Atomic Force Microscopy Analysis of the Role of Major DNA-Binding Proteins in Organization of the Nucleoid in Escherichia coli

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Ohniwa, Ryosuke L ^a   Muchaku, Hiroki ^a   Saito, Shinji ^a   Wada, Chieko ^b   Morikawa, Kazuya ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b Yoshida Biological Laboratory   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; FACTOR FOR INVERSION STIMULATION; HEAT UNSTABLE NUCLEOID PROTEIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; HOST FACTOR FOR PHAGE RNA QBETA REPLICATION; INTEGRATION HOST FACTOR; NAKED DNA; RIBONUCLEASE A; SUPPRESSOR OF TD PHENOTYPE A; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL NUCLEOID; CELL NUCLEUS; CELLULAR SECRETION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; MICROBIAL MORPHOLOGY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION;

DNA TOPOISOMERASES, TYPE I; DNA, BACTERIAL; DNA-BINDING PROTEINS; ENDOPEPTIDASE K; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROSCOPY, ATOMIC FORCE; MUTATION;

EID: 84881508032     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072954     Document Type: Article

References (28)

1. Ishihama A, (2009) The nucleoid: an overview. In Böck A, Curtiss R III, Kaper JB, Karp PD, Neidhardt FC, eds. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, DC: ASM Press. doi:10.1128/ecosal.2.6.
2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, et al. (2002) Chapter 4: DNA and Chromosomes. In: Alberts B, Johnson A, Lewis J, Raff M, Roberts K, eds. Molecular Biology of the Cell, 4th edition Chapter. New York: Garland Publishing House Science. pp. pp. 235-298.
3. Paull TT, Haykinson MJ, Johnson RC, (1993) The nonspecific DNA-binding and-bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev 7: 1521-1534. doi:10.1101/gad.7.8.1521. PubMed: 8339930.
4. Swinger KK, Rice PA, (2004) IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 14: 28-35. doi:10.1016/j.sbi.2003.12.003. PubMed: 15102446.
5. Swinger KK, Lemberg KM, Zhang Y, Rice PA, (2003) Flexible DNA bending in HU-DNA cocrystal structures. EMBO J 22: 3749-3760. doi:10.1093/emboj/cdg351. PubMed: 12853489.
6. Dame RT, Noom MC, Wuite GJ, (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444: 387-390. doi:10.1038/nature05283. PubMed: 17108966.
7. Altuvia S, Almirón M, Huisman G, Kolter R, Storz G, (1994) The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13: 265-272. doi:10.1111/j.1365-2958.1994.tb00421.x. PubMed: 7984106.
8. Hübner P, Arber W, (1989) Mutational analysis of a prokaryotic recombinational enhancer element with two functions. EMBO J 8: 577-585. PubMed: 2656257.
9. Skoko D, Yan J, Johnson RC, Marko JF, (2005) Low-force DNA condensation and discontinuous high-force decondensation reveal a loop-stabilizing function of the protein Fis. Phys Rev Lett 95: 208101. doi:10.1103/PhysRevLett.95.208101. PubMed: 16384101.
10. Skoko D, Yoo D, Bai H, Schnurr B, Yan J, et al. (2006) Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J Mol Biol 364: 777-798. doi:10.1016/j.jmb.2006.09.043. PubMed: 17045294.
11. Sonnenfield JM, Burns CM, Higgins CF, Hinton JC, (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. doi:10.1016/S0300-9084(01)01232-9. PubMed: 11278075.
12. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, et al. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313: 236-238. doi:10.1126/science.1128794. PubMed: 16763111.
13. Ohniwa RL, Morikawa K, Kim J, Kobori T, Hizume K, et al. (2007) Atomic force microscopy dissects the hierarchy of genome architectures in eukaryote, prokaryote, and chloroplast. Microsc Microanal 13: 3-12. doi:10.1017/S1431927607070055. PubMed: 17234031.
14. Takeyasu K, Kim J, Ohniwa RL, Kobori T, Inose Y, et al. (2004) Genome architecture studied by nanoscale imaging: analyses among bacterial phyla and their implication to eukaryotic genome folding. Cytogenet Genome Res 107: 38-48. doi:10.1159/000079570. PubMed: 15305055.
15. Kim J, Yoshimura SH, Hizume K, Ohniwa RL, Ishihama A, et al. (2004) Fundamental structural units of the Escherichia coli nucleoid revealed by atomic force microscopy. Nucleic Acids Res 32: 1982-1992. doi:10.1093/nar/gkh512. PubMed: 15060178.
16. Ohniwa RL, Morikawa K, Takeshita SL, Kim J, Ohta T, et al. (2007) Transcription-coupled nucleoid architecture in bacteria. Genes Cells 12: 1141-1152. doi:10.1111/j.1365-2443.2007.01125.x. PubMed: 17903174.
17. Morikawa K, Ohniwa RL, Kim J, Maruyama A, Ohta T, et al. (2006) Bacterial nucleoid dynamics: oxidative stress response in Staphylococcus aureus. Genes Cells 11: 409-423. doi:10.1111/j.1365-2443.2006.00949.x. PubMed: 16611244.
18. Ohniwa RL, Ushijima Y, Saito S, Morikawa K, (2011) Proteomic analyses of nucleoid-associated proteins in Escherichia coli, Pseudomonas aeruginosa, Bacillus subtilis, and Staphylococcus aureus. PLOS ONE 6: e19172. doi:10.1371/journal.pone.0019172. PubMed: 21541338.
19. Ohniwa RL, Morikawa K, Ohta T, Wada C, Takeyasu K, (2009) Nucleoid architecture and dynamics. In: Knudsen WD, Bruns SS, eds. Bacterial DNA, DNA Polymerase and DNA Helicase. New York: Nova Science Publisher. pp. pp. 91-117.
20. Azam TA, Ishihama A, (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274: 33105-33113. doi:10.1074/jbc.274.46.33105. PubMed: 10551881.
21. Claret L, Rouviere-Yaniv J, (1997) Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J Mol Biol 273: 93-104. doi:10.1006/jmbi.1997.1310. PubMed: 9367749.
22. Oberto J, Nabti S, Jooste V, Mignot H, Rouviere-Yaniv J, (2009) The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLOS ONE 4: e4367. doi:10.1371/journal.pone.0004367. PubMed: 19194530.
23. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biol: msb, 2: 4100050-E4100051-msb4100050-E4100011. PubMed: 16738554.
24. Ohniwa RL, Morikawa K, Kim J, Ohta T, Ishihama A, et al. (2006) Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25: 5591-5602. doi:10.1038/sj.emboj.7601414. PubMed: 17093499.
25. Takeyasu K, Omote H, Nettikadan S, Tokumasu F, Iwamoto-Kihara A, et al. (1996) Molecular imaging of Escherichia coli F0F1-ATPase in reconstituted membranes using atomic force microscopy. FEBS Lett 392: 110-113. doi:10.1016/0014-5793(96)00796-X. PubMed: 8772185.
26. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ, (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251-260. doi:10.1038/38444. PubMed: 9305837.
27. Wada M, Kano Y, Ogawa T, Okazaki T, Imamoto F, (1988) Construction and characterization of the deletion mutant of hupA and hupB genes in Escherichia coli. J Mol Biol 204: 581-591. doi:10.1016/0022-2836(88)90357-9. PubMed: 3066907.
28. Kano Y, Imamoto F, (1990) Requirement of integration host factor (IHF) for growth of Escherichia coli deficient in HU protein. Gene 89: 133-137. doi:10.1016/0378-1119(90)90216-E. PubMed: 2197178.