Information de reference pour ce titreAccession Number: | 00005797-200102040-00021.
|
Author: | Balandina, Anna 1 3; Claret, Laurent 1 4; Hengge-Aronis, Regine 2; Rouviere-Yaniv, Josette 1 1
|
Institution: | (1)Laboratoire de Physiologie Bacterienne, CNRS, UPR 9073, Institut de Biologie Physico-Chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France. (2)Institute of Biology-Microbiology, Freie Universitat Berlin, Konigin-Luise-Strasse 12-16a, 14195 Berlin, Germany.
|
Title: | |
Source: | Molecular Microbiology. 39(4):1069-1079, February 2001.
|
Abstract: | Escherichia coli HU protein is a major component of the bacterial nucleoid. HU stabilizes higher order nucleoprotein complexes and belongs to a family of DNA architectural proteins. Here, we report that HU is required for efficient expression of the sigma S subunit of RNA polymerase. This rpoS-encoded alternative [sigma]S factor induces a number of genes implicated in cell survival in stationary phase and in multiple stress resistance. By analysis of rpoS-lacZ fusions and by pulse-chase experiments, we show that the efficiency of rpoS translation is reduced in cells lacking HU, whereas neither rpoS transcription nor protein stability is affected by HU. Gel mobility shift assays show that HU is able to bind specifically an RNA fragment containing the translational initiation region of rpoS mRNA 1000-fold more strongly than double-stranded DNA. Together with the in vivo data, this finding strongly suggests that, by binding to rpoS mRNA, HU directly stimulates rpoS translation. We demonstrate here that HU, an abundant DNA-binding, histone-like protein, is able specifically to recognize an RNA molecule and therefore play a role in post-transcriptional regulation.
(C) 2001 Blackwell Science Ltd.
|
References: | Aki, T., and Adhya, S. (1997) Repressor induced site-specific binding of HU for transcriptional regulation. EMBO J 16: 3666-3674.
Altuvia, S., Weinstein-Fisher, D., Zhang, A., Postow, L., and Storz, G. (1997) A small, stable RNA induced by oxidative stress: roles as a pleiotropic regulator and antimutator. Cell 90: 43-53.
Barth, M., Marschall, C., Muffler, A., Fischer, D., and Hengge-Aronis, R. (1995) A role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of [sigma]S and many [sigma]S dependent genes in Escherichia coli. J Bacteriol 177: 3455-3464.
Becker, G., Klauck, E., and Hengge-Aronis, R. (1999) Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci USA 96: 6439-6444.
Bensaid, A., Almeida, A., Drlica, K., and Rouviere-Yaniv, J. (1996) Cross-talk between topoisomerase I and HU in Escherichia coli. J Mol Biol 256: 292-300.
Bonnefoy, E., Takahashi, M., and Rouviere-Yaniv, J. (1994) DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J Mol Biol 242: 116-129.
Boubrik, F., and Rouviere-Yaniv, J. (1995) Increased sensitivity to gamma irradiation in bacteria lacking protein HU. Proc Natl Acad Sci USA 92: 3958-3962.
Bramhill, D., and Kornberg, A. (1988) A model for initiation at origins of DNA replication. Cell 54: 915-918.
Brown, L., and Elliott, T. (1996) Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178: 3763-3770.
Brown, L., and Elliott, T. (1997) Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in S. typhimurium. J Bacteriol 179: 656-662.
Castaing, B., Zelwer, C., Laval, J., and Boiteux, S. (1995) HU protein of E. coli binds specifically to DNA that contains single-strand breaks or gaps. J Biol Chem 270: 10291-10296.
Claret, L., and Rouviere-Yaniv, J. (1997) Variation in HU composition during growth of E. coli: the heterodimer is required for long term survival. J Mol Biol 273: 93-104.
Cusick, M., and Belfort, M. (1998) Domain structure and RNA annealing activity of the Escherichia coli regulatory protein StpA. Mol Microbiol 28: 847-857.
Deighan, P., Free, A., and Dorman, C.J. (2000) A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression trough modulation of micF RNA stability. Mol Microbiol 38: 126-139.
