DNA protection by histone-like protein HU from the hyperthermophilic eubacterium Thermotoga maritima

Nucleic Acids Research

Volumn 36, Issue 12, 2008, Pages 3956-3968

  Mukherjee, Anirban ^a   Sokunbi, Abimbola O ^a,b   Grove, Anne ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DEOXYRIBONUCLEASE I; DNA TOPOISOMERASE; GENOMIC DNA; HISTONE; HU PROTEIN; PLASMID DNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA FLANKING REGION; DNA FOOTPRINTING; DNA SUPERCOILING; ENZYME DEGRADATION; EUBACTERIUM; GEL MOBILITY SHIFT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN FAMILY; THERMOTOGA MARITIMA;

BACTERIAL PROTEINS; DNA; DNA TOPOISOMERASES, TYPE I; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; TEMPERATURE; THERMOTOGA MARITIMA;

BACTERIA (MICROORGANISMS); PROKARYOTA; THERMOTOGA MARITIMA;

EID: 47249161238     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn348     Document Type: Article

References (60)

1. Azam,T.A. and Ishihama,A. (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. J. Biol. Chem., 274, 33105-33113.
2. Kellenberger,E. and Arnold-Schultz-Gahmen,B. (1992) Chromatins of low-protein-content: Special features of their compaction and condensation. FEMS Microbiol. Lett., 100, 361-370.
3. Dame,R.T. (2005) The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 56, 858-870.
4. Achenbach-Richter,L., Gupta,R., Stetter,K.O. and Woese,C.R. (1987) Were the original eubacteria thermophiles? Syst. Appl. Microbiol., 9 34-39.
5. Bocchetta,M., Gribaldo,S., Sanangelantoni,A. and Cammarano,P. (2000) Phylogenetic depth of the bacterial genera Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J. Mol. Evol., 50, 366-380.
6. Rouvière-Yaniv,J., Yaniv,M. and Germond,J.E. (1979) E. coli DNA binding protein HU forms nucleosome like structure with circular double-stranded DNA. Cell, 17, 265-274.
7. Griffith,J.D. (1976) Visualization of prokaryotic DNA in a regularly condensed chromatin-like fiber. Proc. Natl Acad. Sci. USA, 73 563-567.
8. Brunetti,R., Prosseda,G., Beghetto,E., Colonna,B. and Micheli,G. (2001) The looped domain organization of the nucleoid in histone-like protein defective Escherichia coli strains. Biochimie, 83, 873-882.
9. Dame,R.T., Noom,M.C. and Wuite,G.J. (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature, 444, 387-390.
10. McGovern,V., Higgins,N.P., Chiz,R.S. and Jaworski,A. (1994) H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie, 76, 1019-1029.
11. Kar,S., Edgar,R. and Adhya,S. (2005) Nucleoid remodeling by an altered HU protein: Reorganization of the transcription program. Proc. Natl Acad. Sci. USA, 102, 16397-16402.
12. Kar,S., Choi,E.J., Guo,F., Dimitriadis,E.K., Kotova,S.L. and Adhya,S. (2006) Right-handed DNA supercoiling by an octameric form of histone-like protein HU: Modulation of cellular transcription. J. Biol. Chem., 281, 40144-40153.
13. Pontiggia,A., Negri,A., Beltrame,M. and Bianchi,M.E. (1993) Protein HU binds specifically to kinked DNA. Mol. Microbiol., 7, 343-350.
14. Castaing,B., Zelwer,C., Laval,J. and Boiteux,S. (1995) HU protein of Escherichia coli binds specifically to DNA that contains single-strand breaks or gaps. J. Biol. Chem., 270, 10291-10296.
15. Balandina,A., Kamashev,D. and Rouvière-Yaniv,J. (2002) The bacterial histone-like protein HU specifically recognizes similar structures in all nucleic acids. DNA, RNA, and their hybrids. J. Biol. Chem., 277, 27622-27628.
16. Pinson,V., Takahashi,M. and Rouvière-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.
17. Esser,D., Rudolph,R., Jaenicke,R. and Bohm,G. (1999) The HU protein from Thermotoga maritima: Recombinant expression, purification and physicochemical characterization of an extremely hyperthermophilic DNA-binding protein. J. Mol. Biol., 291, 1135-1146.
