Identification of the ribosome binding sites of translation initiation factor IF3 by multidimensional heteronuclear NMR spectroscopy

RNA

Volumn 5, Issue 1, 1999, Pages 82-92

  Sette, Marco ^a,c   Spurio, Roberto ^b   Van Tilborg, Paul ^a   Gualerzi, Claudio O ^b   Boelens, Rolf ^c  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF CAMERINO   (Italy)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

30S ribosomes; NMR titrations; Protein domains; Protein synthesis; RNA protein interaction

Indexed keywords

INITIATION FACTOR 3; RNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN SYNTHESIS REGULATION; RIBOSOME SUBUNIT; TRANSLATION REGULATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; ESCHERICHIA COLI; EUKARYOTIC INITIATION FACTOR-3; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE INITIATION FACTORS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RIBONUCLEOPROTEINS; RIBOSOMES; RNA-BINDING PROTEINS;

ESCHERICHIA COLI;

EID: 0032899119     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1355838299981487     Document Type: Article

References (55)

1. Aevarsson A, Brazhnikov E, Garber M, Zheltonosova J, Chirgadze Yu, Al-Karadaghi S, Svensson LA, Liljas A. 1994. Three-dimensional structure of the ribosomal translocase: Elongation factor G from Thermus thermophilus. EMBO J 13:3669-3677.
2. Allain F-HT, Howe PWA, Neuhaus D, Varani G. 1997. Structural basis of the RNA-binding specificity of human U1A protein. EMBO J 16:5764-5774.
3. Biou V, Shu F, 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.
4. Brombach M, Pon C. 1987. The unusual translational initiation codon AUU limits the expression of the infC (initiation factor 3) gene of Escherichia coli. Mol Gen Genet 208:94-100.
5. Bruhns J, Gualerzi C. 1980. Structure-function relationship in Escherichia coli initiation factors: Role of tyrosine residues in ribosomal binding and functional activity of IF-3. Biochemistry 19: 1670-1676.
6. Brünger AT. 1992. X-PLOR. A system for X-ray crystallography and NMR. New Haven, Connecticut: Yale University Press.
7. Czworkowski J, Wang J, Steitz TA, Moore PB. 1994. The crystal structure of elongation factor G complexed with GDP at 2.7 Å. EMBO J 13:3661-3668.
8. De Bellis D, Liveris D, Goss D, Ringquist S, Schwartz I. 1992. Structure-function analysis of Escherichia coli translation initiation factor IF3: Tyrosine 107 and lysine 110 are required for ribosome binding. Biochemistry 31:11984-11990.
9. Ehresmann C, Moine H, Mougel M, Dondon J, Grunberg-Manago M, Ebel JP, Ehresmann B. 1986. Cross-linking of initiation factor IF3 to E. coli 30S ribosomal subunit by trans-diamminedichloroplatinum (II): Characterization of two cross-linking sites in 16S rRNA; a possible way of functioning for IF3. Nucleic Acids Res 14:4803-4821.
10. Firpo MA, Connelly MB, Gross DJ, Dahlberg AE. 1996. Mutation at two invariant nucleotides in the 3'-minor domain of E. coli 16S rRNA affecting translation initiation and initiation factor 3 function. J Biol Chem 271:4693-4698.
11. Fortier PL, Schmitter JM, Garcia C, Dardel F. 1994. The N-terminal half of initiation factor IF3 is folded as a stable independent domain. Biochimie 76:376-383.
12. 15N resonance assignments and structure of the N-terminal domain of Escherichia coli initiation factor 3. Eur J Biochem 228:395-402.
13. Garcia C, Fortier PL, Blanquet S, Lallemand JY, Dardel F. 1995b. Solution structure of the ribosome-binding domain of E. coli translation initiation factor 3. Homology with the U1A protein of the eukaryotic spliceosome. J Mol Biol 254:247-259.
14. Gualerzi CO, Pon CL. 1990. Initiation of mRNA translation in prokaryotes. Biochemistry 29:5881-5889.
