Messenger RNA release from ribosomes during 5'-translational blockage by consecutive low-usage arginine but not leucine codons in Escherichia coli

Molecular Microbiology

Volumn 25, Issue 4, 1997, Pages 707-716

  Gao, Wenwu ^a,d   Tyagi, Sanjay ^b   Kramer, Fred Russell ^b   Goldman, Emanuel ^a,c  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LEUCINE;

ARTICLE; ESCHERICHIA COLI; GENE INSERTION; HYBRIDIZATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA ANALYSIS; SEQUENCE HOMOLOGY; STOP CODON;

ESCHERICHIA COLI;

EID: 0030799017     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.5081871.x     Document Type: Article

References (49)

1. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1987) Preparation and analysis of RNA. In Current Protocols in Molecular Biology, Vol. 1, Chap. 4. New York: John Wiley & Sons.
2. Barak, Z., Lindsley, D., and Gallant, J. (1996) On the mechanism of leftward frameshifting at several hungry codons. J Mol Biol 256: 676-684.
3. Beyer, D., Skripkin, E., Wadzack, J., and Nierhaus, K.H. (1994) How the ribosome moves along the mRNA during protein synthesis. J Biol Chem 269: 30713-30717.
4. Bochner, B.R., and Ames, B.N. (1982) Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J Biol Chem 257: 9759-9769.
5. Brinkmann, U., Mattes, R.E., and Buckel, P. (1989) High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene 85: 109-114.
6. Broeze, R.J., Solomon, C.J., and Pope, D.H. (1978) Effects of low temperature on in vivo and in vitro protein synthesis in Escherichia coli and Pseudomonas fluorescens. J Bacteriol 134: 861-874.
7. Caplan, A.B., and Menninger, J.R. (1979) Tests of the ribosomal editing hypothesis: amino acid starvation differentially enhances the dissociation of peptidyl-tRNA from the ribosome. J Mol Biol 134: 621-637.
8. Chen, G.F.T., and Inouye, M. (1990) Suppression of the negative effect of minor arginine codons on gene expression: preferential usage of minor codons within the first 25 codons of the Escherichia coli genes. Nucleic Acids Res 18: 1465-1473.
9. Chen, G.F.T., and Inouye, M. (1994) Role of the AGA/AGG codons, the rarest codons in global gene expression in Escherichia coli. Genes Dev 8: 2641-2652.
10. Dong, H., and Kurland, C.G. (1995) Ribosome mutants with altered accuracy translate with reduced processivity. J Mol Biol 248: 551-561.
11. Farabaugh, P.J. (1996) Programmed translational frameshifting. Microbiol Rev 60: 103-134.
12. Forchhammer, J., and Lindahl, L. (1971) Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15. J Mol Biol 55: 563-568.
13. Gao, W. (1996) Studies of translational accuracy in Escherichia coli: editing and methionyl-tRNA synthetase; uncharged tRNA and a programmed translational frameshift; low-usage codons and ribosome release. PhD thesis, University of Medicine and Dentistry of New Jersey, Newark, NJ, pp. 170-171.
14. Goldman, E. (1972) Shutoff of RNA phage f2 infected cells by superinfection with phage T4. PhD thesis, Massachusetts Institute of Technology, Cambridge, MA, p. 113.
15. Goldman, E. (1982) Effect of rate-limiting elongation on bacteriophage MS2 RNA-directed protein synthesis in extracts of Escherichia coli. J Mol Biol 158: 619-636.
16. Goldman, E., and Lodish, H.F. (1971) Inhibition of replication of ribonucleic acid bacteriophage f2 by superinfection with bacteriophage T4. J Virol 8: 417-429.
17. Goldman, E., and Zubay, G. (1994) Investigating codon usage in E. coli. Methods Mol Genet 3: 159-178.
18. Goldman, E., Rosenberg, A.R., Zubay, G., and Studier, F.W. (1995) Consecutive low-usage leucine codons block translation only when near the 5′ end of a message in Escherichia coli. J Mol Biol 245: 467-473.
19. Hamkalo, B.A., and Miller, O.L. (1973) Electron microscopy of genetic activity. Annu Rev Biochem 42: 379-396.
20. Heurgué-Hamard, V., Mora, L., Guarneros, G., and Buckingham, R.H. (1996) The growth defect in Escherichia coli deficient in peptidyl-tRNA hydrolase is due to starvation for Lys-tRNALys. EMBO J 15: 2826-2833.
