Genetica

, Volume 97, Issue 3, pp 363–378

How is osmotic regulation of transcription of the Escherichia coli proU operon achieved?

A review and a model
  • J. Gowrishankar
  • Dipankar Manna
Article

Abstract

The proU operon in enterobacteria encodes a binding-protein-dependent transporter for the active uptake of glycine betaine and L-proline, and serves an adaptive role during growth of cells in hyperosmolar environments. Transcription of proU is induced 400-fold under these conditions, but the underlying signal transduction mechanisms are incompletely understood. Increased DNA supercoiling and activation by potassium glutamate have each been proposed in alternative models as mediators of proU osmoresponsivity. We review here the available experimental data on proU regulation, and in particular the roles for DNA supercoiling, potassium glutamate, histone-like proteins of the bacterial nucleoid, and alternative sigma factors of RNA polymerase in such regulation. We also propose a new unifying model, in which the pronounced osmotic regulation of proU expression is achieved through the additive effects of at least three separate mechanisms, each comprised of a cis element [two promoters P1 and P2, and negative-regulatory-element (NRE) downstream of both promoters] and distinct trans-acting factors that interact with it: stationary-phase sigma factor RpoS with P1, nucleoid proteins HU and IHF with P2, and nucleoid protein H-NS with the NRE. In this model, potassium glutamate may activate proU expression through each of the three mechanisms whereas DNA supercoiling has a very limited role, if any, in the osmotic induction of proU transcription. We also suggest that proU may be a virulence gene in the pathogenic enterobacteria.

Key words

proU osmoregulation Escherichia coli HNS HU IHF RpoS supercoiling 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altuvia, S., M., Almirón, G., Huisman, R., Kolter & G., Storz, 1994. The dps promoter is activated by OxyR during growth and by IHF and 374–1 in stationary phase. Mol. Microbiol. 13: 265–272.Google Scholar
  2. Ames, G.F.-L., C.S., Mimura & V., Shyamala, 1990. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: traffic ATPases. FEMS Microbiol. Rev. 75: 429–446.Google Scholar
  3. Arnqvist, A., A., Olsen & S., Normark, 1994. 374–2-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by 374–3 in the absence of the nucleoidassociated protein H-NS. Mol. Microbiol. 13: 1021–1032.Google Scholar
  4. Barron, A., J.U., Jung & M., Villarejo, 1987. Purification and characterization of a glycine betaine binding protein from Escherichia coli. J. Biol. Chem. 262: 11841–11846.Google Scholar
  5. Borowiec, J.A. & J.D., Gralla, 1985. Supercoiling response of the lacPs promoter in vitro. J. Mol. Biol. 184: 587–598.Google Scholar
  6. Borowiec, J.A. & J.D., Gralla, 1987. All three elements of the lacPs promoter mediate its transcriptional response to DNA supercoiling. J. Mol. Biol. 195: 89–97.Google Scholar
  7. Brown, A.D., 1976. Microbial water stress. Bacteriol. Rev. 40: 803–846.Google Scholar
  8. Calrney, J., I.R., Booth & C.F., Higgins, 1985. Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. J. Bacteriol. 164: 1224–1232.Google Scholar
  9. Cayley, S., B.A., Lewis, H.J., Guttman & M.T., RecordJr., 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: implications for protein-DNA interactions in vivo. J. Mol. Biol. 222: 281–300.Google Scholar
  10. Cayley, S., B.A., Lewis & M.T., RecordJr., 1992. Origins of the osmoprotective properties of betaine and proline in Escherichia coli K-12. J. Bacteriol. 174: 1586–1595.Google Scholar
