DNA looping-mediated repression by histone-like protein H-NS: Specific requirement of Eσ70 as a cofactor for looping

Genes and Development

Volumn 19, Issue 19, 2005, Pages 2388-2398

  Shin, Minsang ^a   Song, Miryoung ^a   Joon, Haeng Rhee ^a   Hong, Yeongjin ^a   Kim, You Jin ^b   Seok, Yeong Jae ^b   Ha, Kwon Soo ^c   Jung, Se Hui ^c   Choy, Hyon E ^a  

^a Chonnam National University Medical School   (South Korea)

^b Seoul National University   (South Korea)

^c Kangwon National University   (South Korea)

Author keywords

DNA looping; DNA protein interaction; E. coli; H NS; RNA polymerase; Transcription repression

Indexed keywords

DNA BINDING PROTEIN; HISTONE; ISOPROTEIN; PERMANGANATE POTASSIUM; PROTEIN SUBUNIT; RNA POLYMERASE;

AMINO ACID SEQUENCE; ARTICLE; ASSAY; ATOMIC FORCE MICROSCOPY; COMPLEX FORMATION; DNA FLANKING REGION; ESCHERICHIA COLI; GENETIC ANALYSIS; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PURIFICATION; PURIFICATION; TRANSCRIPTION INITIATION;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; DOWN-REGULATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MICROSCOPY, ATOMIC FORCE; PROMOTER REGIONS (GENETICS); SIGMA FACTOR; TRANSCRIPTION INITIATION SITE;

ESCHERICHIA COLI;

EID: 25844463677     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1316305     Document Type: Article

References (67)

