: 35-50.
42. Krafft, C., Diehl, A., Laettig, S., Behlke, J., Heinemann, U., Pon, C.L., Gualerzi, C.O., and Welfle, H. 2000. Interaction of fMet-tRNA(fMet) with the C-terminal domain of translational initiation factor IF2 from Bacillus stearothermophilus. FEBS Lett. 471: 128-132.
43. La Teana, A., Pon, C.L., and Gualerzi, C.O. 1993. Translation of mRNAs with degenerate initiation triplet AUU displays high initiation factor 2 dependence and is subject to initiation factor 3 repression. Proc. Natl. Acad. Sci. 90: 4161-4165.
44. La Teana, A., Gualerzi, C.O., and Dahlberg, A.E. 2001. Initiation factor IF 2 binds to the alpha-sarcin loop and helix 89 of Escherichia coli 23S ribosomal RNA. RNA 7: 1173-1179.
45. Lancaster, L., Kiel, M.C., Kaji, A., and Noller, H.F. 2002. Orientation of ribosome recycling factor in the ribosome from directed hydroxyl radical probing. Cell 111: 129-140.
46. 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. 24: 24.
47. Lieberman, K.R., Firpo, M.A., Herr, A.J., Nguyenle, T., Atkins, J.F., Gesteland, R.F., and Noller, H.F. 2000. The 23 S rRNA environment of ribosomal protein L9 in the 50 S ribosomal subunit. J. Mol. Biol. 297: 1129-1143.
48. Mazumder, A., Chen, C.B., Gaynor, R., and Sigman, D.S. 1992. 1,10-Phenanthroline-copper, a footprinting reagent for single-stranded regions of RNAS. Biochem. Biophys. Res. Commun. 187: 1503-1509.
49. McCutcheon, J.P., Agrawal, R.K., Philips, S.M., Grassucci, R.A., Gerchman, S.E., Clemons Jr., W.M., Ramakrishnan, V., and Frank, J. 1999. Location of translational initiation factor IF3 on the small ribosomal subunit. Proc. Natl. Acad. Sci. 96: 4301-4306.
50. Meunier, S., Spurio, R., Czisch, M., Wechselberger, R., Guenneugues, M., Gualerzi, C.O., and Boelens, R. 2000. Structure of the fMet-tRNA(fMet)-binding domain of B. stearothermophilus initiation factor IF2. EMBO J. 19: 1918-1926.
51. Misselwitz, R., Welfe, K., Krafft, C., Gualerzi, C.O., and Welfle, H. 1997. Translational initiation factor IF2 from Bacillus stearothermophilus: A spectroscopic and microcalorimetric study of the C-domain. Biochemistry 36: 3170-3178.
52. Misselwitz, R., Welfle, K., Krafft, C., Welfle, H., Brandi, L., Caserta, E., and Gualerzi, C.O. 1999. The fMet-tRNA binding domain of translational initiation factor IF2: Role and environment of its two Cys residues. FEBS Lett. 459: 332-336.
53. Moazed, D., Robertson, J.M., and Noller, H.F. 1988. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334: 362-364.
54. Moazed, D., Samaha, R.R., Gualerzi, C., and Noller, H.F. 1995. Specific protection of 16 S rRNA by translational initiation factors. J. Mol. Biol. 248: 207-210.
55. Moreno, J.M., Drskjotersen, L., Kristensen, J.E., Mortensen, K.K., and Sperling-Petersen, H.U. 1999. Characterization of the domains of E. coli initiation factor IF2 responsible for recognition of the ribosome. FEBS Lett. 455: 130-134.
56. Moreno, J.M., Sorensen, H.P., Mortensen, K.K., and Sperling-Petersen, H.U. 2000. Macromolecular mimicry in translation initiation: A model for the initiation factor IF2 on the ribosome. IUBMB Life 50: 347-354.
57. Moser, H.E. and Dervan, P.B. 1987. Sequence-specific cleavage of double helical DNA by triple helix formation. Science 238: 645-650.
58. Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., Reshetnikova, L., Clark, B.F., and Nyborg, J. 1995. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270: 1464-1472.
59. Nissen, P., Thirup, S., Kjeldgaard, M., and Nyborg, J. 1999. The crystal structure of Cys-tRNACys-EF-Tu-GDPNP reveals general and specific features in the ternary complex and in tRNA. Structure Fold Des. 7: 143-156.
60. Perrin, D.M., Mazumder, A., Sadeghi, F., and Sigman, D.S. 1994. Hybridization of a complementary ribooligonucleotide to the transcription start site of the lacUV-5-Escherichia coli RNA polymerase open complex. Potential for gene-specific inactivation reagents. Biochemistry 33: 3848-3854.
61. Pioletti, M., Schlunzen, F., Harms, J., Zarivach, R., Gluhmann, M., Avila, H., Bashan, A., Bartels, H., Auerbach, T., Jacobi, C., et al. 2001. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20: 1829-1839.