  11. Chambers, S.T. & C.M., Kunin, 1987. Isolation of glycine betaine and proline betaine from human urine. Assessment of their role as osmoprotective agents for bacteria and the kidney. J. Clin. Invest. 79: 731–737.Google Scholar
  12. Chambers, S.T., C.M., Kunin, D., Miller & A., Hamada, 1987. Dimethylthetin can substitute for glycine betaine as an osmoprotectant molecule for Escherichia coli. J. Bacteriol. 169: 4845–4847.Google Scholar
  13. Christian, J.H.B., 1955. The influence of nutrition on the water relations of Salmonella oranienburg. Aust. J. Biol. Sci. 8: 75–82.Google Scholar
  14. Claverie-Martin, F. & B., Magasanik, 1991. Role of integration host factor in the regulation of the glnHp2 promoter of Escherichia coli. Proc. Natl. Acad. Sci. USA 88: 1631–1635.Google Scholar
  15. Csonka, L.N., 1982. A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotie strength, J. Bacteriol. 151: 1433–1443.Google Scholar
  16. Csonka, L.N., 1989. Regulation of cytoplasmic proline levels in Salmonella typhimurium: effect of osmotic stress on synthesis, degradation and cellular retention of proline. J. Bacteriol. 170: 2374–2378.Google Scholar
  17. Csonka, L.N., 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53: 121–147.Google Scholar
  18. Csonka, L.N. & A.D., Hanson, 1991. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbial. 45: 569–606.Google Scholar
  19. Culham, D.E., K.S., Emmerson, B., Lasby, D., Mamelak, B.A., Steer, C.L., Gyles, M., Villarejo & J.M., Wood, 1994. Genes encoding osmoregulatory proline/glycine betaine transporters and the proline catabolic system are present and expressed in diverse clinical Escherichia coli isolates. Can. J. Microbiol. 40: 397–402.Google Scholar
  20. Dattananda, C.S. & J., Gowrishankar, 1989. Osmoregulation in Escherichia coli: complementation analysis and gene-protein relationships in the proU locus. J. Bacteriol. 171: 1915–1922.Google Scholar
  21. Dattananda, C.S., K., Rajkumari & J., Gowrishankar, 1991. Multiple mechanisms contribute to osmotic inducibility of proU operon expression in Escherichia coli: two osmoresponsive promoters and a negative regulatory element within the first structural gene. J. Bacteriol. 173: 7481–7490.Google Scholar
  22. Dayn, A., S., Malkhosyan, D., Duzhy, V., Lyamichev, Y., Panchenko & S., Mirkin, 1991. Formation of (dA-dT)n cruciforms in Escherichia coli cells under different environmental conditions. J. Bacteriol. 173: 2658–2664.Google Scholar
  23. del, Castillo, I., J.M., Gomez & F., Moreno, 1990. mprA, an Escherichia coli gene that reduces growth-phase-dependent synthesis of microcins B17 and C7 and blocks osmoinduction of proU when cloned on a high-copy-number plasmid. J. Bacteriol. 172: 437–445.Google Scholar
  24. del, Castillo, I., J.E., González-Pastor, J.L.S., Millan & F., Moreno, 1991. Nucleotide sequence of the Escherichia coli regulatory gene mprA and construction and characterization of mprA-deficient mutants. J. Bacteriol. 173: 3924–3929.Google Scholar
  25. Dersch, P., S., Kneip & E., Bremer, 1994. The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol. Gen. Genet. 245: 255–259.Google Scholar
  26. Dersch, P., K., Schmidt & E., Bremer, 1993. Synthesis of the Escherichia coli K-12 nucleoid-associated DNA-binding protein H-NS is subjected to growth-phase control and autoregulation. Mol. Microbiol. 8: 875–889.Google Scholar
  27. DiNardo, S., K.A., Voelkel, R., Sternglanz, A.E., Reynolds & A., Wright, 1982. Escherichia coli DNA topoisomerase 1 mutants have compensatory mutations in DNA gyrase genes. Cell 31: 43–51.Google Scholar