Dri, A., Moreau, P., and Rouviere-Yaniv, J. (1992) Role of the histone-like proteins OsmZ and HU in homologous recombination. Gene 120: 11-16.
Drlica, K., and Rouviere-Yaniv, J. (1987) Histone-like proteins of bacteria. Microbiol Rev 51: 301-319.
Falconi, M., Gualtieri, M.T., La Teana, A., Losso, M.A., and Pon, C.L. (1988) Proteins from the procaryotic nucleoid: primary and quaternary structure of the 15 kDa Escherichia coli DNA-binding protein H-NS. Mol Microbiol 2: 323-329.
Huisman, O., Faelen, M., Girard, D., Jaffe, A., and Rouviere-Yaniv, J. (1989) Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol 171: 3704-3712.
Ito, K., Bassford, P.J., and Beckwith, J. (1981) Protein localization in E. coli: in the secretion of periplasmic and outer-membrane proteins? Cell 24: 707-717.
Itoh, K., Takiyama, N., Kasen, R., Kondoh, K., Sano, A., and Oshima, A. (1993) Purification and characterization of human lysosomal protective protein expressed in stably transformed chinese hamster ovary cells. J Biol Chem 268: 1180-1186.
Kamashev, D., and Rouviere-Yaniv, J. (2000) The histone-like protein HU binds specifically to DNA recombination and repair intermediates. EMBO J 19: 6527-6535.
Kamashev, D., Balandina, A., and Rouviere-Yaniv, J. (1999) The binding motif recognized by HU on both nicked and cruciform DNA. EMBO J 18: 5434-5444.
Lange, R., and Hengge-Aronis, R. (1991) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5: 49-59.
Lange, R., and Hengge-Aronis, R. (1994) The cellular concentration of the [sigma]S subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev 8: 1600-1612.
Lavoie, B.D., and Chaconas, G. (1993) Site-specific HU binding in the Mu transpososome: conversion of a sequence-independent DNA-binding protein into chemical nuclease. Genes Dev 7: 2510-2519.
Lavoie, B.D., Shaw, G.S., Millner, A., and Chaconas, G. (1996) Anatomy of a flexer-DNA complex inside a higher-order transposition intermediate. Cell 85: 761-771.
Leese, R.A., Cusick, M.E., and Belfort, M. (1998) Riboregulation in Escherichia coli: dsrA RNA acts by RNA: RNA interactions at multiple loci. Proc Natl Acad Sci USA 95: 12456-12461.
Lewis, D.E., Geanacopoulos, M., and Adhya, S. (1999) Role of HU and DNA supercoiling in transcription repression: specialized nucleoprotein complex at gal promoters in Escherichia coli. Mol Microbiol 31: 451-461.
Loewen, P.C., and Hengge-Aronis, R. (1994) The role of the sigma factor [sigma]S (KatF) in bacterial global regulation. Annu Rev Microbiol 48: 53-80.
Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T., and Gottesman, S. (1998) DsrA RNA regulates translation of RpoS message by an antisilencer of transcription. Proc Natl Acad Sci USA 95: 12462-12467.
Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Muffler, A., Fisher, D., Altuvia, S., Storz, G., and Hengge-Aronis, R. (1996a) The response regulator RssB controls stability of the [sigma]S subunit of RNA polymerase in Escherichia coli. EMBO J 15: 1333-1339.
Muffler, A., Fischer, D., and Hengge-Aronis, R. (1996b) The RNA-binding protein HF-I, known as a host factor for Q[beta] RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10: 1143-1151.
Muffler, A., Traulsen, D.D., Lange, R., and Hengge-Aronis, R. (1996c) Post-transcriptional osmotic regulation of the [sigma]S subunit of RNA polymerase in Escherichia coli. J Bacteriol 178: 1607-1613.
Nakamura, K., Yahagi, S., Yamazaki, T., and Yamane, K. (1999) Bacillus subtilis histone-like protein, HBsu, is an integral component of a SRP-like particle that can bind the Alu domain of small cytoplasmic RNA. J Biol Chem 274: 13569-13576.
