Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins

Current Opinion in Microbiology

Volumn 14, Issue 2, 2011, Pages 136-141

  Rimsky, Sylvie ^a   Travers, Andrew ^a,b  

^a Ecole Normale Superieure de Cachan   (France)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; FACTOR FOR INVERSION STIMULATION; HISTONE; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; INTEGRATION HOST FACTOR; MESSENGER RNA; NUCLEOID ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL CHROMOSOME; DNA PROTEIN COMPLEX; DNA SUPERCOILING; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TRANSCRIPTION INITIATION; TRANSLATION INITIATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79954579293     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2011.01.003     Document Type: Review

References (51)

1. Ali Azam T., Iwata A., Nishimura A., Ueda S., Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 1999, 181:6361-6370.
2. Browning D.F., Grainger D.C., Busby S.J. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 2010, 13:773-780.
3. Dillon S.C., Dorman C.J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 2010, 8:185-195.
4. Travers A., Muskhelishvili G. DNA supercoiling-a global transcriptional regulator for enterobacterial growth?. Nat Rev Microbiol 2005, 3:157-169.
5. Finkel S.E., Johnson R.C. The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol 1992, 6:3257-3265.
6. Valens M., Penaud S., Rossignol M., Cornet F., Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J 2004, 23:4330-4341.
7. Mathelier A., Carbone A. Chromosomal periodicity and positional networks of genes in Escherichia coli. Mol Syst Biol 2010, 6:366.
8. Berger M., Farcas A., Geertz M., Zhelyazkova P., Brix K., Travers A., Muskhelishvili G. Coordination of genomic structure and transcription by the main bacterial nucleoid-associated protein HU. EMBO Rep 2010, 11:59-64.
9. Montero Llopis P., Jackson A.F., Sliusarenko O., Surovtsev I., Heinritz J., Emonet T., Jacobs-Wagner C. Spatial organization of the flow of genetic information in bacteria. Nature 2010, 466:77-81.
10. Janga S.C., Salgado H., Martinez-Antonio A. Transcriptional regulation shapes the organization of genes on bacterial chromosomes. Nucleic Acids Res 2009, 37:3680-3688.
11. Nasser W., Schneider R., Travers A., Muskhelishvili G. CRP modulates fis transcription by alternate formation of activating and repressing nucleoprotein complexes. J Biol Chem 2001, 276:17878-17886.
12. Bordes P., Conter A., Morales V., Bouvier J., Kolb A., Gutierrez C. DNA supercoiling contributes to disconnect sigmaS accumulation from sigmaS-dependent transcription in Escherichia coli. Mol Microbiol 2003, 48:561-571.
13. Crozat E., Winkworth C., Gaffe J., Hallin P.F., Riley M.A., Lenski R.E., Schneider D. Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Mol Biol Evol 2010, 27:2113-2128.
14. Jeong K.S., Xie Y., Hiasa H., Khodursky A.B. Analysis of pleiotropic transcriptional profiles: a case study of DNA gyrase inhibition. PLoS Genet 2006, 2:e152.
15. Malik M., Bensaid A., Rouviere-Yaniv J., Drlica K. Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. J Mol Biol 1996, 256:66-76.
16. Rochman M., Blot N., Dyachenko M., Glaser G., Travers A., Muskhelishvili G. Buffering of stable RNA promoter activity against DNA relaxation requires a far upstream sequence. Mol Microbiol 2004, 53:143-152.
17. Corcoran C.P., Dorman C.J. DNA relaxation-dependent phase biasing of the fim genetic switch in Escherichia coli depends on the interplay of H-NS, IHF and LRP. Mol Microbiol 2009, 74:1071-1082.
18. Hardy C.D., Cozzarelli N.R. A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 2005, 57:1636-1652.
19. Cho B.K., Knight E.M., Barrett C.L., Palsson B.O. Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 2008, 18:900-910.
20. Noom M.C., Navarre W.W., Oshima T., Wuite G.J., Dame R.T. H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 2007, 17:R913-914.
21. Junier I., Martin O., Kepes F. Spatial and topological organization of DNA chains induced by gene co-localization. PLoS Comput Biol 2010, 6:e1000678.
22. Muskhelishvili G, Travers A.: DNA structure and bacterial nucleoid-associated proteins. In Bacterial Gene Regulation and Transcriptional Networks. Edited by Babu MM: Horizon Scientific Press; in press.
23. Lucchini S., McDermott P., Thompson A., Hinton J.C. The H-NS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium. Mol Microbiol 2009, 74:1169-1186.