15. Gualerzi CO, Pon CL, Kaji A. 1971. Initiation factor dependent release of aminoacyl-tRNAs from complexes of 30S ribosomal subunits, synthetic polynucleotide and aminoacyl tRNA. Biochem Biophys Res Comm 45:1312-1319.
16. Gualerzi CO, Risuleo G, Pon CL. 1977. Initial rate kinetic analysis of the mechanism of initiation complex formation and the role of initiation factor IF3. Biochemistry 16:1684-1689.
17. Haggerty TJ, Lovett ST. 1993. Suppression of recJ mutations of E. coli by mutations in translation initiation factor IF3. J Bacteriol 175:6118-6125.
18. Hartz D, Binkley J, Hollinsworth T, Gold L. 1990. Domains of the initiator tRNA and initiation codon crucial for tRNA selection by E. coli IF3. Genes & Dev 4:1790-1800.
19. Hartz D, McPheeters DS, Gold L. 1989. Selection of the initiator tRNA by E. coli initiation factors. Genes & Dev 3:1899-1912.
20. Hershey JWB. 1987. Protein synthesis. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE, eds. Escherichia coli and Salmonella typhimurium: Cellular and molecular biology. Washington, DC: American Society for Microbiology, pp 613-647.
21. Holm L, Sander C. 1993. Protein structure comparison by alignment of distance matrices. J Mol Biol 233:123-138.
22. Klimasauskas S, Kumar S, Roberts RJ, Cheng X. 1994. Hhal methyltransferase flips its target base out of the DNA helix. Cell 76:357-369.
23. Koradi R, Billeter M, Wüthrich K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graph 14:51-55.
24. Kycia JH, Biou V, Shu F, Gerchman SE, Graziano V, Ramakrishnam V. 1995. Prokaryotic translation initiation factor IF3 is an elongated protein consisting of two crystallizable domains. Biochemistry 34:6183-6187.
25. Lahm A, Suck D. 1991. DNase I-induced DNA conformation. 2. A structure of a DNase l-octamer complex. J Mol Biol 221:645-667.
26. 1H NMR spectroscopic study on the involvement of the His residue in the interaction between IF3 and ribosomes. Biochem Int 5:429-436.
27. 2-terminal cleavage of Escherichia coli translational initiation factor IF3. FEBS Lett 215:115-121.
28. LaTeana A, Gualerzi CO, Brimacombe R. 1995. From stand-by to decoding site: Adjustment of the mRNA on the 30S ribosomal subunit under the influence of the initiation factors. RNA 1:772-782.
29. LaTeana A, Pon CL, Gualerzi CO. 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 USA 90:4161-4165.
30. McCarthy JEG, Gualerzi C. 1990. Translational control of prokaryotic gene expression. Trends Genet 6:78-85.
31. Moazed D, Samaha RR, Gualerzi C, Noller HF. 1995. Specific protection of 16S rRNA by translational initiation factors. J Mol Biol 248:207-210.
32. Moreau M, de Cock E, Fortier PL, Garcia C, Albaret C, Blanquet S, Lallemand JY, Dardel F. 1997. Heteronuclear NMR studies of E. coli translation initiation facotor IF3. Evidence that the inter-domain region is disordered in solution. J Mol Biol 266:15-22.
33. Mueller F, Brimacombe R. 1997. A new model for the three-dimensional folding of Escherichia coli 16S ribosomal RNA. II. The RNA-protein interaction data. J Mol Biol 271:545-565.
34. Muralikrishna P, Wickstrom E. 1989. Escherichia coli initiation factor 3 protein binding to 30S ribosomal subunits alters the accessibility of nucleotides within the conserved central region of 16S rRNA. Biochemistry 28:7505-7510.
35. Nureki O, Vassylyev DG, Katayanagi K, Shimizu T, Sekine S, Kigawa T, Miyazawa T, Yokoyama S, Morikawa K. 1995. Architectures of class-defining and specific domains of glutamyl-tRNA synthetase. Science 267:1958-1965.
