In vivo effect of inactivation of ribosome recycling factor - Fate of ribosomes after unscheduled translation downstream of open reading frame

Molecular Microbiology

Volumn 54, Issue 4, 2004, Pages 1011-1021

  Hirokawa, Go ^a,b   Inokuchi, Hachiro ^c   Kaji, Hideko ^d   Igarashi, Kazuei ^a   Kaji, Akira ^b  

^a CHIBA UNIVERSITY   (Japan)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; ELONGATION FACTOR G; GENE PRODUCT; MESSENGER RNA; RIBOSOME RECYCLING FACTOR; RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CODON; DNA SYNTHESIS; GENE INACTIVATION; IN VIVO STUDY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; RNA SYNTHESIS; RNA TRANSLATION; TEMPERATURE SENSITIVITY;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; OPEN READING FRAMES; PEPTIDES; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER; TEMPERATURE;

EID: 8544281643     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04324.x     Document Type: Article

References (57)

1. Abo, T., Inada, T., Ogawa, K., and Aiba, H. (2000) SsrA-mediated tagging and proteolysis of Lacl and its role in the regulation of lac operon. EMBO J 19: 3762-3769.
2. Agrawal, R.K., Sharma, M.R., Kiel, M.C., Hirokawa, G., Booth, T.M., Spahn, C.M.T., et al. (2004) Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications. Proc Natl Acad Sci USA 101: 8900-8905.
3. Blumenthal, T. (1979) Qβ RNA replicase and protein synthesis elongation factors EF-Tu and EF-Ts. Methods Enzymol LX: 628-638.
4. Cruz-Vera, L.R., Hernandez-Ramon, E., Perez-Zamorano, B., and Guarneros, G. (2003) The rate of peptidyl-tRNA dissociation from the ribosome during minigene expression depends on the nature of the last decoding interaction. J Biol Chem 278: 26065-26070.
5. Ermolaeva, M.D., Khalak, H.G., White, O., Smith, H.O., and Salzberg, S.L. (2000) Prediction of transcription terminators in bacterial genomes. J Mol Biol 301: 27-33.
6. Felden, B., Himeno, H., Muto, A., McCutcheon, J.P., Atkins, J.F., and Gesteland, R.F. (1997) Probing the structure of the Escherichia coli 10Sa RNA (tmRNA). RNA 3: 89-103.
7. Flessel, C.P., Ralph, P., and Rich, A. (1967) Polyribosomes of growing bacteria. Science 158: 658-660.
8. Freistroffer, D.V., Pavlov, M.Y., MacDougall, J., Buckingham, R.H., and Ehrenberg, M. (1997) Release factor RF3 in E. coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. EMBO J 16: 4126-4133.
9. Fujiwara, T., Ito, K., Nakayashiki, T., and Nakamura, Y. (1999) Amber mutations in ribosome recycling factors of Escherichia coli and Thermus thermophilus: evidence for C-terminal modulator element. FEBS Lett 447: 297-302.
10. Fujiwara, T., Ito, K., and Nakamura, Y. (2001) Functional mapping of ribosome-contact sites in the ribosome recycling factor: a structural view from a tRNA mimic. RNA 7: 64-70.
11. Gilbert, R.J., Fucini, P., Connell, S., Fuller, S.D., Nierhaus, K.H., Robinson, C.V., et al. (2004) Three-dimensional structures of translating ribosomes by cryo-EM. Mol Cell 14: 57-66.
12. Hanes, J., and Pluckthun, A. (1997) In vitro selection and evolution of functional proteins by using ribosome display. Proc Natl Acad Sci USA 94: 4937-4942.
13. Hayes, C.S., Bose, B., and Sauer, R.T. (2002a) Proline residues at the C-terminus of nascent chains induce SsrA-tagging during translation termination. J Biol Chem 277: 33825-33832.
14. Hayes, C.S., Bose, B., and Sauer, R.T. (2002b) Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli. Proc Natl Acad Sci USA 99: 3440-3445.
15. Heurgue-Hamard, V., Karimi, R., Mora, L., MacDougall, J., Leboeuf, C., Grentzmann, G., et al. (1998) Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome. EMBO J 17: 808-816.
