The fourth step of protein synthesis: Disassembly of the posttermination complex is catalyzed by elongation factor G and ribosome recycling factor, a near-perfect mimic of tRNA

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 66, Issue , 2001, Pages 515-529

  Kaji, A ^b   Kiel, M C ^b   Hirokawa, G ^a   Muto, A R ^b   Inokuchi, Y ^b   Kaji, H ^b  

^a CHIBA UNIVERSITY   (Japan)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA GALACTOSIDASE; ELONGATION FACTOR G; MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RECYCLING FACTOR; TRANSFER RNA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BACTERIAL GENE; BACTERIAL SURVIVAL; CHLOROPLAST; CODON; CONFERENCE PAPER; DRUG TARGETING; ESCHERICHIA COLI; EUKARYOTE; GENE MUTATION; GENETIC CODE; MOLECULAR MIMICRY; MUTATIONAL ANALYSIS; MYCOPLASMA GENITALIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLANT GENETICS; POLYSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REPORTER GENE; RIBOSOME SUBUNIT; RNA TRANSLATION; SEQUENCE HOMOLOGY; TEMPERATURE SENSITIVITY; THERMOSTABILITY; TRANSLATION REGULATION; ARTICLE; PROTEIN DEPLETION; RNA SEQUENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MYCOPLASMA GENITALIUM;

EID: 0001393990     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2001.66.515     Document Type: Conference Paper

References (68)

