Polynucleotide phosphorylase is required for the rapid degradation of the RNase E-processed rpsO mRNA of Escherichia coli devoid of its 3′ hairpin

Molecular Microbiology

Volumn 19, Issue 5, 1996, Pages 997-1005

  Braun, Frédérique ^a   Hajnsdorf, Eliane ^a   Régnier, Philippe ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; RNA CLEAVAGE; RNA DEGRADATION;

ASPERGILLUS NUCLEASE S1; BASE SEQUENCE; BINDING SITES; DNA, BACTERIAL; ENDORIBONUCLEASES; ESCHERICHIA COLI; EXORIBONUCLEASES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBOSOMAL PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SEQUENCE DELETION;

ESCHERICHIA COLI;

EID: 0029961542     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.440971.x     Document Type: Article

References (43)

1. Arraiano, M.C., Yancey, S.D., and Kushner, S.R. (1988) Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutant of Escherichia coli K-12. J Bacteriol 170: 4625-4633.
2. Bardwell, J.C.A., Régnier, P., Chen, S.-M., Nakamura, Y., Grunberg-Manago, M., and Court, D. (1989) Autoregulation of RNase III operon by mRNA processing. EMBO J 8: 3401-3407.
3. Belasco, J.G. (1993) mRNA degradation in prokaryotic cells: an overview. In Control of Messenger RNA Stability. Belasco, J.G., and Brawerman, G. (eds). New York: Academic Press, pp. 3-12.
4. Belasco, J.G., and Higgins, C.F. (1988) Mechanism of mRNA decay in bacteria: a perspective. Gene 72: 15-23.
5. Cannistraro, V.J., and Kennell, D. (1994) The processive reaction mechanism of ribonuclease II. J Mol Biol 243: 930-943.
6. Carpousis, A.G., Van Houwe, G., Ehretsmann, C., and Krisch, H.M. (1994) Co-purification of E. coli RNase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76: 889-900.
7. Causton, H., Py, E., McLaren, R.S., and Higgins, C.F. (1994) mRNA degradation in Escherichia coli: a novel factor which impedes the exoribonucleolytic activity of PNPase at stem-loop structures. Mol Microbiol 14: 731-741.
8. Cormack, R.S., Genereaux, J.L., and Mackie, G.A. (1993) RNase E activity is conferred by a single polypeptide: overexpression, purification and properties of the ams/rne/hmp1 gene product. Proc Natl Acad Sci USA 90: 9006-9010.
9. Donovan, W.P., and Kushner, S.R. (1986) Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci USA 83: 120-124.
10. Ehretsmann, C.P., Carpousis, A.J., and Krisch, H.M. (1992a) mRNA degradation in procaryotes. The FASEB J 6: 3186-3192.
11. Ehretsmann, C.P., Carpousis, A.J., and Krisch, H.M. (1992b) Specificity of Escherichia coli endoribonuclease E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev 6: 149-159.
12. Grunberg-Manago, M. (1963) Polynucleotide phosphorylase. In Progress in Nucleic Acids Research. Vol. 1. Cohn, W. (ed.). New York: Academic Press, pp. 93-133.
13. Guarneros, G., and Portier, C. (1990) Different specificities of ribonuclease II and polynucleotide phosphorylase in 3′ mRNA decay. Biochimie 72: 771-777.
14. Gupta, R.S., Kasai, T., and Schlessinger, D. (1977) Purification and some novel properties of Escherichia coli RNase II. J Biol Chem 252: 8945-8949.
15. Hajnsdorf, E., Carpousis, A.J., and Régnier, P. (1994a) Nucleolytic inactivation and degradation of the RNase III processed pnp message encoding polynucleotide phosphorylase of Escherichia coli. J Mol Biol 239: 439-454.
16. Hajnsdorf, E., Steier, O., Coscoy, L., Teysset, L., and Régnier, P. (1994b) Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcript of Escherichia coli: stabilizing function and evidence for efficient degradation in an ams-pnp-rnb mutant. EMBO J 13: 3368-3377.
17. Hajnsdorf, E., Braun, F., Haugel-Nielsen, J., and Régnier, P. (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc Natl Acad Sci USA 92: 3973-3977.
18. Higgins, C.F., Causton, H.C., Dance, G.S.C., and Mudd, E.A. (1993) The role of 3′ end in mRNA stability and decay. In Control of Messenger RNA Stability. Belasco, J.G., and Brawerman, G. (eds). New York: Academic Press, pp. 13-30.
19. Iost, I., and Dreyfus, M. (1994) mRNAs can be stabilized by DEAD-box proteins. Nature 372: 193-196.
20. Jacobson, A.B., Good, L., Simonetti, J., and Zuker, M. (1984) Some simple computational methods to improve the folding of large RNAs. Nucl Acids Res 12: 45-52.
