The actinobacterial signature protein ParJ (SCO1662) regulates ParA polymerization and affects chromosome segregation and cell division during Streptomyces sporulation

Molecular Microbiology

Volumn 78, Issue 6, 2010, Pages 1403-1415

  Ditkowski, Bartosz ^a   Troć, Paulina ^b   Ginda, Katarzyna ^b   Donczew, Magdalena ^b   Chater, Keith F ^c   Zakrzewska Czerwińska, Jolanta ^a,b   Jakimowicz, Dagmara ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b UNIVERSITY OF WROC AW   (Poland)

^c NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; PROTEIN PARA; PROTEIN PARJ; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BACTERIAL SPORE; CELL DIVISION; CHROMOSOME SEGREGATION; IN VITRO STUDY; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; SPOROGENESIS; STREPTOMYCES COELICOLOR;

BACTERIAL PROTEINS; CELL DIVISION; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; POLYMERIZATION; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); STREPTOMYCES; STREPTOMYCES COELICOLOR; STREPTOMYCINEAE;

EID: 78650005661     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07409.x     Document Type: Article

References (38)

1. Autret, S., Nair, R., and 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. Barillà, D., Rosenberg, M.F., Nobbmann, U., and Hayes, F. (2005) Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J 24: 1453-1464.
3. Barillà, D., Carmelo, E., and Hayes, F. (2007) The tail of the ParG DNA segregation protein remodels ParF polymers and enhances ATP hydrolysis via an arginine finger-like motif. Proc Natl Acad Sci USA 104: 1811-1816.
4. Bouet, J.Y., Ah-Seng, Y., Benmeradi, N., and Lane, D. (2007) Polymerization of SopA partition ATPase: regulation by DNA binding and SopB. Mol Microbiol 63: 468-481.
5. Donovan, C., Schwaiger, A., Krämer, R., and Bramkamp, M. (2010) Subcellular localization and characterization of the ParAB system from Corynebacterium glutamicum. J Bacteriol 192: 3441-3451.
6. Easter, J., Jr, and Gober, J.W. (2002) ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol Cell 10: 427-434.
7. Ebersbach, G., and Gerdes, K. (2004) Bacterial mitosis: partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Microbiol 52: 385-398.
8. Flärdh, K. (2003) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6: 564-571.
9. Flärdh, K., and Buttner, M.J. (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
10. Fogel, M.A., and Waldor, M.K. (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20: 3269-3282.
11. Gao, B., Sugiman-Marangos, S., Junop, M.S., and Gupta, R.S. (2009) Structural and phylogenetic analysis of a conserved actinobacteria-specific protein (ASP1; SCO1997) from Streptomyces coelicolor. BMC Struct Biol 9: 40.
12. Garner, E.C., Campbell, C.S., and Mullins, R.D. (2004) Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 306: 1021-1025.
13. Gerdes, K., Møller-Jensen, J., and Bugge Jensen, R. (2000) Plasmid and chromosome partitioning: surprises from phylogeny. Mol Microbiol 37: 455-466.
14. Gerdes, K., Møller-Jensen, J., Ebersbach, G., Kruse, T., and Nordström, K. (2004) Bacterial mitotic machineries. Cell 116: 359-366.
15. Gust, B., Challis, G.L., Fowler, K., Kieser, T., and Chater, K.F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100: 1541-1546.
16. Hayes, F., and Barillà, D. (2006) The bacterial segregosome: a dynamic nucleoprotein machine for DNA trafficking and segregation. Nat Rev Microbiol 4: 133-143.
17. Jakimowicz, D., Chater, K., and Zakrzewska-Czerwińska, J. (2002) The ParB protein of Streptomyces coelicolor A3(2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome. Mol Microbiol 45: 1365-1377.
18. Jakimowicz, D., Gust, B., Zakrzewska-Czerwińska, J., and Chater, K.F. (2005) Developmental-stage-specific assembly of ParB complexes in Streptomyces coelicolor hyphae. J Bacteriol 187: 3572-3580.
19. Jakimowicz, D., Mouz, S., Zakrzewska-Czerwińska, J., and Chater, K.F. (2006) Developmental control of a parAB promoter leads to formation of sporulation-associated ParB complexes in Streptomyces coelicolor. J Bacteriol 188: 1710-1720.
20. Jakimowicz, D., Zydek, P., Kois, A., Zakrzewska-Czerwińska, J., and Chater, K.F. (2007) Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol Microbiol 65: 625-641.
21. Karimova, G., Ullmann, A., and Ladant, D. (2000) A bacterial two-hybrid system that exploits a cAMP signaling cascade in Escherichia coli. Methods Enzymol 328: 59-73.
22. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich: The John Innes Foundation.
23. Kim, H.J., Calcutt, M.J., Schmidt, F.J., and Chater, K.F. (2000) Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J Bacteriol 182: 1313-1320.
24. Leonard, T.A., Butler, P.J., and Löwe, J. (2004) Structural analysis of the chromosome segregation protein Spo0J from Thermus thermophilus. Mol Microbiol 53: 419-432.
25. Leonard, T.A., Butler, P.J., and Löwe, J. (2005a) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J 24: 270-282.
26. Leonard, T.A., Møller-Jensen, J., and Löwe, J. (2005b) Towards understanding the molecular basis of bacterial DNA segregation. Philos Trans R Soc Lond B Biol Sci 360: 523-535.
27. Lim, G.E., Derman, A.I., and Pogliano, J. (2005) Bacterial DNA segregation by dynamic SopA polymers. Proc Natl Acad Sci USA 102: 17658-17663.
28. Lin, D.C., and Grossman, A.D. (1998) Identification and characterization of a bacterial chromosome partitioning site. Cell 92: 675-685.
29. McCormick, J.R., Su, E.P., Driks, A., and Losick, R. (1994) Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol Microbiol 14: 243-254.
30. Marston, A.L., and Errington, J. (1999) Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell 4: 673-682.
31. Møller-Jensen, J., Borch, J., Dam, M., Jensen, R.B., Roepstorff, P., and Gerdes, K. (2003) Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell 12: 1477-1487.
32. Murray, H., and Errington, J. (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74-84.
33. Nisa, S., Blokpoel, M.C., Robertson, B.D., Tyndall, J.D., Lun, S., Bishai, W.R., and O'Toole, R. (2010) Targeting the chromosome partitioning protein ParA in tuberculosis drug discovery. J Antimicrob Chemother doi:10.1093/jac/dkq311.
34. Quisel, J.D., Lin, D.C., and Grossman, A.D. (1999) Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell 4: 665-672.
35. Ringgaard, S., Van Zon, J., Howard, M., and Gerdes, K. (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369-19374.
36. Ruban-Ośmiałowska, B., Jakimowicz, D., Smulczyk-Krawczyszyn, A., Chater, K.F., and Zakrzewska-Czerwińska, J. (2006) Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J Bacteriol 188: 7311-7316.
37. Smith, C.P., and Chater, K.F. (1988) Cloning and transcription analysis of the entire glycerol utilization (gylABX) operon of Streptomyces coelicolor A3(2) and identification of a closely associated transcription unit. Mol Gen Genet 211: 129-137.
38. Toro, E., and Shapiro, L. (2010) Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol 2: a000349.