  28. Dorman, C.J., A.S., Lynch, N., Ni Bhriain & C.F., Higgins, 1989. DNA supercoiling in Escherichia coli: topA mutations can be suppressed by amplifications involving the tolC locus. Mol. Microbiol. 3: 531–540.Google Scholar
  29. Dorman, C.J., N.Ni, Bhriain & C.F., Higgins, 1990. DNA supercoiling and the environmental regulation of virulence gene expression in Shigella flexneri. Nature (London) 344: 789–792.Google Scholar
  30. Drew, H.R., J.R., Week & A.A., Travers, 1985. Negative supercoiling induces spontaneous unwinding of a bacterial promoter. EMBO J. 4: 1025–1032.Google Scholar
  31. Drlica, K. & J., Rouviere-Yaniv, 1987. Histonelike proteins of bacteria. Microbiol. Rev. 51: 301–319.Google Scholar
  32. Druger-Liotta, J., V.J., Prange, D.G., Overdier & L.N., Csonka, 1987. Selection of mutations that alter osmotic control of transcription, of the Salmonella typhimurium proU operon. J. Bacteriol. 169: 2449–2459.Google Scholar
  33. Dunlap, V.J. & L.N., Csonka, 1985. Osmotic regulation of L-proline transport in Salmonella typhimurium. J. Bacteriol. 163: 296–304.Google Scholar
  34. Epstein, W., 1986. Osmoregulation by potassium transport in Escherichia coli. FEMS Mirobiol. Rev. 39: 73–78.Google Scholar
  35. Epstein, W. & S.G., Schultz, 1965. Cation transport in Escherichia coli. V. Regulation of cation content. J. Gen. Physiol. 49: 221–234.Google Scholar
  36. Espinosa-Urgel, M. & A., Tormo, 1993. 375–1 promoters in Escherichia coli are located in DNA regions with intrinsic curvature. Nucleic Acids Res. 21: 3667–3670.Google Scholar
  37. Faatz, E., A., Middendorf & E., Bremer, 1988. Cloned structural genes for the osmotically regulated binding-protein-dependent glycine betaine transport system (ProU) of Escherichia coli K-12. Mol. Microbiol. 2: 265–279.Google Scholar
  38. Falconi, M., N.P., Higgins, R., Spurio, C.L., Pon & C.O., Gualerzi, 1993. Expression of the gene encoding the major bacterial nucleoid protein H-NS is subject to transcriptional autorepression. Mol. Microbiol. 10: 273–282.Google Scholar
  39. Fang, F.C., S.J., Libby, N.A., Buchmeier, P.C., Loewen, J., Switala, J., Harwood & D.C., Guiney, 1992. The alternative σ factor KatF (RpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. USA 89: 11978–11982.Google Scholar
  40. Forsberg, A.J., G.D., Pavitt & C.F., Higgins, 1994. Use of transcriptional fusions to monitor gene expression: a cautionary tale. J. Bacteriol. 176: 2128–2132.Google Scholar
  41. Freundlich, M., N., Ramani, E., Mathew, A., Sirko & P., Tsui, 1992. The role of integration host factor in gene expression in Escherichia coli. Mol. Microbiol. 6: 2557–2563.Google Scholar
  42. Goodman, S.D., S.C., Nicholson & H.A., Nash, 1992. Deformation of DNA during site-specific recombination of bacteriophage λ: replacement of IHF protein by HU protein or sequence-directed bends. Proc. Natl. Acad. Sci. USA 89: 11910–11914.Google Scholar
  43. Goodrich, J.A., M.L., Schwartz & W.R., McClure, 1990. Searching for and predicting the activity of sites for DNA binding proteins: compilation and analysis of the binding sites for Escherichia coli integration host factor (IHF). Nucleic Acids Res. 18: 4993–5000.Google Scholar
  44. Göransson, M., B., Sonden, P., Nilsson, B., Dagberg, K., Forsman, K., Emanuelsson & B.E., Uhlin, 1990. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature (London) 34: 682–685.Google Scholar
  45. Gowrishankar, J., 1985. Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J. Bacteriol. 164: 434–445.Google Scholar
  46. Gowrishanhar, J., 1986. proP-mediated proline transport also plays a role in Escherichia coli osmoregulation. J. Bacteriol. 166: 331–333.Google Scholar