62. Polekhina, G., Thirup, S., Kjeldgaard, M., Nissen, P., Lippmann, C., and Nyborg, J. 1996. Helix unwinding in the effector region of elongation factor EF-Tu-GDP. Structure 4: 1141-1151.
63. Pon, C.L., Paci, M., Pawlik, R.T., and Gualerz, C.O. 1985. Structure-function relationship in Escherichia coli initiation factors. Biochemical and biophysical characterization of the interaction between IF-2 and guanosine nucleotides. J. Biol. Chem. 260: 8918-8924.
64. Pope, L.E. and Sigman, D.S. 1984. Secondary structure specificity of the nuclease activity of the 1,10-phenanthroline-copper complex. Proc. Natl. Acad. Sci. 81: 3-7.
65. Rana, T.M. and Meares, C.F. 1991. Transfer of oxygen from an artificial protease to peptide carbon during proteolysis. Proc. Natl. Acad. Sci. 88: 10578-10582.
66. Riddles, P.W., Blakeley, R.L., and Zerner, B. 1983. Reassessment of Ellman's reagent. Methods Enzymol. 91: 49-60.
67. Rodnina, M.V., Semenkov, Y.P., and Wintermeyer, W. 1994. Purification of fMet-tRNA(fMet) by fast protein liquid chromatography. Anal. Biochem. 219: 380-381.
68. 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.
69. 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.
70. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102: 615-623.
71. Selmer, M., Al-Karadaghi, S., Hirokawa, G., Kaji, A., and Liljas, A. 1999. Crystal structure of Thermotoga maritima ribosome recycling factor:Aa tRNA mimic. Science 286: 2349-2352.
72. 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.
73. Severini, M., Choli, T., La Teana, A., and Gualerzi, C.O. 1992. Proteolysis of Bacillus stearothermophilus IF2 and specific protection by fMet-tRNA. FEBS Lett. 297: 226-228.
74. Spurio, R., Brandi, L., Caserta, E., Pon, C.L., Gualerzi, C.O., Misselwitz, R., Krafft, C., Welfle, K., and Welfle, H. 2000. The C-terminal subdomain (IF2 C-2) contains the entire fMet-tRNA binding site of initiation factor IF2. J. Biol. Chem. 275: 2447-2454.
75. Stark, H., Rodnina, M.V., Rinke-Appel, J., Brimacombe, R., Wintermeyer, W., and van Heel, M. 1997. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389: 403-406.
76. Stark, H., Rodnina, M.V., Wieden, H.J., van Heel, M., and Wintermeyer, W. 2000. Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100: 301-309.
77. Tomsic, J. 2002. "Role of IF2 dependent GTPase during late events of procaryotic translation initiation." Ph.D. thesis, University of Camerino, Camerino, Italy.
78. Tomsic, J., Vitali, L.A., Daviter, T., Savelsbergh, A., Spurio, R., Striebeck, P., Wintermeyer, W., Rodnina, M.V., and Gualerzi, C.O. 2000. Late events of translation initiation in bacteria: A kinetic analysis. EMBO J. 19: 2127-2136.
79. Vestergaard, B., Van, L.B., Andersen, G.R., Nyborg, J., Buckingham, R.H., and Kjeldgaard, M. 2001. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell 8: 1375-1382.
80. Wakao, H., Romby, P., Westhof, E., Laalami, S., Grunberg-Manago, M., Ebel, J.P., Ehresmann, C., and Ehresmann, B. 1989. The solution structure of the Escherichia coli initiator tRNA and its interactions with initiation factor 2 and the ribosomal 30 S subunit. J. Biol. Chem. 264: 20363-20371.
81. Wakao, H., Romby, P., Laalami, S., Ebel, J.P., Ehresmann, C., and Ehresmann, B. 1990. Binding of initiation factor 2 and initiator tRNA to the Escherichia coli 30S ribosomal subunit induces allosteric transitions in 16S rRNA. Biochemistry 29: 8144-8151.
82. Wakao, H., Romby, P., Ebel, J.P., Grunberg-Manago, M., Ehresmann, C., and Ehresmann, B. 1991. Topography of the Escherichia coli ribosomal 30S subunit-initiation factor 2 complex. Biochimie 73: 991-1000.
83. Wilson, K.S. and Noller, H.F. 1998. Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing. Cell 92: 131-139.
84. Wimberly, B.T., Brodersen, D.E., Clemons Jr., W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
85. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H., and Noller, H.F. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.
86. Yusupova, G., Reinbolt, J., Wakao, H., Laalami, S., Grunberg-Manago, M., Romby, P., Ehresmann, B., and Ehresmann, C. 1996. Topography of the Escherichia coli initiation factor 2/fMet-tRNA(f) (Met) complex as studied by cross-linking. Biochemistry 35: 2978-2984.