RNase E: Still a wonderfully mysterious enzyme

Molecular Microbiology

Volumn 23, Issue 6, 1997, Pages 1099-1106

  Cohen, Stanley N ^a   McDowall, Kenneth J ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; RIBONUCLEASE E; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ENDORIBONUCLEASES; ESCHERICHIA COLI; GENES, BACTERIAL;

EID: 0031000662     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.1997.tb02593.x     Document Type: Review

References (70)

1. Apirion, D., and Gitelman, D.R. (1980) Decay of RNA in RNA processing mutants of Escherichia coli. Mol Gen Genet 177: 339-343.
2. Apirion, D., and Lassar, A.B. (1978) A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J Biol Chem 53: 1738-1742.
3. Babitzke, P., and Kushner, S.R. (1991) The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad SciUSA 88: 1-5.
4. Bouvet, P., and Belasco, J.G. (1992) Control of RNase E-mediated RNA degradation by 5′-terminal base pairing in E. coli. Nature 360: 488-491.
5. Braun, F., Hajnsdorf, E., and Regnier, P. (1995) Polynucleotide phosphorylase is required for the rapid degradation of the RNase E-processed rpsO messenger RNA of Escherichia coli devoid of its 3′ hairpin. Mol Microbiol 19: 997-1005.
6. Carpousis, A.J., van Houwe, G., Ehretsmann, C., and Krisch, H.M. (1994) Copurification 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. Carrara, G., Calandra, P., Fruscoloni, P., and Tocchini-Valentini, G.P. (1995) Two helices plus a linker: a small model substrate for eukaryotic RNase P. Proc Natl Acad Sci USA 92: 2627-2631.
8. Casaregola, S., Jacq, A., Laoudj, D., McGurk, G., Margarson, S., Tempete, M., Norris, V., and Holland, I.B. (1992) Cloning and analysis of the entire Escherichia coli ams gene, ams is identical to hmp1 and encodes a 114 kDa protein that migrates as a 180 kDa protein. J Mol Biol 228: 30-40.
9. Casaregola, S., Jacq, A., Laoudj, D., McGurk, G., Margarson, S., Tempete, M., Norris, V., and Holland, I.B. (1994) Correction: Cloning and analysis of the entire Escherichia coli ams gene. J Mol Biol 238: 867.
10. Chanda, P.K., Ono, M., Kuwano, M., and Kung, H.F. (1985) Cloning, sequence analysis, and expression of alteration of the messenger RNA stablility (ams) gene of Escherichia coli. J Bacteriol 161: 446-449.
11. Chauhan, A.K., Miczak, A., Taraseviciene, L., and Apirion, D. (1991) Sequencing and expression of the rne gene of Escherichia coli. Nucleic Acids Res 19: 125-129.
12. Claverie-Martin, F., Diaz-Torres., M., Yancey, S.D., and Kushner, S.R. (1991) Analysis of the altered mRNA stability (ams) gene from Escherichia coli: nucleotide sequence, transcriptional analysis, and homology of its product to MRP3, a mitochondrial ribosomal protein from Neurospora crassa. J Biol Chem 266: 2843-2851.
13. Cohen, S.N. (1995) Surprises at the 3′ end of prokaryotic RNA. Cell 80: 829-832.
14. Cormack, R.S., and Mackie, G.A. (1992) Structural requirements for the processing of Escherichia coli 5S ribosomal RNA by RNase E in vitro. J Mol Biol 228: 1078-1090.
15. 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.
16. Darr, S.C., Brown, J.W., and Pace, N.R. (1992) The varieties of ribonuclease P. Trends Biochem Sci 17: 178-182.
17. Ehretsmann, C., Carpousis, A.J., and Krisch, H.M. (1990) Mutational analysis of a RNase E dependent cleavage site from a bacteriophage T4 mRNA. NATO (Adv Sci Inst) Ser H Cell Biol H49: 21-30.
18. Ehretsmann, C.P., Carpousis, A.J., and Krisch, H.M. (1992a) mRNA degradation in procaryotes. FASEB J 6: 3186-3192.
19. Ehretsmann, C.P., Carpousis, A.J., and Krisch, H.M. (1992b) Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes & Dev 6: 149-159.
20. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.F., Dougherty, B.A., Merrick, J.M., McKenney, K., Sutton, G., Fitzhugh, W., Fields, C., Gocayne, J.D., Scott, J., Shirley, R., Liu, L.I., Glodek, A., Kelley, J.M., Weidman, J.F., Phillips, C.A., Spriggs, T., Hedblom, E., Cotton, M.D., Utterback, T.R., Hanna, M.C., Nguyen, D.T., Saudek, D.M., Brandon, R.C., Fine, L.D., Fritchman, J.L., Fuhrmann, J.L., Geoghagen, N.S.M., Gnehm, C.L., McDonald, L.A., Fraser, C.M., Smith, H.O., and Venter, J.C. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae. Science 269: 496-512.
21. Franzetti, B., Sohlberg, B., Zaccai, G., and von Gabain, A. (1997) Biochemical and serological evidence for an RNase E-like activity in halophilic Archaea. J Bacteriol, in press.