21. Lopilato, J., Bortner, S., and Beckwith, J. (1986) Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives. Mol Gen Genet 205: 285-290.
22. Mackie, G.A., and Genereaux, J.L. (1993) The role of RNA structure in determining RNase E-dependent cleavage sites in the mRNA for ribosomal protein S20 in vitro. J Mol Biol 234: 998-1012.
23. McLaren, R.S., Newbury, S.F., Dance, G.S.C., Causton, H.C., and Higgins, C.F. (1991) mRNA degradation by processive 3′-5′ exonucleases in vivo and the implication for procaryotic mRNA decay in vivo. J Mol Biol 221: 81-95.
24. Mulligan, J.F., Groebe, D.R., Witherell, G.W., and Uhlenbeck, O.C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and DNA templates. Nucl Acids Res 15: 8783-8798.
25. Newbury, S.F., Smith, N.H., and Higgins, C.F. (1987) Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell 51: 1131-1143.
26. Pepe, C.M., Maslesa-Galic, S., and Simons, R.W. (1994) Decay of the IS 10 antisense RNA by 3′ exonucleases: evidence that RNase II stabilizes RNA-out against PNPase attack. Mol Microbiol 13: 1133-1142.
27. Petersen, C. (1993) Translation and mRNA stability in bacteria: a complex relationship. In Control of Messenger RNA Stability. Belasco, J.G., and Brawerman, G. (eds). New York: Academic Press, pp. 117-147.
28. Plamann, M.D., and Stauffer, G.V. (1990) E coli glyA mRNA decay: the role of 3′ secondary structure and the effects of the pnp and rnb mutations. Mol Gen Genet 220: 301-306.
29. Plumbridge, J.A., and Springer, M. (1983) Organization of the Escherichia coli chromosome around the genes for translation initiation factor IF2 (inf2) and a transcription terminator factor (nusA). J Mol Biol 167: 227-243.
30. Portier, C., Dondon, L., Grunberg-Manago, M., and Régnier, P. (1987) The first step in the functional inactivation of the E. coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5′ end. EMBO J 6: 2165-2170.
31. Portier, C., Migot, C., and Grunberg-Manago, M. (1981) Cloning of Escherichia coli pnp gene from an episome. Mol Gen Genet 183: 298-305.
32. Py, B., Causton, H., Mudd, E.A., and Higgins, C.F. (1994) A protein complex mediating mRNA degradation in Escherichia coli. Mol Microbiol 14: 717-729.
33. Régnier, P., and Grunberg-Manago, M. (1989) Cleavage by RNase III in the transcripts of the metY-nusA-infB operon of E. coli releases the tRNA and initiates the decay of the downstream mRNA. J Mol Biol 210: 293-302.
34. Régnier, P., and Grunberg-Manago, M. (1990) RNase III cleavages in non-coding leaders of Escherichia coli transcripts control mRNA stability and genetic expression. Biochimie 72: 825-834.
35. Régnier, P., and Hajnsdorf, E. (1991) Decay of mRNA encoding ribosomal protein S15 of Escherichia coli is initiated by an RNase E-dependent endonucleolytic cleavage that removes the 3′ stabilizing stem and loop structure. J Mol Biol 217: 283-292.
36. Régnier, P., and Portier, C. (1986) Initiation, attenuation and RNase III processing of transcripts from the E. coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J Mol Biol 187: 23-32.
37. Régnier, P., Grunberg-Manago, M., and Portier, C. (1987) Nucleotide sequence of the pnp gene of E. coli encoding polynucleotide phosphorylase; homology of the primary structure of the protein with the RNA binding domain of ribosomal protein S1. J Biol Chem 262: 63-68.
38. Sambrook, J., Maniatis, T., and Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
39. Sorensen, M.A., and Pedersen, S. (1991) Absolute in vivo translation rates of individual codons in Escherichia coli. J Mol Biol 222: 265-280.
40. Spahr, P.F., and Schlessinger, D. (1964) Breakdown of messenger ribonucleic acid by a potassium-activated phosphodiesterase from Escherichia coli. J Biol Chem 238: PC2251-PC2253.
41. Thang, M.N., Guschlbauer, W., Zachau, H.G., and Grunberg-Manago, M. (1967) Degradation of transfer nucleic acid by polynucleotide phosphorylase. J Mol Biol 26: 403-421.
42. Xu, F., and Cohen, S. (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374: 180-183.
43. Zilhao, R., Caillet, R., Régnier, P., and Arraiano, C. (1995) Precise physical mapping of the Escherichia coli rnb gene, encoding the ribonuclease II. Mol Gen Genet 248: 242-246.