18. Grove,A. and Lim,L. (2001) High-affinity DNA binding of HU protein from the hyperthermophile Thermotoga maritima. J. Mol. Biol., 311 491-502.
19. Bonnefoy,E. and Rouvière-Yaniv,J. (1991) HU and IHF, two homologous histone-like proteins of Escherichia coli, form different protein-DNA complexes with short DNA fragments. EMBO J., 10, 687-696.
20. Tanaka,I., Appelt,K., Dijk,J., White,S.W. and Wilson,S. (1984) 3-A resolution structure of a protein with histone-like properties in prokaryotes. Nature, 310, 376-381.
21. Vis,H., Mariani,M., Vorgias,C.E., Wilson,K.S., Kaptein,R. and Boelens,R. (1995) Solution structure of the HU protein from Bacillus stearothermophius J. Mol. Biol., 254, 692-703.
22. Rice,P.A., Yang,S.-W., Mizuuchi,K. and Nash,H.A. (1996) Crystal structure of an IHF-DNA complex: A protein-induced DNA U-turn. Cell 87, 1295-1306.
23. Swinger,K.K., Lemberg,K.M., Zhang,Y. and Rice,P.A. (2003) Flexible DNA bending in HU-DNA cocrystal structures. EMBO J., 22, 3749-3760.
24. Christodoulou,E., Rypniewski,W.R. and Vorgias,C.R. (2003) High-resolution X-ray structure of the DNA-binding protein HU from the hyper-thermophilic Thermotoga maritima and the determinants of its thermostability. Extremophiles, 7, 111-122.
25. Mouw,K.W. and Rice,P.A. (2007) Shaping the Borrelia burgdorferi genome: Crystal structure and binding properties of the DNA-bending protein Hbb. Mol. Microbiol., 63, 1319-1330.
26. Grove,A. and Saavedra,T.C. (2002) The role of surface-exposed lysines in wrapping DNA about the bacterial histone-like protein HU. Biochemistry, 41, 7597-7603.
27. Kamau,E., Tsihlis,N.D., Simmons,L.A. and Grove,A. (2005) Surface salt bridges modulate DNA site size of bacterial histone-like HU proteins. Biochem. J., 250, 49-55.
28. Broyles,S.S. and Pettijohn,D.E. (1986) Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosorne-like structures with altered DNA helical pitch. J. Mol. Biol., 187 47-60.
29. Le Hegarat,F., Salti-Montesanto,V., Hauck,Y. and Hirschbein,L. (1993) Purification and characterization of the HU-like protein HPB9 from the Bacillus subtilis nucleoid. Biochim. Biophys. Acta, 1172 101-107.
30. Ross,M.A. and Setlow,P. (2000) The Bacillus subtilis HBsu protein modifies the effects of alpha/beta-type, small acid-soluble spore proteins on DNA. J. Bacteriol., 182, 1942-1948.
31. Chen,C., Ghosh,S. and Grove,A. (2004) Substrate specificity of Helicobacter pylori HU is determined by insufficient stabilization of DNA flexure points. Biochem. J., 383, 343-351.
32. Kobryn,K., Naigamwalla,D.Z. and Chaconas,G. (2000) Site-specific DNA binding and bending by the Borrelia burgdorferi Hbb protein. Mol. Microbiol., 37, 145-155.
33. Bensaid,A., Almeida,A., Drlica,K. and Rouvière-Yaniv,J. (1996) Cross-talk between topoisomerase I and HU in Escherichia coli. J. Mol. Biol., 256, 292-300.
34. Guipaud,O., Marguet,E., Noll,K.M., Bouthier de la Tour,C. and Forterre,P. (1997) Both DNA gyrase and reverse gyrase are present in the hyperthermophilic bacterium Thermotoga maritima. Proc. Natl Acad. Sci. USA, 94, 10606-10611.
35. Whitehall,S.K., Kassavetis,G.A. and Geiduschek,E.P. (1995) The symmetry of the yeast U6 RNA gene's TATA box and the orientation of the TATA-binding protein in yeast TFIIIB. Genes Dev., 9, 2974-2985.
36. Ghosh,S. and Grove,A. (2004) Histone-like protein HU from Deinococcus radiodurans binds preferentially to four-way DNA junctions. J. Mol. Biol., 337, 561-571.
37. Wang,J.C. (1974) The degree of unwinding of the DNA helix by ethidium. I. Titration of twisted PM2 DNA molecules in alkaline cesium chloride density gradients. J. Mol. Biol., 89, 783-801.
38. Malcolm,A.D. and Snounou,G. (1983) Netropsin increases the linking number of DNA. Cold Spring Harb. Symp. Quant. Biol., 47, 323-326.