16. 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.
17. Hirokawa, G., Kiel, M.C., Muto, A., Kawai, G., Igarshi, K., Kaji, H., and Kaji, A. (2002a) Binding of ribosome recycling factor to ribosomes - comparison with tRNA. J Biol Chem 277: 35847-35852.
18. Hirokawa, G., Kiel, M.C., Muto, A., Selmer, M., Raj, V.S., Liljas, A., et al. (2002b) Post-termination complex disassembly by ribosome recycling factor, a functional tRNA mimic. EMBO J 21: 2272-2281.
19. Janosi, L., Shimizu, I., and Kaji, A. (1994) Ribosome recycling factor (ribosome releasing factor) is essential for bacterial growth. Proc Natl Acad Sci USA 91: 4249-4253.
20. Janosi, L., Mottagui-Tabar, S., Isaksson, L.A., Sekine, Y., Ohtsubo, E., Zhang, S., et al. (1998) Evidence for in vivo ribosome recycling, the fourth step in protein biosynthesis. EMBO J 17: 1141-1151.
21. 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: 815-829.
22. Jin, H., Bjornsson, A., and Isaksson, L.A. (2002) Cis control of gene expression in E. coli by ribosome queuing at an inefficient translational stop signal. EMBO J 21: 4357-4367.
23. Kaji, A., Kiel, M.C., Hirokawa, G., Muto, A., Inokuchi, Y., and Kaji, H. (2001) The fourth step of protein synthesis: disassembly of the post termination complex is catalyzed by elongation factor G and ribosome recycling factor, a near-perfect mimic of tRNA. Cold Spring Harb Symp Quant Biol 66: 515-529.
24. Kanai, T., Takeshita, S., Atomi, H., Umemura, K., Ueda, M., and Tanaka, A. (1998) A regulatory factor, Fil1p, 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: 212-220.
25. Karzai, A.W., Susskind, M.M., and Sauer, R.T. (1999) SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J 18: 3793-3799.
26. Keiler, K.C., Waller, P.R.H., and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990-993.
27. Kiel, M.C., Raj, V.S., Kaji, H., and Kaji, A. (2003) Release of ribosome-bound ribosome recycling factor by elongation factor G. J Biol Chem 278: 48041-48050.
28. Kim, K.K., Min, K., and Suh, S.W. (2000) Crystal structure of the ribosome recycling factor from Escherichia coli. EMBO J 19: 2362-2370.
29. Komine, Y., Kitabatake, M., Yokogawa, T., Nishikawa, K., and Inokuchi, H. (1994) A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc Natl Acad Sci USA 91: 9223-9227.
30. Kung, H.-F., Treadwell, B.V., Spears, C., Tai, P.-C., and Weissbach, H. (1977) DNA-directed synthesis in vitro of β-galactosidase: requirement for a ribosome release factor. Proc Natl Acad Sci USA 74: 3217-3221.
31. 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.
32. Mans, R.J., and Novelli, G.D. (1960) A convenient, rapid and sensitive method for measuring the incorporation of radioactive amino acids into protein. Biochem Biophys Res Commun 3: 540-543.
33. Mattheakis, L.C., Bhatt, R.R., and Dower, W.J. (1994) An in vitro polysome display system for identifying ligands from very large peptide libraries. Proc Natl Acad Sci USA 91: 9022-9026.
34. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. 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.
36. Nakano, H., Yoshida, T., Uchiyama, S., Kawachi, M., Matsuo, H., Kato, T., et al. (2003) Structure and binding mode of a ribosome recycling factor (RRF) from mesophilic bacterium. J Biol Chem 278: 3427-3436.
37. Nirenberg, M.W., and Matthaei, J.H. (1961) The dependence of cell-free protein synthesis in E. coli upon naturally occuring or synthetic template RNA. Pros Natl Acad Sci USA 47: 1588-1602.