22. Fritsch, J., Rothfuchs, R., Rauhut, R., and Klug, G. (1995) Identification of an mRNA element promoting rate-limiting cleavage of the polycistronic puf mRNA in Rhodobacter capsulatus by an enzyme similar to RNase E. Mol Microbiol 15: 1017-1029.
23. Gegenheimer, P., Watson, N., and Apirion, D. (1977) Multiple pathways for primary processing of ribosomal RNA in Escherichia coli. J Biol Chem 252: 3064-3073.
24. Georgellis, D., Sohlberg, B., Hartl, F.U., and von Gabain, A. (1995) Identification of GroEL as a constituent of a messenger RNA-protection complex in Escherichia coli. Mol Microbiol 16: 1259-1268.
25. Ghora, B.K., and Apirion, D. (1978) Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15: 1055-1066.
26. Gurevitz, M., Watson, N., and Apirion, D. (1982) A cleavage site of ribonuclease F, a putative processing endoribonuclease from Escherichia coli. Eur J Biochem 124: 553-559.
27. Hajnsdorf, E., Braun, F., Haugel-Nielsen, J., and Regnier, P. (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc Natl Acad Sci USA 92: 3973-3977.
28. Hardt, W.-D., Schlegl, J., Erdmann, V.A., and Hartmann, R.K. (1993) Role of the D arm and the anticodon arm in tRNA recognition by eubacterial and eukaryotic RNase P enzymes. Biochemistry 32: 13046-13053.
29. Hartl, F.D. (1995) Mechanisms and pathways of chaperone-mediated protein folding. Cold Spring Harb Symp Quant Biol 60: 429-434.
30. Hiraga, S. (1992) Chromosome and plasmid partitioning in Escherichia coli. Annu Rev Biochem 61: 283-306.
31. +, whose overexpression inhibits sexual development, encodes an RNaselll-like RNase. EMBO J 10: 221-226.
32. Jain, C., and Belasco, J.G. (1995) RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 9: 84-96.
33. Kaberdin, V.R., Chao, Y.-H., and Lin-Chao, S. (1996) RNase E cleaves at multiple sites in bubble region of RNAI stemloops yielding products that dissociate differentially from the enzyme. J Biol Chem 271: 13103-13109.
34. Kido, M., Yamanaka, K., Mitani, T., Niki, H., Ogura, T., and Hiraga, S. (1996) RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli. J Bacteriol 178: 3917-3925.
35. Kuwano, M., Ono, M., Endo, H., Hori, K., Nakamura, K., Hirota, Y., and Ohnishi, Y. (1977) Gene affecting longevity of messenger RNA: a mutant of Escherichia coli with altered mRNA stability. Mol Gen Genet 154: 279-285.
36. Lin-Chao, S., and Cohen, S.N. (1991) The rate of processing and degradation of antisense RNAI regulates the replication of ColE1-type plasmids in vivo. Cell 65: 1233-1242.
37. Lin-Chao, S., Wong, T.T., McDowall, K.J., and Cohen, S.N. (1994) Effects of nucleotide sequence on the specificity of rne-dependent and RNase E-mediated cleavages of RNAI encoded by the pBR322 plasmid. J Biol Chem 269: 10797-10803.
38. Lundberg, U., von Gabain, A., and Melefors, O. (1990) Cleavages in the 5′ region of the ompA and bla messenger RNA control stability: studies with a mutant altering messenger RNA stability and a novel endoribonuclease. EMBO J 9: 2731-2742.
39. Lundberg, U., Melefors, O., Sohlberg, B., Georgellis, D., and von Gabain, A. (1995) RNase K: one less letter in the alphabet soup. Mol Microbiol 17: 595-596.
40. McDowall, K.J., and Cohen, S.N. (1996) The N-terminal domain of the rne gene product has Rnase E activity and is non-overlapping with the arginine-rich RNA-binding motif. J Mol Biol 255: 349-355.
41. McDowall, K.J., Hernandez, R.G., Lin-Chao, S., and Cohen, S.N. (1993) The ams-1 and rne-3071 temperature-sensitive mutations in the ams gene are in close proximity to each other and cause substitutions within a domain that resembles a product of the Escherichia coli mre locus. J Bacteriol 175: 4245-4249.
42. McDowall, K.J., Lin-Chao, S., and Cohen, S.N. (1994) A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269: 10790-10796.
43. McDowall, K.J., Kaberdin, V.R., Wu, S.W., Cohen, S.N., and Lin-Chao, S.N. (1995) Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature 374: 287-290.
44. Mackie, G.A. (1991) Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the product of the ams gene in vivo and in vitro. J Bacteriol 173: 2488-2497.
45. Mackie, G.A. (1992) Secondary structure of the mRNA for ribosomal protein S20. Implications for cleavage by ribonuclease E. J Biol Chem 267: 1054-1061.
46. 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.