39. Holbrook,J.A., Tsodikov,O.V., Saecker,R.M. and Record,M.T. Jr. (2001) Specific and non-specific interactions of integration host factor with DNA: Thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding. J. Mol. Biol., 310, 379-401.
40. Grove,A. (2003) Surface salt bridges modulate DNA wrapping by the type II DNA binding protein TFI. Biochemistry, 42, 8739-8747.
41. Rudnick,J. and Bruinsma,R. (1999) DNA-protein cooperative binding through variable-range elastic coupling. Biophys. J., 76, 1725-1733.
42. Köhler,P. and Marahiel,M.A. (1997) Association of the histone-like protein HBsu with the nucleoid of Bacillus subtilis. J. Bacteriol. 179, 2060-2064.
43. Woldringh,C.L. (2002) The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol. Microbiol., 45, 17-29.
44. Nelson,K.E., Clayton,R.A., Gill,S.R., Gwinn,M.L., Dodson,R.J., Haft,D.H., Hickey,E.K., Peterson,J.D., Nelson,W.C., Ketchum,K.A. et al. (1999) Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature, 399, 323-329.
45. Bouthier de la Tour,C., Portemer,C., Huber,R., Forterre,P. and Duguet,M. (1991) Reverse gyrase in thermophilic eubacteria. J. Bacteriol., 173, 3921-3923.
46. Decanniere,K., Babu,A.M., Sandman,K., Reeve,J.N. and Heinemann,U. (2000) Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic, archaeon Methanothermus fervidus. J. Mol. Biol. 303, 35-47.
47. Grayling,R.A., Sandman,K. and Reeve,J.N. (1996) DNA stability and DNA binding proteins. Adv. Protein Chem., 48, 437-467.
48. Marc,F., Sandman,K., Lurz,R. and Reeve,J.N. (2002) Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J. Biol. Chem., 277, 30879-30886.
49. Musgrave,D.R., Sandman,K.M. and Reeve,J.N. (1991) DNA binding by the archaeal histone HMf results in positive supercoiling. Proc. Natl Acad Sci. USA, 88, 10397-10401.
50. 2 tetramer of the nucleosome with positively supercoiled DNA minicircles: Potential flipping of the protein from a left- to a right-handed superhelical form. Proc. Natl Acad. Sci. USA, 93, 7588-7593.
51. Napoli,A., Kvaratskelia,M., White,M.F., Rossi,M. and Ciaramella,M. (2001) A novel member of the bacterial-archaeal regulator family is a nonspecific DNA-binding protein and induces positive supercoiling. J. Biol. Chem., 276, 10745-10752.
52. Pavlicek,J.W., Oussatcheva,E.A., Sinden,R.R., Potaman,V.N., Sankey,O.F. and Lyubchenko,Y.L. (2004) Supercoiling-induced DNA bending. Biochemistry, 43, 10664-10668.
53. Pulleyblank,D.E., Shure,M., Tang,D., Vinograd,J. and Vosberg,H.P. (1975) Action of nicking-closing enzyme on supercoiled and nonsupercoiled closed circular DNA: Formation of a Boltzmann distribution of topological isomers. Proc. Natl Acad. Sci. USA, 72, 4280-4284.
54. Depew,D.E. and Wang,J.C. (1975) Conformational fluctuations of DNA helix. Proc. Natl Acad. Sci. USA, 72, 4275-4279.
55. Wang,J.C. (1979) Helical repeat of DNA in solution. Proc. Natl Acad. Sci. USA, 76, 200-203.
56. Skoko,D., Yan,J., Johnson,R.C. and Marko,J.F. (2005) Low-force DNA condensation and discontinuous high-force decondensation reveal a loop-stabilizing function of the protein Fis. Phys. Rev. Lett., 95, 208101.
57. Dame,R.T. and Goosen,N. (2002) HU: Promoting or counteracting DNA compaction? FEBS Lett., 529, 151-156.
58. van Noort,J., Verbrugge,S., Goosen,N., Dekker,C. and Dame,R.T. (2004) Dual architectural roles of HU: Formation of flexible hinges and rigid filaments. Proc. Natl Acad. Sci. USA, 101, 6969-6974.
59. Sagi,D., Friedman,N., Vorgias,C., Oppenheim,A.B. and Stavans,J. (2004) Modulation of DNA conformations through the formation of alternative high-order HU-DNA complexes. J. Mol. Biol., 341, 419-428.
60. Salomo,M., Kroy,K., Kegler,K., Gutsche,C., Struhalla,M., Reinmuth,J., Skokov,W., Immisch,C., Hahn,U. and Kremer,F. (2006) Binding of TmHU to single dsDNA as observed by optical tweezers. J. Mol. Biol., 359, 769-776.