ParB spreading requires DNA bridging

Genes and Development

Volumn 28, Issue 11, 2014, Pages 1228-1238

  Graham, Thomas G W ^a   Wang, Xindan ^a   Song, Dan ^a   Etson, Candice M ^a,b   van Oijen, Antoine M ^a,c   Rudner, David Z ^a   Loparo, Joseph J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TUFTS UNIVERSITY   (United States)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Bacterial chromosome segregation; ParB; Single molecule fluorescence; Spo0J

Indexed keywords

CONDENSIN; DNA BINDING PROTEIN; GENOMIC DNA; PROTEIN PARB; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; COLONY FORMING UNIT; COMPLEX FORMATION; DIMERIZATION; DNA BRIDGING; DNA REPLICATION ORIGIN; DNA STRUCTURE; GENETIC CONSERVATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STOICHIOMETRY;

BACTERIAL CHROMOSOME SEGREGATION; PARB; SINGLE-MOLECULE FLUORESCENCE; SPO0J;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CELL NUCLEUS SHAPE; DNA PRIMASE; DNA, BACTERIAL; POINT MUTATION; PROTEIN BINDING;

EID: 84901761890     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.242206.114     Document Type: Article

References (48)

1. Autret S., Nair R, Errington J. 2001. Genetic analysis of the chromosome segregation protein Spo0J of Bacillus subtilis: evidence for separate domains involved in DNA binding and interactions with Soj protein. Mol Microbiol 41: 743-755.
2. Bartosik A.A., Mierzejewska J, Thomas CM, Jagura-Burdzy G. 2009. ParB deficiency in Pseudomonas aeruginosa destabilizes the partner protein ParA and affects a variety of physiological parameters. Microbiology 155: 1080-1092.
3. Becker N.A., Kahn JD, Maher LJ. 2007. Effects of nucleoid proteins on DNA repression loop formation in Escherichia coli. Nucleic Acids Res 35: 3988-4000.
4. Bingle L.E.H., Macartney DP, Fantozzi A, Manzoor SE, Thomas CM. 2005. Flexibility in repression and cooperativity by KorB of broad host range IncP-1 plasmid RK2. J Mol Biol 349: 302-316.
5. Blumberg S., Tkachenko AV, Meiners J-C. 2005. Disruption of protein-mediated DNA looping by tension in the substrate DNA. Biophys J 88: 1692-1701.
6. Breier A.M., Grossman AD. 2007. Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome. Mol Microbiol 64: 703-718.
7. Broedersz C.P., Wang X, Meir Y, Loparo JJ, Rudner DZ, Wingreen NS. 2014. Condensation and localization of the partitioning protein ParB on the bacterial chromosome. Proc Natl Acad Sci (in press).
8. Chen R., Guttenplan SB, Blair KM, Kearns DB. 2009. Role of the sD-dependent autolysins in Bacillus subtilis population heterogeneity. J Bacteriol 191: 5775-5784.
9. Chiu C-M, Manzoor SE, Batt SM, Muntaha St, Bingle LEH, Thomas CM. 2008. Distribution of the partitioning protein KorB on the genome of IncP-1 plasmid RK2. Plasmid 59: 163-175.
10. Dupaigne P., Tonthat NK, Espéli O, Whitfill T, Boccard F, SchumacherMA. 2012. Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell 48: 560-571.
11. Edgar R., Chattoraj DK, Yarmolinsky M. 2001. Pairing of P1 plasmid partition sites by ParB. Mol Microbiol 42: 1363-1370.
12. Finkelstein I.J., Visnapuu M-L, Greene EC. 2010. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468: 983-987.
13. Garner E.C., Campbell CS, Weibel DB, Mullins RD. 2007. Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 315: 1270-1274.
14. Glaser P., Sharpe ME, Raether B, Perego M, Ohlsen K, Errington J. 1997. Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 11: 1160-1168.
15. Gruber S., Errington J. 2009. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685-696.
16. Havey J.C., Vecchiarelli AG, Funnell BE. 2012. ATP-regulated interactions between P1 ParA, ParB and non-specific DNA that are stabilized by the plasmid partition site, parS. Nucleic Acids Res 40: 801-812.
17. Hirano T. 2006. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311-322.
18. Ireton K., Gunther NW, Grossman AD. 1994. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176: 5320-5329.
19. Kusiak M., Gapczynska A, Plochocka D, Thomas CM, Jagura-Burdzy G. 2011. Binding and spreading of ParB on DNA determine its biological function in Pseudomonas aeruginosa. J Bacteriol 193: 3342-3355.