  47. Gowrishankar, J., 1989. Nucleotide sequence of the osmoregulatory proU operon of Escherichia coli. J. Bacteriol. 171: 1923–1931. Erratum. 1990. 172: 1165.Google Scholar
  48. Gowrishankar, J., P., Jayashree & K., Rajkumari, 1986. Molecular cloning of an osmoregulatory locus in Escherichia coli: increased proU gene dosage results in enhanced osmotolerance. J. Bacteriol. 168: 1197–1204.Google Scholar
  49. Graeme-Cook, K.A., G., May, E., Bremer & C.F., Higgins, 1989. Osmotic regulation of porin expression: a role for DNA supercoiling. Mol. Microbiol. 3: 1287–1294.Google Scholar
  50. Gutierrez, F., J., Barondess, C., Manoil & J., Beckwith, 1987. The use of transposon TnphoA to detect genes for cell envelope proteins subject to common regulatory stimulus. J. Mol. Biol. 195: 289–297.Google Scholar
  51. Haardt, M., B., Kempf, E., Faatz & E., Bremer, 1995. The osmoprotectant proline betaine is a major substrate for the binding-protein-dependent transport system ProU of Escherichia coli K-12. Mol. Gen. Genet. 246: 783–786.Google Scholar
  52. Haniford, D.B. & D.E., Pulleyblank, 1985. Transition of a cloned d(AT)n-d(AT)n tract to a cruciform in vivo. Nucleic Acids Res. 13: 4343–4363.Google Scholar
  53. Harrison, J.A., D., Pickard, C.F., Higgins, A., Khan, S.N., Chatfield, T., Ali, C.J., Dorman, C.E., Hormaeche & G., Dougan, 1994. Role of hns in the virulence phenotype of pathogenic Salmonellae. Mol. Microbiol. 13: 133–140.Google Scholar
  54. Hengge-Aronis, R. & D., Fischer, 1992. Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol. Microbiol. 6: 1877–1886.Google Scholar
  55. Hengge-Aronis, R., W., Klein, R., Lange, M., Remmele & W., Boos, 1991. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J. Bacteriol. 173: 7918–7924.Google Scholar
  56. Hengge-Aronis, R., R., Lange, N., Henneberg & D., Fischer, 1993. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J. Bacteriol. 175: 259–265.Google Scholar
  57. Higgins, C.F., J., Cairney, D.A., Stirling, L., Sutherland & I.R., Booth, 1987a. Osmotic regulation of gene expression: ionic strength as an intracellular signal? Trends Biochem. Sci. 12: 339–344.Google Scholar
  58. Higgins, C.F., L., Sutherland, J., Cairney & I.R., Booth, 1987b. The osmotically regulated proU locus of Salmonella typhimurium encodes a periplasmic betaine-binding protein. J. Gen. Microbiol. 133: 305–310.Google Scholar
  59. Higgins, C.F., C.J., Dorman, D.A., Stirling, L., Waddell, I.R., Booth, G., May & E., Bremer, 1988. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52: 569–584.Google Scholar
  60. Higgins, C.F., J.C.D., Hinton, C.S.J., Hulton, T., Owen-hughes, G.D., Pavitt & A., Seirafi, 1990. Protein H1: a role for chromatin structure in the regulation of bacterial gene expression and virulence? Mol. Microbiol. 4: 2007–2012.Google Scholar
  61. Hinton, J.C.D., D.S., Santos, A., Seirafi, C.S.J., Hulton, G.D., Pavitt & C.F., Higgins, 1992. Expression and mutational analysis of the nucleoid-associated protein H-NS of Salmonella typhimurium. Mol. Microbiol. 6: 2327–2337.Google Scholar
  62. Hromockyi, A.E., S.C., Tucker & A.T., Maurelli, 1992. Temperature regulation of Shigella virulence: identification of the repressor gene virR, an analogue of hns, and partial complementation by tyrosyl transfer RNA (tRNAf1Tyr). Mol. Microbiol. 6: 2113–2124.Google Scholar
  63. Huisman, O., M., Faelen, D., Girard, A., Jaffé, A., Toussaint & J., Rouvière-Yaniv, 1989. Multiple defects in Escherichia coli mutants lacking HU protein. J. Bacteriol. 171: 3704–3712.Google Scholar
  64. Hulton, C.S.J., A., Seirafi, J.C.D., Hinton, J.M., Sidebotham, L., Waddell, G.D., Pavitt, T., Owen-Hughes, A., Spassky, H., Buc & C.F., Higgins, 1990. Histone-like protein H1 (H-NS), DNA super-coiling, and gene expression in bacteria. Cell 63: 631–642.Google Scholar