1. Aki, T., Choy, H.E., and Adhya, S. 1996. Histone-like protein HU as a specific transcriptional regulator: Co-factor role in repression of gal transcription by GAL repressor. Genes Cells 1: 179-188.
2. Arnqvist, A., Olsen, A., and Normark, S. 1994. σ S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by σ 70 in the absence of the nucleoid-associated protein H-NS. Mol. Microbiol. 13: 1021-1032.
3. Atlung, T. and Ingmer, H. 1997. H-NS: A modulator of environmentally regulated gene expression. Mol. Microbiol. 24: 7-17.
4. Badaut, C., Williams, R., Arluison, V., Bouffartigues, E., Robert, B., Buc, H., and Rimsky, S. 2002. The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J. Biol. Chem. 277: 41657-41666.
5. Bordes, P., Repoila, F., Kolb, A., and Gutierrez, C. 2000. Involvement of differential efficiency of transcription by eσs and eσ70 RNA polymerase holoenzymes in growth phase regulation of the Escherichia coli osmE promoter. Mol. Microbiol. 35: 845-853.
6. Ceschini, S., Lupidi, G.., Coletta, M., Pon, C.L., Fioretti, E., and Angeletti, M. 2000. Multimeric self-assembly equilibria involving the histone-like protein H-NS. A thermodynamic study. J. Biol. Chem. 275: 729-734.
7. Choy, H.E. and Adhya, S. 1993. RNA polymerase idling and clearance in gal promoters: Use of supercoiled minicircle DNA template made in vivo. Proc. Natl. Acad. Sci. 90: 472-476.
8. _. 1996. Negative control. In Escherichia coli and Salmonella: Cellular and molecular biology (eds. F.C. Neidhardt et al.), Vol. 1, pp. 1287-1299. ASM Press, Washington, D.C.
9. Choy, H.E., Park, S.W., Aki, T., Parrack, P., Fujita, N., Ishihama, A., and Adhya, S. 1995. Repression and activation of transcription by Gal and Lac repressors: Involvement of α subunit of RNA polymerase. EMBO J. 14: 4523-4529.
10. Colland, F., Barth, M., Hengge-Aronis, R., and Kolb, A. 2000. σ Factor selectivity of Escherichia coli RNA polymerase: Role for CRP, IHF and lrp transcription factors. EMBO J. 19: 3028-3037.
11. Craig, M.L., Suh, W.C., and Record Jr., M.T. 1995. HO. and DNase I probing of E σ 70 RNA polymerase-λ PR promoter open complexes: Mg2+ binding and its structural consequences at the transcription start site. Biochemistry 34: 15624-15632.
12. Dame, R.T. 2005. The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 56: 858-870.
13. Dame, R.T., Wyman, C., and Goosen, N. 2001. Structural basis for preferential binding of H-NS to curved DNA. Biochimie 83: 231-234.
14. Dame, R.T., Wyman, C., Wurm, R., Wagner, R., and Goosen, N. 2002. Structural basis for H-NS-mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1. J. Biol. Chem. 277: 2146-2150.
15. Darst, S.A., Kubalek, E.W., and Kornberg, R.D. 1989. Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electron crystallography. Nature 340: 730-732.
16. Deighan, P., Beloin, C., and Dorman, C.J. 2003. Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol. Microbiol. 48: 1401-1416.
17. Dersch, P., Schmidt, K., and Bremer, E. 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.
18. Dorman, C.J. 2004. H-NS: A universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2: 391-400.
19. Dorman, C.J., Hinton, J.C., and Free, A. 1999. Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol. 7: 124-128.
20. Drlica, K. and Rouviere-Yaniv, J. 1987. Histonelike proteins of bacteria. Microbiol. Rev. 51: 301-319.
21. Espinosa-Urgel, M., Chamizo, C., and Tormo, A. 1996. A consensus structure for σ S-dependent promoters. Mol. Microbiol. 21: 657-659.
22. Falconi, M., Gualtieri, M.T., La Teana, A., Losso, M.A., and Pon, C.L. 1988. Proteins from the prokaryotic nucleoid: Primary and quaternary structure of the 15-kD Escherichia coli DNA binding protein H-NS. Mol. Microbiol. 2: 323-329.
23. Fried, M.G. 1989. Measurement of protein-DNA interaction parameters by electrophoresis mobility shift assay. Electrophoresis 10: 366-376.
24. Friedrich, K., Gualerzi, C.O., Lammi, M., Losso, M.A., and Pon, C.L. 1988. Proteins from the prokaryotic nucleoid. Interaction of nucleic acids with the 15 kDa Escherichia coli histone-like protein H-NS. FEBS Lett. 229: 197-202.
25. Gralla, J.D. 2005. Escherichia coli ribosomal RNA transcription: Regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase-binding protein. Mol. Microbiol. 55: 973-977.
26. Hayatsu, H., Takeishi, K.I., and Ukita, T. 1966. The modification of nucleosides and nucleotides. 3. A selective modification of cytidine with semicarbazide. Biochim. Biophys. Acta 123: 445-457.
27. Hengge-Aronis, R. 1996. Back to log phase: σ S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol. Microbiol. 21: 887-893.
28. Hommais, F., Krin, E., Laurent-Winter, C., Soutourina, O., Malpertuy, A., Le Caer, J.P., Danchin, A., and Bertin, P. 2001. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol. 40: 20-36.
29. Ishihama, A. 2000. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 54: 499-518.
30. Kim, E.Y., Shin, M.S., Rhee, J.H., and Choy, H.E. 2004. Factors influencing preferential utilization of RNA polymerase containing σ-38 in stationary-phase gene expression in Escherichia coli. J. Microbiol. 42: 103-110.
31. Kusano, S., Ding, Q., Fujita, N., and Ishihama, A. 1996. Promoter selectivity of Escherichia coli RNA polymerase E σ 70 and E σ 38 holoenzymes. Effect of DNA supercoiling. J. Biol. Chem. 271: 1998-2004.
32. 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.
33. Le Bret, M. 1979. Catastrophic variation of twist and writhing of circular DNAs with constraint? Biopolymers 18: 1709-1725.
34. Lee, S.J. and Gralla, J.D. 2001. σ38 (rpoS) RNA polymerase promoter engagement via -10 region nucleotides. J. Biol. Chem. 276: 30064-30071.