24. Tani T.H., Khodursky A., Blumenthal R.M., Brown P.O., Matthews R.G. Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis. Proc Natl Acad Sci U S A 2002, 99:13471-13476.
25. Zare H., Sangurdekar D., Srivastava P., Kaveh M., Khodursky A. Reconstruction of Escherichia coli transcriptional regulatory networks via regulon-based associations. BMC Syst Biol 2009, 3:39.
26. Xiao G., Reilly C., Khodursky A.B. Improved detection of differentially expressed genes through incorporation of gene locations. Biometrics 2009, 65:805-814.
27. Frenkiel-Krispin D., Ben-Avraham I., Englander J., Shimoni E., Wolf S.G., Minsky A. Nucleoid restructuring in stationary-state bacteria. Mol Microbiol 2004, 51:395-405.
28. Dame R.T., Noom M.C., Wuite G.J. Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 2006, 444:387-390.
29. Schneider R., Lurz R., Luder G., Tolksdorf C., Travers A., Muskhelishvili G. An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res 2001, 29:5107-5114.
30. Bouffartigues E., Buckle M., Badaut C., Travers A., Rimsky S. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol 2007, 14:441-448.
31. Maurer S., Fritz J., Muskhelishvili G., Travers A. RNA polymerase and an activator form discrete subcomplexes in a transcription initiation complex. EMBO J 2006, 25:3784-3790.
32. Arold S.T., Leonard P.G., Parkinson G.N., Ladbury J.E. H-NS forms a superhelical protein scaffold for DNA condensation. Proc Natl Acad Sci U S A 2010, 107:15728-15732.
33. Bloch V., Yang Y., Margeat E., Chavanieu A., Auge M.T., Robert B., Arold S., Rimsky S., Kochoyan M. The H-NS dimerization domain defines a new fold contributing to DNA recognition. Nat Struct Biol 2003, 10:212-218.
34. Luijsterburg M.S., Noom M.C., Wuite G.J., Dame R.T. The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J Struct Biol 2006, 156:262-272.
35. Stella S., Spurio R., Falconi M., Pon C.L., Gualerzi C.O. Nature and mechanism of the in vivo oligomerization of nucleoid protein H-NS. EMBO J 2005, 24:2896-2905.
36. Cosgriff S., Chintakayala K., Chim Y.T., Chen X., Allen S., Lovering A.L., Grainger D.C. Dimerization and DNA-dependent aggregation of the Escherichia coli nucleoid protein and chaperone CbpA. Mol Microbiol 2010, 77:1289-1300.
37. Stella S., Cascio D., Johnson R.C. The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev 2010, 24:814-826.
38. Weisberg R.A., Freundlich M., Friedman D., Gardner J., Goosen N., Nash H., Oppenheim A., Rouviere-Yaniv J. Nomenclature of the genes encoding IHF. Mol Microbiol 1996, 19:642.
39. Rice P.A., Yang S., Mizuuchi K., Nash H.A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 1996, 87:1295-1306.
40. Koh J., Saecker R.M., Record M.T. DNA binding mode transitions of Escherichia coli HUαβ: evidence for formation of a bent DNA-protein complex on intact, linear duplex DNA. J Mol Biol 2008, 383:324-346.
41. van Noort J., Verbrugge S., Goosen N., Dekker C., Dame R.T. Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci U S A 2004, 101:6969-6974.
42. Claret L., Rouviere-Yaniv J. Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long-term survival. J Mol Biol 1997, 273:93-104.
43. Oberto J., Nabti S., Jooste V., Mignot H., Rouviere-Yaniv J. The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS One 2009, 4:e4367.
44. Grove A. Functional evolution of bacterial histone-like HU proteins. Curr Issues Mol Biol 2010, 13:1-12.
45. Dorman C.J. Horizontally acquired homologues of the nucleoid-associated protein H-NS: implications for gene regulation. Mol Microbiol 2010, 75:264-267.
46. Muller C.M., Schneider G., Dobrindt U., Emody L., Hacker J., Uhlin B.E. Differential effects and interactions of endogenous and horizontally acquired H-NS-like proteins in pathogenic Escherichia coli. Mol Microbiol 2010, 75:280-293.
47. Johansson J., Uhlin B.E. Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary-phase survival of Escherichia coli. Proc Natl Acad Sci U S A 1999, 96:10776-10781.
48. Zhang A., Rimsky S., Reaban M.E., Buc H., Belfort M. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J 1996, 15:1340-1349.
49. Dillon S.C., Cameron A.D., Hokamp K., Lucchini S., Hinton J.C., Dorman C.J. Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 2010, 76:1250-1265.
50. Banos R.C., Vivero A., Aznar S., Garcia J., Pons M., Madrid C., Juarez A. Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 2009, 5:e1000513.
51. Maurer S., Fritz J., Muskhelishvili G. A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid-associated proteins revealing novel types of DNA organization. J Mol Biol 2009, 387:1261-1276.