36. Ohsawa H, Gualerzi C. 1981. Structure-function relationship in Escherichia coli initiation factor. Identification of a lysine residue in the ribosomal binding site of initiation factor by site-specific chemical modification with pyridoxal phosphate. J Biol Chem 256:4905-4912.
37. Olsson CL, Graffe M, Springer M, Hershey JWB. 1996. Physiological effects of translational initiation factor IF3 and ribosomal protein L20 limitation in E. coli. Mol Gen Genet 250:705-714.
38. Oubridge C, Ito N, Evans PR, Teo C-H, Nagai K. 1994. Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372:432-438.
39. 1H-n.m.r. study of the interaction between initiation factor IF1 and 30S ribosomal subunits. EMBO J 2:521-526.
40. 1H NMR spectroscopy. J Biol Chem 260:887-892.
41. Pawlik RT, Littlechild J, Pon CL, Gualerzi C. 1981. Purification and properties of Escherichia coli translational initiation factors. Biochem Int 2:421-428.
42. Petrelli D, Lammi M, Spurio R, Gualerzi CO, Pon CL. 1998. Mutagenesi sito-diretta della Arginine del dominio C del tattore d'inizio della sintesi proteica IF3. Atti Convegno Congiunto FISV, Oct. 1-4, Montesilvano, Italy, p 57.
43. Pon C, Cannistraro S, Giovane A, Gualerzi C. 1982a. Structure-function relationship in Escherichia coli initiation factors. Environment of the Cys residue and evidence for a hydrophobic region in initiation factor IF3 by fluorescence and ESR spectroscopy. Arch Biochem Biophys 217:47-57.
44. Pon CL, Gualerzi CO. 1974. Effect of initiation factor 3 binding on the 30S ribosomal subunits of Escherichia coli. Proc Natl Acad Sci USA 71:4950-4954.
45. Pon CL, Pawlik RT, Gualerzi C. 1982b. The topographical localization of IF3 on Escherichia coli 30S ribosomal subunits as a clue to its way of functioning. FEBS Lett 137:163-167.
46. Risuleo G, Gualerzi C, Pon C. 1976. Specificity and properties of the destabilization, induced by initiation factor IF3, of ternary complexes of the 30S ribosomal subunit, aminoacyl-tRNA and poly-nucleotides. Eur J Biochem 67:603-613.
47. Sacerdot C, Chiaruttini C, Engst K, Graffe M, Milet M, Mathy N, Dondon J, Springer M. 1996. The role of the AUU initiation codon in the negative feedback regulation of the gene for translation initiation factor IF3 in Escherichia coli. Mol Microbiol 21:331-346.
48. Sacerdot C, Fayat G, Dessen P, Springer M, Plumbridge JA, Grunberg-Manago M, Blanquet S. 1982. Sequence of a 1.26 Kb DNA fragment containing the structural gene for E. coli IF3: Presence of an AUU initiator codon. EMBO J 1:311-315.
49. Santer M, Dahlberg AE. 1996. Ribosomal RNA: A historical perspective. In: Zimmermann RA, Dahlberg AE, eds. Ribosomal RNA. Structure, evolution, processing, and function in protein biosynthesis. Boca Raton, Florida: CRC Press, pp 3-20.
50. Schluckebier G, O'Gara M, Saenger W, Cheng X. 1995. Universal catalytic domain structure of AdoMet-dependent methyltransferases. J Mol Biol 247:16-20.
51. Sette M, van Tilborg P, Spurio R, Kaptein R, Paci M, Gualerzi CO, Boelens R. 1997. The structure of the translation initiation factor IF1 from E. coli contains an oligomer-binding motif. EMBO J 16:1436-1443.
52. Sussman JK, Simons E, Simons RW. 1996. Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Mol Microbiol 21:347-360.
53. Tapprich WE, Goss D, Dahlberg AE. 1989. Mutation of position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis. Proc Natl Acad Sci USA 86:4927-4931.
54. Weston SA, Lahm A, Suck D. 1992. X-ray structure of the DNase l-d(GGTATACC)2 complex at 2.3 Å resolution. J Mol Biol 226: 1237-1256.
55. Wintermeyer W, Gualerzi CO. 1983. Effect of Escherichia coli initiation factors on the kinetics of N-AcPhe-tRNAPhe binding to 30S ribosomal subunits. A fluorescenze stopped-flow study. Biochemistry 22:690-694.