35. Lee, S.E., Shin, S.H., Kim, S.Y., Kim, Y.R., Shin, D.H., Chung, S.S., Lee, Z.H., Lee, J.Y., Jeong, K.C., Choi, S.H., et al. 2000. Vibrio vulnificus has the transmembrane transcription activator ToxRS stimulating the expression of the hemolysin gene vvhA. J. Bacteriol. 182: 3405-3415.
36. Lucht, J.M., Dersch, P., Kempf, B., and Bremer, E. 1994. Interactions 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.
37. Marschall, C., Labrousse, V., Kreimer, M., Weichart, D., Kolb, A., and Hengge-Aronis, R. 1998. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on σ s and requires activation by cAMP-CRP. J. Mol. Biol. 276: 339-353.
38. Miller, J.H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
39. Mulvey, M.R. and Loewen, P.C. 1989. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel σ transcription factor. Nucleic Acids Res. 17: 9979-9991.
40. Oehler, S., Eismann, E.R., Kramer, H., and Muller-Hill, B. 1990. The three operators of the lac operon cooperate in repression. EMBO J. 9: 973-979.
41. Putnam, S.L. and Koch, A.L. 1975. Complications in the simplest cellular enzyme assay: Lysis of Escherichia coli for the assay of β-galactosidase. Anal. Biochem. 63: 350-360.
42. Riggs, A.D., Bourgeois, S., and Cohn, M. 1970. The lac repressor-operator interaction. 3. Kinetic studies. J. Mol. Biol. 53: 401-417.
43. Rimsky, S. 2004. Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr. Opin. Microbiol. 7: 109-114.
44. Rimsky, S., Zuber, F., Buckle, M., and Buc, H. 2001. A molecular mechanism for the repression of transcription by the H-NS protein. Mol. Microbiol. 42: 1311-1323.
45. Rivetti, C., Guthold, M., and Bustamante, C. 1999. Wrapping of DNA around the E. coli RNA polymerase open promoter complex. EMBO J. 18: 4464-4475.
46. Robbe-Saule, V., Schaeffer, F., Kowarz, L., and Norel, F. 1997. Relationships between H-NS, σ S, SpvR and growth phase in the control of spvR, the regulatory gene of the Salmonella plasmid virulence operon. Mol. Gen. Genet. 256: 333-347.
47. Rostoks, N., Park, S., and Choy, H.E. 2000. Reiterative transcription initiation from galP2 promoter of Escherichia coli. Biochim. Biophys. Acta 1491: 185-195.
48. Roy, S., Garges, S., and Adhya, S. 1998. Activation and repression of transcription by differential contact: Two sides of a coin. J. Biol. Chem. 273: 14059-14062.
49. Sasse-Dwight, S. and Gralla, J.D. 1989. KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo. J. Biol. Chem. 264: 8074-8081.
50. Schickor, P., Metzger, W., Werel, W., Lederer, H., and Heumann, H. 1990. Topography of intermediates in transcription initiation of E. coli. EMBO J. 9: 2215-2220.
51. Schroder, O. and Wagner, R. 2000. The bacterial DNA-binding protein H-NS represses ribosomal RNA transcription by trapping RNA polymerase in the initiation complex. J. Mol. Biol. 298: 737-748.
52. _. 2002. The bacterial regulatory protein H-NS - A versatile modulator of nucleic acid structures. Biol. Chem. 383: 945-960.
53. Shin, M., Kang, S., Hyun, S.J., Fujita, N., Ishihama, A., Valentin-Hansen, P., and Choy, H.E. 2001. Repression of deoP2 in Escherichia coli by CytR: Conversion of a transcription activator into a repressor. EMBO J. 20: 5392-5399.
54. Simons, R.W., Houman, F., and Kleckner, N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96.
55. Smyth, C.P., Lundback, T., Renzoni, D., Siligardi, G.., Beavil, R., Layton, M., Sidebotham, J.M., Hinton, J.C., Driscoll, P.C., Higgins, C.F., et al. 2000. Oligomerization of the chromatin-structuring protein H-NS. Mol. Microbiol. 36: 962-972.
56. Sonden, B. and Uhlin, B.E. 1996. Coordinated and differential expression of histone-like proteins in Escherichia coli: Regulation and function of the H-NS analog StpA. EMBO J. 15: 4970-4980.
57. Sonnenfield, J.M., Burns, C.M., Higgins, C.F., and Hinton, J.C. 2001. The nucleoid-associated protein StpA binds curved DNA, has a greater DNA-binding affinity than H-NS and is present in significant levels in hns mutants. Biochimie 83: 243-249.
58. Spurio, R., Falconi, M., Brandi, A., Pon, C.L., and Gualerzi, C.O. 1997. The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J. 16: 1795-1805.
59. Tanaka, K., Kusano, S., Fujita, N., Ishihama, A., and Takahashi, H. 1995. Promoter determinants for Escherichia coli RNA polymerase holoenzyme containing σ 38 (the rpoS gene product). Nucleic Acids Res. 23: 827-834.
60. Ueguchi, C., Suzuki, T., Yoshida, T., Tanaka, K., and Mizuno, T. 1996. Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. J. Mol. Biol. 263: 149-162.
61. Ussery, D.W., Hinton, J.C., Jordi, B.J., Granum, P.E., Seirafi, A., Stephen, R.J., Tupper, A.E., Berridge, G., Sidebotham, J.M., and Higgins, C.F. 1994. The chromatin-associated protein H-NS. Biochimie 76: 968-980.
62. Waterman, S.R. and Small, P.L. 2003. Transcriptional expression of Escherichia coli glutamate-dependent acid resistance genes gadA and gadBC in an hns rpoS mutant. J. Bacteriol. 185: 4644-4647.
63. Wise, A., Brems, R., Ramakrishnan, V., and Villarejo, M. 1996. Sequences in the -35 region of Escherichia coli rpoS-dependent genes promote transcription by E σ S. J. Bacteriol. 178: 2785-2793.
64. Yoshida, T., Ueguchi, C., Yamada, H., and Mizuno, T. 1993. Function of the Escherichia coli nucleoid protein, H-NS: Molecular analysis of a subset of proteins whose expression is enhanced in a hns deletion mutant. Mol. Gen. Genet. 237: 113-122.
65. Yu, R.R. and DiRita, V.J. 2002. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol. 43: 119-134.
66. Zambrano, M.M. and Kolter, R. 1996. GASPing for life in stationary phase. Cell 86: 181-184.
67. Zhang, A., Rimsky, S., Reaban, M.E., Buc, H., and Belfort, M. 1996. Escherichia coli protein analogs StpA and H-NS: Regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 15: 1340-1349.