1. Adhin M.R. and van Duin J. 1990. Scanning model for translational reinitiation in eubacteria. J. Mol. Biol. 213: 811.
2. 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.
3. Atarashi K. and Kaji A. 2000. Inhibitory effect of heterologous ribosome recycling factor on growth of Escherichia coli. J. Bacteriol. 182: 6154.
4. 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.
5. Beremand M.N. and Blumenthal T. 1979. Overlapping genes in RNA phage: A new protein implicated in lysis. Cell 18: 257.
6. Das A. and Yanofsky C. 1984. A ribosome binding site sequence is necessary for efficient expression of the distal gene of a translationally-coupled gene pair. Nucleic Acids Res. 12: 4757.
7. Davies J. and Davis B.D. 1968. Misreading of ribonucleic acid code words induced by aminoglycoside antibiotics: The effect of drug concentration. J. Biol. Chem. 243: 3312.
8. Davis B.D. 1971. Role of subunits in the ribosome cycle. Nature 321: 153.
9. Dincbas V., Heurgue-Hamard V., Buckingham R.H., Karimi R., and Ehrenberg M. 1999. Shutdown in protein synthesis due to the expression of mini-genes in bacteria. J. Mol. Biol. 291: 745.
10. Draper D.E. 1996. Translational initiation. In Escherichia coli and Salmonella: Cellular and molecular biology (ed. F.C. Neidhart et al.), p. 902. ASM Press, Washington, D.C.
11. Frank J. and Agrawal R.K. 2000. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 318.
12. Fraser C.M., Gocayne J.D., White O., Adams M.D., Clayton R.A., Fleischmann R.D., Bult C.J., Kerlavage A.R., Sutton G., Kelley J.M., Fritchman J.L., Weidman J.F., Small K.V., Sandusky M., Fuhrmann J., Nguyen D., Utterback T.R., Saudek D.M., Phillips C.A., Merrick J.M., Tomb J.-F., Dougherty B.A., Bott K.F., Hu P.-C., Lucier T.S., Peterson S.N., Smith H.O., Hutchison C.A., III, and Venter J.C. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270: 397.
13. Grentzmann G., Kelly P.J., Laalami S., Shuda M., Firpo M.A., Cenatiempo Y., and Kaji A. 1998. Release factor RF-3 GTPase activity acts in disassembly of the ribosome termination complex. RNA 4: 973.
14. Grodzicker T. and Zipser D. 1968. A mutation which creates a new site for the re-initiation of polypeptide synthesis in the z gene of the lac operon of Escherichia coli. J. Mol. Biol. 38: 305.
15. Gualerzi C., Pon C.L., and Kaji A. 1971. Initiation factor dependent release of aminoacyl-tRNAs from complexes of 30S ribosomal subunits, synthetic polynucleotide and aminoacyl tRNA. Biochem. Biophys. Res. Commun. 45: 1312.
16. Gualerzi C.O., Brandi L., Caserta E., Teana A.L., Spurio R., Tomsic J., and Pon C.L. 2000. Translation initiation in bacteria. In The ribosome: Structure, function, antibiotics, and cellular interactions (ed. R.A. Garret et al.), p. 477. ASM Press, Washington, D.C.
17. Heurgue-Hamard V., Karimi R., Mora L., MacDougall J., Leboeuf C., Grentzmann G., Ehrenberg M., and Buckingham R.H. 1998. Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome. EMBO J. 17: 808.
18. Hirashima A. and Kaji A. 1970. Factor dependent breakdown of polysomes. Biochem. Biophys. Res. Commun. 41: 877.
19. -. 1972a. Factor-dependent release of ribosomes from messenger RNA - Requirement for two heat-stable factors. J. Mol. Biol. 65: 43.
20. -. 1972b. Purification and properties of ribosome releasing factor. Biochemistry 11: 4037.
21. -. 1973. Role of elongation factor G and a protein factor on the release of ribosomes from messenger ribonucleic acid. J. Biol. Chem. 248: 7580.
22. Ichikawa S. and Kaji A. 1989. Molecular cloning and expression of ribosome releasing factor. J. Biol. Chem. 264: 20054.
23. Inokuchi Y., Hirashima A., Sekine Y., Janosi L., and Kaji A. 2000. Role of ribosome recycling factor (RRF) in translational coupling. EMBO J. 19: 3788.
24. Janosi L., Ricker R., and Kaji A. 1996a. Dual functions of ribosome recycling factor in protein biosynthesis: Disassembling the termination complex and preventing translational errors. Biochimie 78: 959.
25. Janosi L., Shimizu I., and Kaji A. 1994. Ribosome recycling factor (ribosome releasing factor) is essential for bacterial growth. Proc. Natl. Acad. Sci. 91: 4249.
26. Janosi L., Hara H., Zhang S., and Kaji A. 1996b. Ribosome recycling by ribosome recycling factor (RRF) - An important but overlooked step of protein biosynthesis. Adv. Biophys. 32: 121.
27. Janosi L., Mori H., Sekine Y., Abragan J., Janosi R., Hirokawa G., and Kaji A. 2000. Mutations influencing the frr gene coding for ribosome recycling factor (RRF). J. Mol. Biol. 295: 815.
28. Janosi L., Mottagui-Tabar S., Isaksson L.A., Sekine Y., Ohtsubo E., Zhang S., Goon S., Nelken S., Shuda M., and Kaji A. 1998. Evidence for in vivo ribosome recycling, the fourth step in protein biosynthesis. EMBO J. 17: 1141.
29. Kaempfer R. 1970. Dissociation of ribosomes on polypeptide chain termination and origin of single ribosomes. Nature 228: 534.
30. -. 1972. Initiation factor IF-3: Specific inhibitor of ribosomal subunit association. J. Mol. Biol. 71: 583.
31. Kaji A. and Hirokawa G. 2000. Ribosome recycling factor: An essential factor for protein synthesis. In The ribosome: Structure, function, antibiotics and cellular interactions (ed. R.A. Garret et al.), p. 527. ASM Press, Washington, D.C.
32. Kaji A. and Kaji H. 1963. Specific interaction of soluble RNA with polyribonucleic acid induced polysomes. Biochem. Biophys. Res. Commun. 13: 186.
33. Kaji A., Teyssier E., and Hirokawa G. 1998. Disassembly of the post-termination complex and reduction of translational error by ribosome recycling factor (RRF) - A possible new target for antibacterial agents. Biochem. Biophys. Res. Commun. 250: 1.
34. Kaji H. and Kaji A. 1965. Specific binding of sRNA to ribosomes: Effect of streptomycin. Proc. Natl. Acad. Sci. 54: 213.
35. Kaji H., Suzuka I., and Kaji A. 1966. Binding of specific soluble ribonucleic acid to ribosomes. Binding of soluble ribonucleic acid to the template-30 S subunits complex. J. Biol. Chem. 241: 1251.