Nguyen, I.H., Jensen, D.B., Thompson, N.E., Gentry, D.R., and Burgess, R.R. (1993) In vitro functional characterisation of overproduced Escherichia coli KatF/ rpoS gene product. Biochemistry 19: 11112-11117.
Oberto, J., and Rouviere-Yaniv, J. (1996) Serratia marsescens contains a heterodimeric HU protein like Escherichia coli and Salmonella typhimurium. J Bacteriol 178: 293-297.
Oberto, J., Drlica, K., and Rouviere-Yaniv, J. (1994) Histones, HMG, HU, IHF: meme combat. Biochimie 76: 901-908.
Painbeni, E., Mouray, E., Gottesman, S., and Rouviere-Yaniv, J. (1993) An imbalance of HU synthesis induces mucoidy in Escherichia coli. J Mol Biol 234: 1021-1037.
Painbeni, E., Caroff, M., and Rouviere-Yaniv, J. (1997) Alterations of the outer membrane composition in Escherichia coli lacking the histone-like protein HU. Proc Natl Acad Sci USA 94: 6712-6717.
Pellegrini, O., Oberto, J., Pinson, V., Wery, M., and Rouviere-Yaniv, J. (2000) Overproduction and improved strategies to purify the three native forms of nuclease-free HU protein. Biochimie 82: 1-13.
Pinson, V., Takahashi, M., and Rouviere-Yaniv, J. (1999) Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA. J Mol Biol 287: 485-497.
Pontiggia, A., Negri, A., Beltrame, M., and Bianchi, M.E. (1993) Protein HU binds specifically to kinked DNA. Mol Microbiol 7: 343-350.
Powell, B.S., Court, D.L., Nakamura, Y., Rivas, M.P., and Turnbough, Jr (1994) Rapid conformation of single copy lambda prophage integration by PCR. Nucleic Acids Res 22: 5765-5766.
Pratt, L.A., and Silhavy, T.J. (1996) The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci USA 93: 2488-2492.
Rockabrand, D., Livers, K., Austin, T., Kaiser, R., Jensen, D., Burgess, R., and Blum, P. (1998) Roles of DnaK and RpoS in starvation-induced thermotolerance of Escherichia coli. J Bacteriol 180: 846-854.
Rouviere-Yaniv, J. (1978) Localization of HU protein in the E. coli nucleoid. Cold Spring Harbor Symp Quant Biol 42: 439-447.
Rouviere-Yaniv, J., and Gros, F. (1975) Characterization of a novel, low-molecular weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci USA 72: 3428-3432.
Rouviere-Yaniv, J., and Kjeldgaard, N.O. (1979) Native Escherichia coli HU protein is a heterotypic dimer. FEBS Lett 106: 297-300.
Rouviere-Yaniv, J., Yaniv, M., and Germond, J.E. (1979) Escherichia coli DNA-binding protein HU forms nucleosome-like structure with circular double stranded DNA. Cell 17: 265-274.
Schweder, T., Lee, K.H., Lomovskaya, O., and Matin, A. (1996) Regulation of Escherichia coli starvation sigma factor ([sigma]S) by ClpXP protease. J Bacteriol 178: 470-476.
Sledjeski, D.D., Gupta, A., and Gottesman, S. (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15: 3993-4000.
Touati, E., Dassa, E., Dassa, J., Boquet, P.L., and Touati, D. (1991) Are appR and katF the same Escherichia coli gene encoding a new sigma transcription initiation factor? Res Microbiol 142: 29-36.
Wada, M., Kano, Y., Ogawa, T., Okasaki, T., and Imamoto, F. (1988) Construction and characterisation of the deletion mutant of huA and hupB genes in Escherichia coli. J Mol Biol 204: 581-591.
Yamashino, T., Ueguchi, C., and Mizuno, T. (1995) Quantitative control of the stationary phase-specific sigma factor, [sigma]S in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J 14: 594-602.
Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R., and Storz, G. (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17: 6061-6068.
Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule. Science 244: 48-52.
|
Language: | English.
|
Document Type: | Research Articles.
|
Journal Subset: | Life Sciences.
|
ISSN: | 0950-382X
|
NLM Journal Code: | mom, 8712028
|
Annotation(s) | |
|
|