21. Hüttenhofer, A., and Noller, H.F. (1994) Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13: 3892-3901.
22. Iost, I., and Dreyfus, M. (1994) mRNAs can be stabilized by DEAD-box proteins. Nature 372: 193-196.
23. Iost, I., Guillerez, J., and Dreyfus, M. (1992) Bacteriophage T7 RNA polymerase travels far ahead of ribosomes in vivo. J Bacteriol 174: 619-622.
24. Jørgensen, F., and Kurland, C.G. (1990) Processivity errors of gene expression in Escherichia coli. J Mol Biol 215: 511-521.
25. Kane, J.F. (1995) Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol 6: 494-500.
26. Kang, C., and Cantor, C.R. (1985) Structure of vibosomebound messenger RNA as revealed by enzymatic accessibility studies. J Mol Biol 181: 241-251.
27. Keiler, K.C., Waller, P.R., and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990-993.
28. Kennell, D., and Riezman, H. (1977) Transcription and translation initiation frequencies of the Escherichia coli lac operon. J Mol Biol 114: 1-21.
29. Trp in E. coli infected with bacteriophage MS2. J Mol Biol 168: 747-763.
30. Kurland, C.G. (1992) Translational accuracy and the fitness of bacteria. Annu Rev Genet 26: 29-50.
31. Lewin, B. (1994) Genes V. New York: Oxford University Press, pp. 262-263.
32. Manley, J.L. (1978) Synthesis and degradation of termination and premature-termination fragments of betagalactosidase in vitro and in vivo. J Mol Biol 125: 407-432.
33. Menninger, J.R. (1978) The accumulation as peptidyl-transfer RNA of isoaccepting transfer RNA families in Escherichia coli with temperature-sensitive peptidyl-transfer RNA hydrolase. J Biol Chem 253: 6808-6813.
34. Menninger, J.R., Coleman, R.A., and Tsai, L.-N. (1994) Erythromycin, lincosamides, peptidyl-tRNA dissociation, and ribosome editing. Mol Gen Genet 243: 225-233.
35. O'Farrell, P.H. (1978) The suppression of defective translation by ppGpp and its role in the stringent response. Cell 14: 545-557.
36. Parker, J. (1989) Errors and alternatives in reading the universal genetic code. Microbiol Rev 53: 273-298.
37. Rosenberg, A.H., Lade, B.N., Chui, D., Lin, S., Dunn, J.J., and Studier, F.W. (1987) Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene 56: 125-135.
38. Rosenberg, A.M., Goldman, E., Dunn, J., Studier, F.W., and Zubay, G. (1993) Effects of consecutive AGG codons on translation in Escherichia coli, demonstrated with a versatile codon test system. J Bacteriol 175: 716-722.
39. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, chapters 7, 9 and 10.
40. Spanjaard, R.A., and van Duin, J. (1988) Translation of the sequence AGG-AGG yields 50% ribosomal frameshift. Proc Natl Acad Sci USA 85: 7967-7971.
41. Spanjaard, R.A., Chen, K., Walker, J.R., and van Duin, J. (1990) Frameshift suppression at tandem AGA, and AGG codons by cloned tRNA genes: assigning a codon to argU tRNA and T4 tRNA (Arg). Nucleic Acids Res 18: 5031-5036.
42. Studier, F.W. (1991) Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J Mol Biol 219: 37-44.
43. Studier, F.W., and Moffat, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
44. Studier, F.W., Rosenberg, A.M., Dunn, J.J., and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185: 60-89.
45. Tyagi, S., and Kramer, F.R. (1996) Molecular beacons: probes that fluoresce upon hybridization. Nature Biotechnol 14: 303-308.
46. Varrichio, F., and Monier, R. (1971) Ribosome patterns in Escherichia coli growing at various rates. J Bacteriol 108: 105-110.
47. Yanofsky, C. (1981) Attenuation in the control of expression of bacterial operons. Nature 289: 751-758.
48. Yarchuk, O., Jacques, N., Guillerez, J., and Dreyfus, M. (1992) Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J Mol Biol 226: 581-596.
49. Zahn, K., and Landy, A. (1996) Modulation of lambda integrase synthesis by rare arginine tRNA. Mol Microbiol 21: 69-76.