  65. Hwang, D.S. & A., Kornberg, 1992. Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHP. J. Biol. Chem. 267: 23083–23086.Google Scholar
  66. Jaworski, A., N.P., Higgins, R.D., Wells & W., Zacharias, 1991. Topoisomerase mutants and physiological conditions control supercoiling and Z-DNA formation in vivo. J. Biol. Chem. 266: 2576–2581.Google Scholar
  67. Jebbar, M., R., Talibart, K., Gloux, T., Bernard & C., Blanco, 1992. Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J. Bacteriol. 174: 5027–5035.Google Scholar
  68. Jenkins, D.E., S.A., Chaisson & A., Matin, 1990. Starvation-induced cross protection against osmotic challenge in Escherichia coli. J. Bacteriol. 172: 2779–2781.Google Scholar
  69. Jones, P.G., R., Krah, S.R., Tafuri & A.P., Wolffe, 1992. DNA gyrase, CS7,4, and the cold shock response in Escherichia coli. J. Bacteriol. 174: 5798–5802.Google Scholar
  70. Jordan, A., I., Gibert & J., Barbé, 1994. Cloning and sequencing of the genes from Salmonella typhimurium encoding a new bacterial ribonucleotide reductase. J. Bacteriol. 176: 3420–3427.Google Scholar
  71. Jovanovich, S.B. & J., Lebowitz, 1987. Estimation of the effect of coumermycin A1 on Salmonella typhimurium promoters by using random operon fusions. J. Bacteriol. 169: 4431–4435.Google Scholar
  72. Jovanovich, S.B., M.T., RecordJr. & R.R., Burgess, 1989. In an Escherichia coli coupled transcription-translation system, expression of the osmoregulated gene proU is stimulated at elevated potassium concentrations and by an extract from cells grown at high osmolarity. J. Biol. Chem. 264: 7821–7825.Google Scholar
  73. Kaasen, I., P., Falkenberg, O.B., Styrovold & A.R., Strom, 1992. Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by KatF (AppR). J. Bacteriol. 174: 889–898.Google Scholar
  74. Kawula, T.H. & P.E., Orndorff, 1991. Rapid site-specifle DNA inversion in Escherichia coli mutants lacking the histonelike protein H-NS. J. Bacteriol. 173: 4116–4123.Google Scholar
  75. Koo, S.-P. & I.R., Booth, 1994. Quantitative analysis of growth stimulation by glycine betaine in Salmonella typhimurium. Microbiology 140: 617–621.Google Scholar
  76. Lamark, T., O.B., Styrvold & A.R., Strom, 1992. Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli. FEMS Microbiol. Lett. 96: 149–154.Google Scholar
  77. Lange, R. & R., Hengge-Aronis, 1994. The cellular concentration of the 376–1 subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Devel. 8: 1600–1612.Google Scholar
  78. le, Rudulier, D. & L., Bouillard, 1983. Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae. Appl. Environ. Microbiol. 46: 152–159.Google Scholar
  79. Liu, Q. & C.C., Richardson, 1993. Gene 5,5 protein of bacteriophage T7 inhibits the nucleoid protein H-NS of Escherichia coli. Proc. Natl. Acad. Sci. USA 90: 1761–1765.Google Scholar
  80. Lucht, J.M. & Bremer, 1991. Characterization of mutations affecting the osmoregulated proU promoter of Escherichia coli and identification of 5′ sequences required for high-level expression. J. Bacteriol. 173: 801–809.Google Scholar
  81. Lucht, J.M. & E., Bremer, 1994. Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-affinlty glycine betaine transport system ProU. FEMS Microbiol. Rev. 14: 3–20.Google Scholar
  82. Lucht, J.M., R., Dersch, B., Kempf & E., Bremer, 1994. Interaction of the nucleoid-associated DNA-binding protein H-NS with the regulatory region of the osmotically controlled proU operon of Escherichia coli. J. Biol. Chem. 269: 6578–6586.Google Scholar
