Escherichia coli mrsC is an allele of hflB, encoding a membrane- associated ATPase and protease that is required for mRNA decay

Journal of Bacteriology

Volumn 180, Issue 7, 1998, Pages 1929-1938

  Wang, Rong Fu ^a,b   O'Hara, Eileen B ^a   Aldea, Marti ^a,c   Bargmann, Cornelia I ^a,d   Gromley, Heather ^a   Kushner, Sidney R ^a  

^a University of Georgia ^*  (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF LLEIDA   (Spain)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GLUTATHIONE TRANSFERASE; PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL GROWTH; DATA ANALYSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; RNA ANALYSIS; START CODON; TEMPERATURE SENSITIVITY;

ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0031894053     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.7.1929-1938.1998     Document Type: Article

References (84)

1. Akiyama, Y., A. Kihara, and K. Ito. 1996. Subunit a of proton ATPase F0 sector is a substrate of the FtsH protease in Escherichia coli. FEBS Lett. 399: 26-28.
2. Akiyama, Y., Y. Shirai, and K. Ito. 1994. Involvement of FtsH in protein assembly into and through the membrane. II. Dominant mutations affecting FtsH functions. J. Biol. Chem. 269:5225-5229.
3. Apirion, D. 1973. Degradation of RNA in Escherichia coli: a hypothesis. Mol. Gen. Genet. 122:313-322.
4. Apirion, D., and A. B. Lasser. 1978. A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J. Biol. Chem. 253: 1738-1742.
5. Applied Biosystems. 1986. User bulletin no. 25, November. Applied Biosystems, Foster City, Calif.
6. Arraiano, C. M., S. D. Yancey, and S. R. Kushner. 1993. Identification of endonucleolytic cleavage sites involved in decay of Escherichia coli trxA mRNA. J. Bacteriol. 175:1043-1052.
7. Arraiano, C. M., S. D. Yancey, and S. R. Kushner. 1988. Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J. Bacteriol. 170:4625-4633.
8. Babitzke, P., L. Granger, and S. R. Kushner. 1993. Analysis of mRNA decay and rRNA processing in Escherichia coli multiple mutants carrying a deletion in RNase III. J. Bacteriol. 175:229-239.
9. Babitzke, P., and S. R. Kushner. 1991. The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 88:1-5.
10. Banuett, F., M. A. Hoyt, L. McFarlane, H. Echols, and I. Herskowitz. 1986. hflB, a new Escherichia coli locus regulating lysogeny and the level of bacteriophage lambda cII protein. J. Mol. Biol. 187:213-224.
11. Bardwell, J. C. A., P. Regnier, S.-M. Chen, Y. Nakamura, M. Grunberg-Manago, and D. L. Court. 1989. Autoregulation of RNase III operon by mRNA processing. EMBO J. 8:3401-3407.
12. Belasco, J., and G. Brawerman. 1993. Control of messenger RNA stability. Academic Press, New York, N.Y.
13. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
14. Cao, G.-J., and N. Sarkar. 1992. Identification of the gene for an Escherichia coli poly(A) polymerase. Proc. Natl. Acad. Sci. USA 89:10380-10384.
15. Carafa, Y. A., E. Brody, and C. Thermes. 1990. Prediction of rho-independent Escherichia coli transcription terminators. J. Mol. Biol. 216:835-858.
16. Carpousis, A. J., G. Van Houwe, C. Ehretsmann, and H. M. Krisch. 1994. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76:889-900.
17. Claverie-Martin, F., M. R. Diaz-Torres, S. D. Yancey, and S. R. Kushner. 1989. Cloning of the altered mRNA stability (ams) gene of Escherichia coli K-12. J. Bacteriol. 171:5479-5486.
18. de Boer, P. A. J., R. E. Crossley, A. R. Hand, and L. I. Rothfield. 1991. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10:4371-4380.
19. DeMarini, D. J., M. Winey, D. Ursic, F. Webb, and M. R. Culbertson. 1992. SEN1, a positive effector of tRNA-splicing endonuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2154-2164.
20. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
21. Dubiel, W., K. Ferrell, G. Pratt, and M. Rechsteiner. 1992. Subunit 4 of the 26S protease is a member of a novel eukaryotic ATPase family. J. Biol. Chem. 267:22699-22702.
22. Eakle, K. A., M. Bernstein, and S. D. Emr. 1988. Characterization of a component of the yeast secretion machinery: identification of the SEC18 gene product. Mol. Cell. Biol. 8:4098-4109.
23. Erdmann, R., F. F. Wiebel, A. Flessau, J. Rytka, A. Beyer, K.-U. Frohlich, and W.-H. Kunau. 1991. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 64: 499-510.
24. Figurski, D., R. Meyer, D. S. Miller, and D. R. Helinski. 1976. Generation in vitro of deletions in the broad host range plasmid RK2 using phage Mu insertions and a restriction endonuclease. Gene 1:107-119.