47. Melefors, O., and von Gabain., A. (1991) Genetic studies of cleavage-initiated mRNA decay and processing of ribosomal 9S RNA show that the Escherichia coli ams and me loci are the same. Mol Microbiol 5: 857-864.
48. Melefors, O., Lundberg, U., and von Gabain, A. (1993) RNA processing and degradation by RNase K and RNase E. In Control of Messenger RNA Stability. Belasco, J., and Brawerman, G. (eds). San Diego: Academic Press, pp. 53-70.
49. Miczak, A., Srivastava, R.A., and Apirion, D. (1991) Location of the RNA-processing enzymes RNase III, RNase E and RNase P in the Escherichia coli cell. Mol Microbiol 5: 1801-1810.
50. Miczak, A., Kaberdin, V.R., Wei, C.-L., and Lin-Chao, S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolylic complex. Proc Natl Acad Sci USA 93: 3865-3869.
51. Misra, T.K., and Apirion, D. (1979) RNase E, an RNA processing enzyme from Escherichia coll. J Biol Chem 254: 11154-11159.
52. Mudd, E.A., and Higgins, C.F. (1993) Escherichia coli endoribonuclease RNase E: autoregulalion of expression and site-specific cleavage of mRNA. Mol Microbiol 9: 557-568.
53. Mudd, E.A., Krisch, H.M., and Higgins, C.F. (1990) RNase E, an endoribonuclease, has a general role in the chemical decay of Escherichia coli mRNA: evidence that rne and ams are the same genetic locus. Mol Microbiol 4: 2127-2135.
54. Naureckiene, S., and Uhlin, B.E. (1996) In vitro analysis of messenger RNA processing by RNase E in the pap operon of Escherichia coli. Mol Microbiol 21: 55-68.
55. Niki, H., Jaffe, A., Imamura, R., Ogura, T., and Hiraga, S. (1991) The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 10: 183-193.
56. O'Hara, E.B., Chekanova, J.A., Ingle, C.A., Kushner, Z.R., Peters, E., and Kushner, S.R. (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc Natl Acad Sci USA 92: 1807-1811.
57. Okada, Y., Wachi, M., Hirata, A., Suzuki, K., Nagai, K., and Matsuhashi, M. (1994) Cytoplasmic axial filaments in Escherichia coli cells: possible function in the mechanism of chromosome segragation and cell division. J Bacteriol 176: 917-922.
58. Ono, M., and Kuwano, M. (1979) A conditional lethal mutation in Escherichia coli strain with a longer chemical lifetime of mRNA. J Mol Biol 129: 343-357.
59. Py, B., Higgins, C.F., Krisch, H.M., and Carpousis, A.J. (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381: 169-172.
60. Ray, B.K., and Apirion, D. (1981) Transfer RNA precursors are accumulated in Escherichia coli in the absence of RNase E. Eur J Biochem 114: 517-524.
61. Sohlberg, B., Lundberg, U., Hartl, F.-U., and von Gabain, A. (1993) Functional interaction of heat shock protein GroEL with RNase E-like activity in Escherichia coli. Proc Natl Acad Sci USA 90: 277-281.
62. Taraseviciene, L., Miczak, A., and Apirion, D. (1991) The gene specifying RNase E (rne) and a gene affecting mRNA stability (ams) are the same gene. Mol Microbiol 5: 851-855.
63. Taraseviciene, L., Bjork, G.R., and Uhlin, B.E. (1995) Evidence for an RNA-binding region in the Escherichia coli processing endoribonuclease RNase E. J Biol Chem 270: 26391-26398.
64. Tomcsanyi, T., and Apirion, D. (1985) Processing enzyme ribonuclease E specifically cleaves RNA I. An inhibitor of primer formation in plasmid DNA synthesis. J Mol Biol 185: 713-720.
65. Wachi, M., Doi, M., Tamaki, S., Park, W., Nakajima-Iijima, S., and Matsuhashi, M. (1988) Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and the amount of penicillin-binding proteins in Escherichia coli. J Bacteriol 169: 4935-4940.
66. Wang, M., and Cohen, S.N. (1994) ard-1: a human gene that reverses the effects of temperature-sensitive and deletion mutations in the Escherichia coli rne gene and encodes an activity producing RNase E-like cleavages. Proc Natl Acad Sci USA 91: 10591-10595.
67. Waugh, D.S., and Pace, N.R. (1990) Complementation of an RNase P RNA (rnpB) gene deletion in Escherichia coli by homologous genes from distantly related eubacteria. J Bacteriol 172: 6316-6322.
68. Wennborg, A., Sohlberg, B., Angerer, D., Klein, G., and von Gabain, A. (1995) A human RNase E-like activity which cleaves RNA sequences involved in mRNA stability control. Proc Natl Acad Sci USA 92: 7322-7326.
69. Xu, F., and Cohen, S.N. (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374: 180-183.
70. Zhou, A., Hassel, B.A., and Silverman, R.H. (1993) Expression cloning of 2-5A-dependent RNase: a uniquely regulated mediator of interferon actions. Cell 72: 753-766.