38. Ogawa, K., and Kaji, A. (1975) Ribosome run through of the termination codon in the absence of the ribosome releasing factor. Biochim Biophys Acta 402: 288-296.
39. Olivares-Trejo, J.J., Bueno-Martinez, J.G., Guarneros, G., and Hernandez-Sanchez, J. (2003) The pair of arginine codons AGA AGG close to the initiation codon of the lambda int gene inhibits cell growth and protein synthesis by accumulating peptidyl-tRNAArg4. Mol Microbiol 49: 1043-1049.
40. Pavolov, M.Y., Freistroffer, D.V., MacDougall, J., Buckingham, R.H., and Ehrenberg, M. (1997) Fast recycling of Escherichia coli ribosomes requires both ribosome recycling factor (RRF) and release factor RF3. EMBO J 16: 4134-4141.
41. Roche, E.D., and Sauer, R.T. (1999) SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J 18: 4579-4589.
42. Roche, E.D., and Sauer, R.T. (2001) Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J Biol Chem 276: 28509-28515.
43. Rolland, N., Janosi, L., Block, M.A., Shuda, A., Teyssier, E., Miege, C., et al. (1999) Plant ribosome recycling factor homologue is a chloroplastic protein and is bactericidal in Escherichia coli carrying temperature-sensitive ribosome recycling factor. Proc Natl Acad Sci USA 96: 5464-5469.
44. Ryoji, M. (1981) Studies on the roles of ribosome releasing factor of Escherichia coli. PhD Thesis. University of Pennsylvania School of Medicine.
45. Ryoji, M., Berland, R., and Kaji, A. (1981a) Reinitiation of translation from the triplet next to the amber termination codon in the absence of ribosome-releasing factor. Proc Natl Acad Sci USA 78: 5973-5977.
46. Ryoji, M., Karpen, J.W., and Kaji, A. (1981b) Further characterization of ribosome releasing factor and evidence that it prevents ribosomes from reading through a termination codon. J Biol Chem 256: 5798-5801.
47. 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: 2349-2352.
48. Shimizu, Y., Inoue, A., Tomari, Y., Suzuki, T., Yokogawa, T., Nishikawa, K., and Ueda, T. (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19: 751-755.
49. Sorensen, M.A., and Pedersen, S. (1991) Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J Mol Biol 222: 265-280.
50. Sorensen, M.A., Kurland, C.G., and Pedersen, S. (1989) Codon usage determines translation rate in Escherichia coli. J Mol Biol 207: 365-377.
51. Steitz, J.A. (1969) Polypeptide chain initiation: nucleotide sequences of the three ribomosal binding sites in bacteriophage R17 RNA. Nature 224: 957-964.
52. Teixeira-Gomes, A.P., Cloeckaert, A., and Zygmunt, M.S. (2000) Characterization of heat, oxidative, and acid stress responses in Brucella melitensis. Infect Immun 68: 2954-2961.
53. Teyssier, E., Hirokawa, G., Tretiakova, A., Jameson, B., Kaji, A., and Kaji, H. (2003) Temperature sensitive mutation in yeast mitochondrial ribosome recycling factor (RRF). Nucleic Acid Res 31: 4218-4226.
54. Toyoda, T., Tin, O.P., Ito, K., Fujiwara, T., Kumasaka, T., Yamamoto, M., et al. (2000) Crystal structure combined with genetic analysis of the Thermus thermophilus ribosome recycling factor shows that a flexible hinge may act as a functional switch. RNA 6: 1432-1444.
55. Wickner, S., Maurizi, M.R., and Gottesman, S. (1999) Post-translational quality control: folding, refolding, and degrading proteins. Science 286: 1888-1893.
56. Withey, J.H., and Friedman, D.I. (2002) The biological roles of trans-translation. Curr Opin Microbiol 5: 154-159.
57. Yoshida, T., Uchiyama, S., Nakano, H., Kashimori, H., Kijima, H., Ohshima, T., et al. (2001) Solution structure of the ribosome recycling factor from Aquifex aeolicus. Biochemistry 40: 2387-2396.