20. Landgraf D., Okumus B, Chien P, Baker TA, Paulsson J. 2012. Segregation of molecules at cell division reveals native protein localization. Nat Methods 9: 480-482.
21. Lee P.S., Grossman AD. 2006. The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis. Mol Microbiol 60: 853-869.
22. Leonard T.A., Butler PJG, Löwe J. 2004. Structural analysis of the chromosome segregation protein Spo0J from Thermus thermophilus. Mol Microbiol 53: 419-432.
23. Lewis P.J., Errington J. 1997. Direct evidence for active segregation of oriC regions of the Bacillus subtilis chromosome and co-localization with the SpoOJ partitioning protein. Mol Microbiol 25: 945-954.
24. Lin D.C., Levin PA, Grossman AD. 1997. Bipolar localization of a chromosome partition protein in Bacillus subtilis. Proc Natl Acad Sci 94: 4721-4726.
25. Liu Y., Chen H, Kenney LJ, Yan J. 2010. A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev 24: 339-344.
26. Livny J., Yamaichi Y, Waldor MK. 2007. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703.
27. Lynch A.S., Wang JC. 1995. SopB protein-mediated silencing of genes linked to the sopC locus of Escherichia coli F plasmid. Proc Natl Acad Sci 92: 1896-1900.
28. Minnen A., Attaiech L, Thon M, Gruber S, Veening J-W. 2011. SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol 81: 676-688.
29. Mohl D.A., Easter J, Gober JW. 2001. The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol Microbiol 42: 741-755.
30. Murray H., Ferreira H, Errington J. 2006. The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61: 1352-1361.
31. Rodionov O., LobockaM, YarmolinskyM. 1999. Silencing of genes flanking the P1 plasmid centromere. Science 283: 546-549.
32. Sankararaman S., Marko JF. 2005. Formation of loops in DNA under tension. Phys Rev E Stat Nonlin Soft Matter Phys 71: 021911.
33. Scholefield G., Whiting R, Errington J, Murray H. 2011. Spo0J regulates the oligomeric state of Soj to trigger its switch from an activator to an inhibitor of DNA replication initiation. Mol Microbiol 79: 1089-1100.
34. Shebelut C.W., Guberman JM, van Teeffelen S, Yakhnina AA, Gitai Z. 2010. Caulobacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci 107: 14194-14198.
35. 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.
36. Skoko D., Li M, Huang Y, Mizuuchi M, Cai M, Bradley CM, Pease P.J., Xiao B, Marko JF, Craigie R, et al. 2009. Barrier-toautointegration factor (BAF) condenses DNA by looping. Proc Natl Acad Sci 106: 16610-16615.
37. Sullivan N.L., Marquis KA, Rudner DZ. 2009. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137: 697-707.
38. Surtees J.A., Funnell BE. 2003. Plasmid and chromosome traffic control: how ParA and ParB drive partition. Curr Top Dev Biol 56: 145-180.
39. Swinger K.K., Rice PA. 2004. IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 14: 28-35.
40. van Noort J, Verbrugge S, Goosen N, Dekker C, Dame RT. 2004. Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci 101: 6969-6974.
41. Vecchiarelli A.G., Mizuuchi K, Funnell BE. 2012. Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86: 513-523.
42. Wagner C., Olbrich C, Brutzer H, Salomo M, Kleinekathö fer U, Keyser U.F., Kremer F. 2011. DNA condensation by TmHU studied by optical tweezers, AFM and molecular dynamics simulations. J Biol Phys 37: 117-131.
43. Wang W., Li G-W, Chen C, Xie XS, Zhuang X. 2011. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333: 1445-1449.
44. Wang X., Montero Llopis P, Rudner DZ. 2013. Organization and segregation of bacterial chromosomes. Nat Rev Genet 14: 191-203.
45. Wright D.J., King K, Modrich P. 1989. The negative charge of Glu-111 is required to activate the cleavage center of EcoRI endonuclease. J Biol Chem 264: 11816-11821.
46. Xiao B., Johnson RC, Marko JF. 2010. Modulation of HU-DNA interactions by salt concentration and applied force. Nucleic Acids Res 38: 6176-6185.
47. Xiao B., Zhang H, Johnson RC, Marko JF. 2011. Force-driven unbinding of proteins HU and Fis from DNA quantified using a thermodynamic Maxwell relation. Nucleic Acids Res 39: 5568-5577.
48. Youngman P.J., Perkins JB, Losick R. 1983. Genetic transposition and insertional mutagenesis in Bacillus subtilis with Streptococcus faecalis transposon Tn917. Proc Natl Acad Sci 80: 2305-2309.