  83. Mahajna, J., A.B., Oppenheim, A., Rattray & M., Gottesman, 1986. Translation initiation of bacteriophage lambda gene cII integration host factor. J. Bacteriol. 165: 167–174.Google Scholar
  84. Mahan, M.J., J.M., Slauch & J.J., Mekalanos, 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686–688.Google Scholar
  85. Makris, J.C., P.L., Nordmann & W.S., Reznikoff, 1990. Integration host factor plays a role in IS50 and Tn5 transposition. J. Bacteriol. 172: 1368–1373.Google Scholar
  86. Manna, D. & J., Gowrishankar, 1994. Evidence for involvement of proteins HU and RpoS in transcription of the osmoresponsive proU operon in Escherichia coli. J. Bacteriol. 176: 5378–5384.Google Scholar
  87. May, G., E., Faatz, M., Villarejo & E., Bremer, 1986. Binding protein dependent transport of glycine betaine and its osmotic regulation in Escherichia coli K12. Mol. Gen. Genet. 205: 225–233.Google Scholar
  88. May, G., E., Faatz, J.M., Lucht, M., Haardt, M., Bolliger & E., Bremer, 1989. Characterization of the osmoregulated Escherichia coli proU promoter and identification of ProV as a membraneassociated protein. Mol. Microbiol. 3: 1521–1531.Google Scholar
  89. May, G., P., Dersch, M., Haardt, A., Middendorf & E., Bremer, 1990. The osmZ (bglY) gene encodes the DNA-binding protein H-NS (H1a), a component of the Escherchia coli K12 nucleoid. Mol. Gen. Genet. 224: 81–90.Google Scholar
  90. McClellan, J.A., P., Boublikova, E., Palecek & D.M., Lilley, 1990. Superhelical torsion in cellular DNA responds directly to environmental and genetic factors. Proc. Natl. Acad. Sci. USA 87: 8373–8377.Google Scholar
  91. McLaggan, D. & W., Epstein, 1991. Escherichia coli accumulates the eukaryotic osmolyte taurine at high osmolarity. FEMS Microbiol. Lett. 81: 209–214.Google Scholar
  92. Mellies, J., R., Brems & M., Villarejo, 1994. The Escherichia coli proU promoter element and its contribution to osmotically signalled transcription activation. J. Bacteriol. 176: 3638–3645.Google Scholar
  93. Mellies, J., A., Wise & M., Villarejo, 1995. Two different Escherichia coli proP promoters respond to osmotic and growth phase signals. J. Bacteriol. 177: 144–151.Google Scholar
  94. Mendelson, I., M., Gottesman & A.B., Oppenheim, 1991. HU and integration host factor function as auxiliary proteins in cleavage of phage lambda cohesive ends by terminase. J. Bacteriol. 173: 1670–1676.Google Scholar
  95. Miller, W.G. & R.W., Simons, 1993. Chromosomal suparcoiling in Escherichia coli. Mol. Microbiol. 10: 675–684.Google Scholar
  96. Milner, J.L., D.J., McClellan & J.M., Wood, 1987. Factors reducing and promoting the effectiveness of proline as an osmoprotectant in Escherichia coli K-12. J. Gen. Microbiol. 133: 1851–1860.Google Scholar
  97. Nguyen, L.H., D.B., Jensen, N.E., Thompson, D.r., Gentry & R.R., Burgess, 1993. In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product. Biochemistry 32: 11112–11117.Google Scholar
  98. Ni, Bhriain, N., C.J., Dorman & C.F., Higgins, 1989. An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol. Microbiol. 3: 933–942.Google Scholar
  99. Olsen, A., A., Arnqvist, M., Hammer, S., Sukupolvi & S., Normark, 1993. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol. Microbiol. 7: 523–536.Google Scholar
  100. Overdier, D.G. & L.N., Csonka, 1992. A transcriptional silencer downstream of the promoter in the osmotically controlled proU operon of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 89: 3140–3144.Google Scholar
  101. Overdier, D.G., E.R., Olson, B.D., Erickson, M.M., Ederer & L.N., Csonka, 1989. Nucleotide sequence of the transeriptional control region of the osmotically regulated proU operon of Salmonella typhimurium and identification of the 5′-end point of the proU mRNA. J. Bacteriol. 171: 4694–4706.Google Scholar
