ParA-mediated plasmid partition driven by protein pattern self-organization

EMBO Journal

Volumn 32, Issue 9, 2013, Pages 1238-1249

  Hwang, Ling Chin ^a   Vecchiarelli, Anthony G ^a   Han, Yong Woon ^b   Mizuuchi, Michiyo ^a   Harada, Yoshie ^b   Funnell, Barbara E ^c   Mizuuchi, Kiyoshi ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

bacterial chromosome segregation; diffusion ratchet; nucleoid; protein gradient; spatial organization

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PARA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CELL FREE SYSTEM; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; DIFFUSION; DISSOCIATION; DNA BINDING; DNA PROTEIN COMPLEX; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HYDROLYSIS; IN VIVO STUDY; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DNA INTERACTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIOPHAGE P1; CELL DIVISION; DNA, BACTERIAL; F FACTOR; HYDROLYSIS; KINETICS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TIME-LAPSE IMAGING; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 84877631843     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.34     Document Type: Article

References (30)

1. Adachi S, Hori K, Hiraga S (2006) Subcellular positioning of F plasmid mediated by dynamic localization of SopA and SopB. J Mol Biol 356: 850-863
2. Barilla D, Rosenberg MF, Nobbmann U, Hayes F (2005) Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J 24: 1453-1464
3. Bouet JY, Funnell BE (1999) P1 ParA interacts with the P1 partition complex at parS and an ATP-ADP switch controls ParA activities. EMBO J 18: 1415-1424
4. Castaing JP, Bouet JY, Lane D (2008) F plasmid partition depends on interaction of SopA with non-specific DNA. Mol Microbiol 70: 1000-1011
5. Davey MJ, Funnell BE (1994) The P1 plasmid partition protein ParA. A role for ATP in site-specific DNA binding. J Biol Chem 269: 29908-29913
6. Davis MA, Martin KA, Austin SJ (1992) Biochemical activities of the ParA partition protein of the P1 plasmid. Mol Microbiol 6: 1141-1147
7. Ebersbach G, Gerdes K (2001) The double par locus of virulence factor pB171: DNA segregation is correlated with oscillation of ParA. Proc Natl Acad Sci USA 98: 15078-15083
8. Ebersbach G, Gerdes K (2005) Plasmid segregation mechanisms. Annu Rev Genet 39: 453-479
9. Erdmann N, Petroff T, Funnell BE (1999) Intracellular localization of P1 ParB protein depends on ParA and parS. Proc Natl Acad Sci USA 96: 14905-14910
10. Fung E, Bouet JY, Funnell BE (2001) Probing the ATP-binding site of P1 ParA: partition and repression have different requirements for ATP binding and hydrolysis. EMBO J 20: 4901-4911
11. Funnell BE, Slavcev RA (2004) Partition systems of bacterial plasmids. In: Plasmid Biology (eds) Funnell BE, Phillips GJ. pp 81-103. (Washington, DC: ASM Press)
12. Han YW, Mizuuchi K (2010) Phage Mu transposition immunity: protein pattern formation along DNA by a diffusion-ratchet mechanism. Mol Cell 39: 48-58
13. Hatano T, Niki H (2010) Partitioning of P1 plasmids by gradual distribution of the ATPase ParA. Mol Microbiol 78: 1182-1198
14. Hatano T, Yamaichi Y, Niki H (2007) Oscillating focus of SopA associated with filamentous structure guides partitioning of F plasmid. Mol Microbiol 64: 1198-1213
15. Havey JC, 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
16. Hester CM, Lutkenhaus J (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104: 20326-20331
17. Hirano M, Mori H, Onogi T, Yamazoe M, Niki H, Ogura T, Hiraga S (1998) Autoregulation of the partition genes of the mini-F plasmid and the intracellular localization of their products in Escherichia coli. Mol Gen Genet 257: 392-403
18. Leonard TA, Butler PJ, Lowe J (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J 24: 270-282
19. Lim GE, Derman AI, Pogliano J (2005) Bacterial DNA segregation by dynamic SopA polymers. Proc Natl Acad Sci USA 102: 17658-17663
20. Pratto F, Cicek A, Weihofen WA, Lurz R, Saenger W, Alonso JC (2008) Streptococcus pyogenes pSM19035 requires dynamic assembly of ATP-bound ParA and ParB on parS DNA during plasmid segregation. Nucleic Acids Res 36: 3676-3689
21. Ringgaard S, van Zon J, Howard M, Gerdes K (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369-19374
22. Rodionov O, Yarmolinsky M (2004) Plasmid partitioning and the spreading of P1 partition protein ParB. Mol Microbiol 52: 1215-1223
23. Sengupta M, Nielsen HJ, Youngren B, Austin S (2010) P1 plasmid segregation: accurate redistribution by dynamic plasmid pairing and separation. J Bacteriol 192: 1175-1183
24. Soberon NE, Lioy VS, Pratto F, Volante A, Alonso JC (2011) Molecular anatomy of the Streptococcus pyogenes pSM19035 partition and segrosome complexes. Nucleic Acids Res 39: 2624-2637
25. Vecchiarelli AG, Han YW, Tan X, Mizuuchi M, Ghirlando R, Biertümpfel C, Funnell BE, Mizuuchi K (2010) ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 78: 78-91
26. Vecchiarelli AG, Hwang LC, Mizuuchi K (2013) Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism. Proc Natl Acad Sci USA (in press)
27. Vecchiarelli AG, Mizuuchi K, Funnell BE (2012) Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86: 513-523
28. Vecchiarelli AG, Schumacher MA, Funnell BE (2007) P1 partition complex assembly involves several modes of protein-DNA recognition. J Biol Chem 282: 10944-10952
29. Watanabe E, Wachi M, Yamasaki M, Nagai K (1992) ATPase activity of SopA, a protein essential for active partitioning of F plasmid. Mol Gen Genet 234: 346-352
30. Youngren B, Austin S (1997) Altered ParA partition proteins of plasmid P1 act via the partition site to block plasmid propagation. Mol Microbiol 25: 1023-1030