25. Frohlich, K.-U., H.-W. Fries, M. Rudiger, R. R. Erdmann, D. D. Bolstein, and D. Mecke. 1991. Yeast cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation and gene expression. J. Cell Biol. 114:443-453.
26. Georgellis, D., B. Sohlberg, F. U. Hartl, and A. von Gabain. 1995. Identification of GroEL as a constitutent of an mRNA-protection complex in Escherichia coli. Mol. Microbiol. 16:1259-1268.
27. Ghislain, M., A. Udvardy, and C. Mann. 1993. S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 366:358-362.
28. Ghora, B. K., and D. Apirion. 1978. Structural analysis and in vitro processing to p5 (5S) rRNA of a 9S RNA molecule isolated from an me mutant of E. coli. Cell 15:1055-1066.
29. Gordon, C., G. McGurk, P. Dillon, C. Rosen, and N. D. Hastle. 1993. Defective mitosis due to a mutation in a gene for a fission yeast 26S protease subunit. Nature 366:355-357.
30. Graham, T. R., and S. D. Emr. 1991. Compartmental organization of Golgispecific protein modification and vacuolar protein sorting events defined in a yeast sec18(NSF) mutant. J. Cell Biol. 114:207-218.
31. Granger, L. L., E. B. O'Hara, R.-F. Wang, F. V. Meffen, K. Armstrong, S. D. Yancey, P. Babitzke, and S. R. Kushner. 1998. The Escherichia coli mrsC gene is required for cell growth and mRNA decay. J. Bacteriol. 180:1920-1928.
32. Guyer, M. S. 1978. The γδ sequence of F is an insertion sequence. J. Mol. Biol. 126:347-350.
33. Henikoff, S. 1987. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 155:156-165.
34. Herman, C., T. Ogura, T. Tomoyasu, S. Hiraga, Y. Akiyama, K. Ito, R. Thomas, R. D'Ari, and P. Bouloc. 1993. Cell growth and λ phage development controlled by the same essential Escherichia coli gene, ftsH/hflB. Proc. Natl. Acad. Sci. USA 90:10861-10865.
35. 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA 92:3516-3520.
36. Kahn, M., R. Kolter, C. Thomas, D. Figurski, R. Meyer, E. Remaut, and D. R. Helinski. 1979. Plasmid cloning vehicles derived from plasmids ColE1, F, R6K, and RK2. Methods Enzymol. 68:268-280.
37. Kihara, A., Y. Akiyama, and K. Ito. 1995. FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc. Natl. Acad. Sci. USA 92:4532-4536.
38. Koller, K. J., and M. J. Brownstein. 1987. Use of a cDNA clone to identify a supposed precursor protein containing valosin. Nature 325:542-545.
39. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
40. Leeds, P., J. M. Wood, B.-S. Lee, and M. R. Culbertson. 1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2165-2177.
41. Lin-Chao, S., and S. Cohen. 1991. The rate of processing and degradation of antisense RNA I regulates the replication of ColE1-type plasmids in vivo. Cell 65:1233-1242.
42. Liu, Q., S. D. Yancey, and S. R. Kushner. Unpublished results.
43. Mackie, G. A. 1991. Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the products of the ams gene in vivo and in vitro. J. Bacteriol. 173:2488-2497.
44. Maniatis, T., E. F. Fristch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
45. Melefors, O., and A. von Gabain. 1988. Site-specific endonucleolytic cleavages and the regulation of stability of E. coli ompA mRNA. Cell 52:893-901.
46. Miczak, A., V. R. Kaberdin, C.-L. Wei, and S. Lin-Chao. 1996. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. USA 93:3865-3869.
47. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
48. Mudd, E. A., H. M. Krisch, and C. F. Higgins. 1990. RNase E, an endoribonuclease, has a general role in the chemical decay of Escherichia coli mRNA: evidence that me and ams are the same genetic locus. Mol. Microbiol. 4:2127-2135.
49. Mudd, E. A., P. Prentki, D. Belin, and H. M. Krisch. 1988. Processing of unstable bacteriophage T4 32 mRNAs into a stable species requires Escherichia coli ribonuclease E. EMBO J. 7:3601-3607.
50. Mulligan, M. E., D. K. Hawley, R. Entriken, and W. R. McClure. 1984. Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity. Nucleic Acids Res. 12:789-800.
51. Murthy, K. G. K., P. Park, and J. L. Manley. 1991. A nuclear micrococcal-sensitive, ATP-dependent exoribonuclease degrades uncapped but not capped RNA substrates. Nucleic Acids Res. 19:2685-2692.
52. Nelbock, P., P. J. Dillon, A. Perkins, and C. A. Rosen. 1990. A cDNA for a protein that interacts with the human deficiency virus Tat transactivator. Science 248:1650-1653.
53. O'Hara, E. B., J. A. Chekanova, C. A. Ingle, Z. R. Kushner, E. Peters, and S. R. Kushner. 1995. Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc. Natl. Acad. Sci. USA 92:1807-1811.
54. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
55. Peters, J.-M., M. J. Walsh, and W. W. Franke. 1990. An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J. 9:1757-1767.
56. Py, B., H. Causton, E. A. Mudd, and C. F. Higgins. 1994. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14:717-729.
57. Py, B., C. F. Higgins, H. M. Krisch, and A. J. Carpousis. 1996. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381:169-172.
58. Reddy, P., A. Peterkofsky, and K. McKenney. 1985. Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG codon to GUG or AUG results in increased gene expression. Proc. Natl. Acad. Sci. USA 85:5656-5660.
59. Regnier, P., M. Grunberg-Manago, and C. Portier. 1987. Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. J. Biol. Chem. 262:63-68.
60. Regnier, P., and C. Portier. 1986. Initiation attenuation and RNase III processing of transcripts from the Escherichia coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J. Mol. Biol. 187: 23-32.
61. Reinstein, J., M. Brune, and A. Wittinghofer. 1988. Mutations in the nucleotide binding loop of adenylate kinase of Escherichia coli. Biochemistry 27: 4712-4720.
62. Sancar, A., A. M. Hack, and W. D. Rupp. 1979. Simple method for purification of plasmid-coded proteins. J. Bacteriol. 137:692-693.
63. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
64. Saraste, M., P. R. Sibbald, and W. Wittinghofer. 1990. The P-loop - a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15: 430-434.
65. Seeley, T. W., and L. Grossman. 1989. Mutations in the Escherichia coli UvrB ATPase motif compromise excision repair capacity. Proc. Natl. Acad. Sci. USA 86:6577-6581.
66. Shibuya, H., K. Irie, J. Ninomiya-Tsuji, M. Goebl, T. Taniguchi, and K. Matsumoto. 1992. New human gene encoding a positive modulator of HIV Tat-mediated transactivation. Nature 357:700-702.
67. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
68. Stitt, B. L., and M. R. Webb. 1986. Absence of a phosphorylated intermediate during ATP hydrolysis by Escherichia coli transcription termination protein Rho. J. Biol. Chem. 261:15906-15909.
69. Stoker, N. G., N. F. Fairweather, and B. G. Spratt. 1982. Versatile low-copy-number plasmid vectors for cloning in Escherichia coli. Gene 18:335-341.
70. Sung, P., D. Higgins, L. Prakash, and S. Prakash. 1988. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activity but not the ability to bind ATP. EMBO J. 7:3263-3269.
71. Swaffield, J. C., J. F. Bromberg, and S. A. Johnston. 1992. Alterations in a yeast protein resembling HIV Tat-binding protein relieve requirement for an acidic activation domain in GAL4. Nature 357:698-700.
72. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
73. Taylor, M., and C. Yanofsky. 1964. Transformation of bacterial markers and transfer of a phage marker with DNA isolated from a φ80 hybrid phage carrying the tryptophan genes of E. coli. Biochem. Biophys. Res. Commun. 17:798-804.
74. Tomcsanyi, T., and D. Apirion. 1985. Processing enzyme ribonuclease E specifically cleaves RNA I, an inhibitor of primer formation in plasmid DNA synthesis. J. Mol. Biol. 185:713-720.
75. 32. EMBO J. 14:2551-2560.
76. Tomoyasu, T., K. Yamanaka, K. Murata, T. Suzaki, P. Bouloc, A. Kato, H. Niki, S. Hiraga, and T. Ogura. 1993. Topology and subcellular localization of FtsH protein in Escherichia coli. J. Bacteriol. 175:1352-1357.
77. Tomoyasu, T., T. Yuki, S. Morimura, H. Mori, K. Yamanaka, J. Niki, and S. Hiraga. 1993. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175:1344-1351.
78. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and expression in Escherichia coli. Gene 100:195-199.
79. Wang, R. F., R. R. Dickson, and S. R. Kushner. Unpublished results.
80. Williams, M. G., and P. Rogers. 1987. Expression of arg genes in Escherichia coli during arginine limitation dependent upon stringent control of translation. J. Bacteriol. 169:1644-1650.
81. Wilson, D. W., C. A. Wilcox, G. C. Flynn, C. Ellson, W.-J. Kuang, W. J. Henzel, M. R. Block, A. Ullrich, and J. E. Rothman. 1989. A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature 339:355-359.
82. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
83. Zhang, J., and M. P. Deutscher. 1989. Analysis of the upstream region of the Escherichia coli md gene encoding RNase D. J. Biol. Chem. 264:18228-18233.
84. Zhang, J., and M. P. Deutscher. 1988. Escherichia coli RNase D: sequencing of the rnd structural gene and purification of the overexpressed protein. Nucleic Acids Res. 16:6265-6278.