  102. Owen-Hughes, T.A., G.D., Pavitt, D.S., Santos, J.M., Sidebotham, C.S.J., Hulton, J.C.D., Hinton & C.F., Higgins, 1992. The chromatin-associated protein H-NS interacts with curved DNA to influence topology and gene expression. Cell 71: 255–265.Google Scholar
  103. Park, S.F., D.A., Stirling, C.S.J., Hulton, I.R., Booth, C.F., Higgins & G.S.A.B., Stewart, 1989. A novel, non-invasive promoter probe vector: cloning of the osmoregulated proU promoter of Escherichia coli K12. Mol. Microbiol. 3: 1011–1023.Google Scholar
  104. Pavitt, G.D. & C.F., Higins, 1993. Chromosomal domains of supercoiling in Salmonella typhimurium. Mol. Microbiol. 10: 685–696.Google Scholar
  105. Perroud, B. & D.Le, Rudulier, 1985. Glycine betaine transport in Escherichia coli: osmotic modulation. J. Bacteriol. 161: 393–401.Google Scholar
  106. Porter, M.E. & C.J., Dorman, 1994. A role for H-NS in the thermoosmotic regulation of virulence gene expression in Shigella flexneri. J. Bacteriol. 176: 4187–4191.Google Scholar
  107. Prince, W.S. & M.R., Villarejo, 1990. Osmotic control of proU transcription is mediated through direct action of potassium glutamate on the transcription complex. J. Biol. Chem. 265: 17673–17679.Google Scholar
  108. Ramirez, R.M., W.S., Prince, E., Bremer & M., Villarejo, 1989. In vitro reconstitution of osmoregulated expression of proU of Escherichia coli. Proc. Natl. Acad. Sci. USA, 86: 1153–1157.Google Scholar
  109. Ramirez, R.M. & M.R., Villarejo, 1991. Osmotic signal transduction to proU is independent of DNA supercoiling in Escherichia coli. J. Bacteriol. 173: 879–885.Google Scholar
  110. Shi, X. & G.N., Bennett, 1994. Plasmids bearing hfq and the hns-like gene stpA complement hns mutants in modulating arginine decarboxylase gene expression in Escherichia coli. J. Bacteriol. 176: 6769–6775.Google Scholar
  111. Shi, X., B.C., Waasdorp & G.N., Bennett, 1993. Modulation of acid-induced amino acid decarboxylase gene expression by hns in Escherichia coli. J. Bacteriol. 175: 1182–1186.Google Scholar
  112. Sinden, R.R. & D.E., Pettijohn, 1981. Chromosomes in living E. coli cells are segregated into domains of supercoiling. Proc. Natl. Acad. Sci. USA 78: 224–228.Google Scholar
  113. Sledjeski, D. & S., Gottesman, 1995. A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92: 2003–2007.Google Scholar
  114. Spassky, A., S., Rimsky, H., Garreau & H., Buc, 1984. H1a, an E. coli DNA-binding protein which accumulates in stationary phase, strongly compacts DNA in vitro. Nucleic Acids Res. 12: 5321–5340.Google Scholar
  115. Stenzel, T.T., P., Patel & D., Bastia, 1987. The integration host factor of Escherichia coli binds to bent DNA at the origin of replication of the plasmid pSC101. Cell 49: 709–717.Google Scholar
  116. Stirling, D.A., C.S.J., Hulton, L., Waddell, S.F., Park, G.S.A.B., Stewart, I.R., Booth & C.F., Higgins, 1989. Molecular characterization of the proU loci of Salmonella typhimurium and Escherichia coli encoding osmoregulated glycine betaine transport systems. Mol. Microbiol. 3: 1025–1038.Google Scholar
  117. Sutherland, L., J., Cairney, M.J., Elmore, I.R., Booth & C.F., Higgins, 1986. Osmotic regulation of transcription: induction of the proU betaine transport locus is determined by the accumulation of intracellular potassium. J. Bacteriol. 168: 805–814.Google Scholar
  118. Tanaka, K., S., Muramatsu, H., Yamada & T., Mizuno, 1991. Systematic characterization of curved DNA segments randomly cloned from Escherichia coli and their functional significance. Mol. Gen. Genet. 226: 367–376.Google Scholar
