Bacterial scaffold directs pole-specific centromere segregation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 19, 2014, Pages

  Ptacin, Jerod L ^a   Gahlmann, Andreas ^b   Bowman, Grant R ^a,c   Perez, Adam M ^a   Von Diezmann, Alexander R S ^b   Eckart, Michael R ^a   Moerner, W E ^b   Shapiro, Lucy ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF WYOMING   (United States)

Author keywords

ParAB; Prokaryotic; Replication; Soj; Spo0J

Indexed keywords

MOLECULAR SCAFFOLD;

ALLELE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL GROWTH; CELL STRUCTURE; CENTROMERE; CHROMOSOME SEGREGATION; MICROENVIRONMENT; MITOSIS; NONHUMAN; POLAR BODY; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; ULTRASTRUCTURE;

PARAB; PROKARYOTIC; REPLICATION; SOJ; SPO0J;

BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL DIVISION; CENTROMERE; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; CYTOPLASM; MULTIPROTEIN COMPLEXES; SPINDLE APPARATUS;

EID: 84900510259     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405188111     Document Type: Article

References (39)

1. Nevo-Dinur K, Govindarajan S, Amster-Choder O (2012) Subcellular localization of RNA and proteins in prokaryotes. Trends Genet 28(7):314-322.
2. Lutkenhaus J (2012) The ParA/MinD family puts things in their place. Trends Microbiol 20(9):411-418.
3. Leonard TA, Butler PJ, Löwe J (2005) Bacterial chromosome segregation: Structure and DNA binding of the Soj dimer-A conserved biological switch. EMBO J 24(2): 270-282.
4. Vecchiarelli AG, Mizuuchi K, Funnell BE (2012) Surfing biological surfaces: Exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86(3):513-523.
5. Murray H, Ferreira H, Errington J (2006) The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61(5): 1352-1361.
6. Ptacin JL, et al. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12(8):791-798.
7. Hwang LC, et al. (2013) ParA-mediated plasmid partition driven by protein pattern self-organization. EMBO J 32(9):1238-1249.
8. Vecchiarelli AG, et al. (2010) ATP control of dynamic P1 ParA-DNA interactions: A key role for the nucleoid in plasmid partition. Mol Microbiol 78(1):78-91.
9. Fogel MA, Waldor MK (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20(23):3269-3282.
10. 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(46): 19369-19374.
11. Viollier PH, et al. (2004) Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA 101(25):9257-9262.
12. Harms A, Treuner-Lange A, Schumacher D, Søgaard-Andersen L (2013) Tracking of chromosome and replisome dynamics in Myxococcus xanthus reveals a novel chromosome arrangement. PLoS Genet 9(9):e1003802.
13. Yamaichi Y, et al. (2012) A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev 26(20):2348-2360.
14. Ditkowski B, et al. (2013) Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open Biol 3(3):130006.
15. Ginda K, et al. (2013) ParA of Mycobacterium smegmatis co-ordinates chromosome segregation with the cell cycle and interacts with the polar growth determinant DivIVA. Mol Microbiol 87(5):998-1012.
16. Lam H, Schofield WB, Jacobs-Wagner C (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124(5):1011-1023.
17. Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH (2006) Bacterial birth scar proteins mark future flagellum assembly site. Cell 124(5):1025-1037.
18. Bowman GR, et al. (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134(6):945-955.
19. Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in caulobacter. Cell 134(6):956-968.
20. Schofield WB, Lim HC, Jacobs-Wagner C (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29(18):3068-3081.
21. Shebelut CW, Guberman JM, van Teeffelen S, Yakhnina AA, Gitai Z (2010) Caulo-bacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci USA 107(32):14194-14198.
22. Ebersbach G, Gerdes K (2004) Bacterial mitosis: Partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Microbiol 52(2): 385-398.
23. 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(17):4901-4911.
24. 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(4):1089-1100.
25. Murray H, Errington J (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135(1):74-84.
26. Castaing JP, Bouet JY, Lane D (2008) F plasmid partition depends on interaction of SopA with non-specific DNA. Mol Microbiol 70(4):1000-1011.
27. 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(51): 20326-20331.
28. Bowman GR, et al. (2013) Oligomerization and higher-order assembly contribute to sub-cellular localization of a bacterial scaffold. Mol Microbiol 90(4):776-795.
29. Laloux G, Jacobs-Wagner C (2013) Spatiotemporal control of PopZ localization through cell cycle-coupled multimerization. J Cell Biol 201(6):827-841.
30. Gahlmann A, et al. (2013) Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in three dimensions. Nano Lett 13(3):987-993.
31. Bowman GR, et al. (2010) Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function. Mol Microbiol 76(1):173-189.
32. Kiekebusch D, Michie KA, Essen LO, Löwe J, Thanbichler M (2012) Localized di-merization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46(3):245-259.
33. Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28:231-295.
34. Thanbichler M, Shapiro L (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126(1):147-162.
35. Ely B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204:372-384.
36. Tsai JW, Alley MR (2001) Proteolysis of the Caulobacter McpA chemoreceptor is cell cycle regulated by a ClpX-dependent pathway. J Bacteriol 183(17):5001-5007.
37. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C (2011) High-throughput, sub-pixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80(3):612-627.
38. Lew MD, von Diezmann ARS, Moerner WE (2013) Easy-DHPSF open-source software for three-dimensional localization of single molecules with precision beyond the optical diffraction limit. Protocol Exchange, 10.1038/protex.2013. 026.
39. Jun S, Mulder B (2006) Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 103(33): 12388-12393.