36. Kanai T., Takeshita S., Atomi H., Umemura K., Ueda M., and Tanaka A. 1998. A regulatory factor, Fi11p, involved in derepression of the isocitrate lyase gene in Saccharomyces cerevisiae. A possible mitochondrial protein necessary for protein synthesis in mitochondria. Eur. J. Biochem. 256: 212.
37. 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.
38. Kim K.K., Min K., and Suh S.W. 2000. Crystal structure of the ribosome recycling factor from Escherichia coli. EMBO J. 19: 2362.
39. Kohler R.E., Ron E.Z., and Davis B.D. 1968. Significance of the free 70S ribosomes in Escherichia coli extracts. J. Mol. Biol. 36: 71.
40. Kozak M. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234: 187.
41. Nierhaus K.H., Spahn C., Burkhardt N., Dabrowski M., Diedrich G., Einfeldt E., Kamp D., Marquez V., Patzke S., Schafer M.A., Stelzl U., Blaha G., Willumeit R., and Stuhrmann H.B. 2000. Ribosome elongation cycle. In The ribosome: Structure, function, antibiotics and cellular interactions (ed. R.A. Garret et al.), p. 319. ASM Press, Washington, D.C.
42. Nirenberg M. and Leder P. 1964. RNA codewords and protein synthesis: The effect of trinucleotides upon the binding of sRNA to ribosomes. Science 145: 1399.
43. 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.
44. Pavlov M.Y., Freistroffer D.V., Heurgue-Hamard V., Buckingham R.H., and Ehrenberg M. 1997a. Release factor RF3 abolishes competition between release factor RF1 and ribosome recycling factor (RRF) for a ribosome binding site. J. Mol. Biol. 273: 389.
45. Pavlov M.Y., Freistroffer D.V., MacDougall J., Buckingham R.H., and Ehrenberg M. 1997b. Fast recycling of Escherichia coli ribosomes requires both ribosome recycling factor (RRF) and release factor RF3. EMBO J. 16: 4134.
46. Pestka S. and Nirenberg M. 1966. Regulatory mechanisms and protein synthesis. X. Codon recognition on 30 S ribosomes. J. Mol. Biol. 21: 145.
47. Rao A.R. and Varshney U. 2001. Specific interaction between the ribosome recycling factor and the elongation factor G from Mycobacterium tuberculosis mediates peptidyl-tRNA release and ribosome recycling in Escherichia coli. EMBO J. 20: 2977.
48. Remme J., Margus T., Villems R., and Nierhaus K.H. 1989. The third ribosomal tRNA-binding site, the E site, is occupied in native polysomes. Eur. J. Biochem. 183: 281.
49. Rodnina M.V., Savelsbergh A., Katunin V.I., and Wintermeyer W. 1997. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385: 37.
50. Rodnina M.V., Pape T., Savelsbergh A., Mohr D., Matassova N.B., and Wintermeyer W. 2000. Mechanisms of partial reactions of the elongation cycle catalyzed by elongation factors Tu and G. In The ribosome: Structure, function, antibiotics and cellular interactions (ed. R.A. Garret et al.), p. 301. ASM Press, Washington, D.C.
51. Rodnina M.V., Savelsbergh A., Matassova N.B., Katunin V.I., Semenkov Y.P., and Wintermeyer W. 1999. Thiostrepton inhibits the turnover but not the GTPase of elongation factor G on the ribosome. Proc. Natl. Acad. Sci. 96: 9586.
52. Rolland N., Janosi L., Block M.A., Shuda A., Teyssier E., Miege C., Cheniclet C., Carde J., Kaji A., and Joyard J. 1999. Plant ribosome recycling factor homolog is a chloroplastic protein and is bactericidal in Escherichia coli carrying temperature-sensitive ribosome recycling factor. Proc. Natl. Acad. Sci. 96: 5464.
53. Ryoji M., Berland R., and Kaji A. 1981. Reinitiation of translation from the triplet next to the amber termination codon in the absence of ribosome-releasing factor. Proc. Natl. Acad. Sci. 78: 5973.
54. Santos M.A.S., Perreau V.M., and Tuite M.F. 1996. Transfer RNA structural change is a key element in the reassignment of the CUG codon in Candida albicans. EMBO J. 15: 5060.
55. Sarabhai A. and Brenner S. 1967. A mutant which reinitiates the polypeptide chain after chain termination. J. Mol. Biol. 27: 145.
56. Scolnick E., Tompkins R., Caskey T., and Nirenberg M. 1968. Release factors differing in specificity for terminator codons. Proc. Natl. Acad. Sci. 61: 768.
57. Selmer M., Al-Karadaghi S., Hirokawa G., Kaji A., and Liljas A. 1999. Crystal structure of Thermotoga maritima ribosome recycling factor: A tRNA mimic. Science 286: 2349.
58. Stark H., Orlova E.V., Rinke-Appel J., Jünke N., Mueller F., Rodnina M., Wintermeyer W., Brimacombe R., and van Heel M. 1997. Arrangement of tRNAs in pre- and posttranslocational ribosomes revealed by electron cryomicroscopy. Cell 88: 19.
59. Steitz J.A. 1970. Nucleotide sequenes of the ribosomal binding sites of bacteriophage R17 RNA. Cold Spring Harbor Symp. Quant. Biol. 34: 621.
60. Subramanian A.R. and Davis B.D. 1971. Rapid exchange of subunits between free ribosomes in extracts of Escherichia coli. Proc. Natl. Acad. Sci. 68: 2453.
61. -. 1973. Release of 70S ribosomes from polysomes in Escherichia coli. J. Mol. Biol. 74: 45.
62. Subramanian A.R., Davis B.D., and Beller R.J. 1970. The ribosome dissociation factor and the ribosome-polysome cycle. Cold Spring Harbor Symp. Quant. Biol. 34: 223.
63. Tjandra N. and Bax A. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278: 1111.
64. Tjandra N., Garrett D.S., Gronenborn A.M., Bax A., and Clore G.M. 1997. Defining long range order in NMR structure determination from the dependence of heteronuclear relaxation times on rotational diffusion anisotropy. Nat. Struct. Biol. 4: 443.
65. Wilson D.N., Dalphin M.E., Pel H.J., Major L.L., Mansell J.B., and Tate W.P. 2000. Factor-mediated termination of protein synthesis: A welcome return to the mainstream of translation. In The ribosome: Structure, function, antibiotics, and cellular interactions (ed. R.A. Garret et al.), p. 495. ASM Press, Washington, D.C.
66. 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.
67. Yoshida T., Uchiyama S., Nakano H., Kashimori H., Kijima H., Ohshima T., Saihara Y., Ishino T., Shimahara H., Yoshida T., Yokose K., Ohkubo T., Kaji A., and Kobayashi Y. 2001. Solution structure of the ribosome recycling factor from Aquifex aeolicus. Biochemistry 40: 2387.
68. 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 29: 29.