  119. Tanaka, K., Y., Takayanagi, N., Fujita, A., Ishihama & H., Takahashi, 1993. Heterogeneity of principal σ factor in Escherichia coli: the rpoS gene product, 377–1, is a second principal σ factor of RNA polymerase in stationary-phase Escherichia coli. Proc. Natl. Acad. Sci. USA 90: 3511–3515.Google Scholar
  120. Tanaka, K., C., Ueguchi & T., Mizuno, 1994. Importance of stereospecific positioning of the upstream cis-acting DNA element containing a curved DNA structure for the functioning of the Escherichia coli proV promoter. Biosci. Biotech. Biochem. 58: 1097–1101.Google Scholar
  121. Tobe, T., M., Yoshikawa, T., Mizuno & C., Sasakawa, 1993. Transcriptional control of the invasion regulatory gene virB of Shigella flexneri: Activation by VirF and repression by H-NS. J. Bacteriol. 175: 6142–5149.Google Scholar
  122. Tsui, P. & M., Freundlich, 1990. Integration host factor bends the DNA in the Escherichia coli ilvBN promoter region. Mol. Gen. Genet. 223: 349–352.Google Scholar
  123. Tupper, A.E., T.A., Owen-Hughes, D.W., Ussery, D.S., Santos, D.J.P., Ferguson, J.M., Sidebotham, J.C.D., Hinton & C.F., Higgins, 1994. The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J. 13: 258–268.Google Scholar
  124. Ueguchi, C. & T., Mizuno, 1993. The Escherichia coli nucleoid protein H-NS functions directly as a transcriptional repressor. EMBO J. 12: 1039–1046.Google Scholar
  125. Wang, J.Y. & M., Syvanen, 1992. DNA twist as a transcriptional sensor for environmental changes. Mol. Microbiol. 6: 1861–1866.Google Scholar
  126. Wood, D.C. & J., Lebowitz, 1984. Efect of supercoiling on the abortive initiation kinetics of the RNA-1 promoter of ColE1 plasmid DNA. J. Biol. Chem. 259: 11184–11187.Google Scholar
  127. Wood, J.M., 1988. Proline porters affect the utilization of proline as a nutrient or osmoprotectant for bacteria. J. Memb. Biol. 106: 183–202.Google Scholar
  128. Yamada, H., S., Muramatsu & T., Mizuno, 1990. An Escherichia coli protein that preferentially binds to sharply curved DNA. J. Biochem. 108: 420–425.Google Scholar
  129. Yamashino, T., C., Ueguchi & T., Mizuno, 1995. Quantitative control of the stationary phase-specific sigma factor, 377–2, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J. 14: 594–602.Google Scholar
  130. Yancey, P.H., M.E., Clark, S.C., Hand, R.D., Bowlus & G.N., Somero, 1982. Living with water stress: evolution of osmolyte systems. Science 217: 1214–1222.Google Scholar
  131. Yasuzawa, K., N., Hayashi, N., Goshima, K., Kohno, F., Imamoto & Y., Kano, 1992. Histone-like proteins are required for cell growth and constraint of supercoils in DNA. Gene 122: 9–15.Google Scholar
  132. Yim, H.H., R.L., Brems & M., Villarejo, 1994. Molecular characterization of the promoter of osmY, an rpoS dependent gene. J. Bacteriol. 176: 100–107.Google Scholar
  133. Yoshida, T., T., Yamashino, C., Ueguchi & T., Mizuno, 1993. Expression of the Escherichia coli dimorphic glutamic acid decarboxylases is regulated by the nucleoid protein H-NS. Biosci. Biotech. Biochem. 57: 1568–1569.Google Scholar
  134. Zhang, A. & M., Belfort, 1992. Nucleotide sequence of a newlyidentified Escherichia coli gene, stpA, encoding an H-NS-like protein. Nucleic Acids Res. 20: 6735.Google Scholar
  135. Zuber, F., D., Kotlarz, S., Rimsky & H., Buc, 1994. Modulated expression of promoters containing upstream curved DNA sequences by the Escherichia coli nucleoid protein H-NS. Mol. Microbiol. 12: 231–240.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • J. Gowrishankar
    • 1
  • Dipankar Manna
    • 1
  1. 1.Centre for Cellular and Molecular BiologyHyderabadIndia

Personalised recommendations