Multilayer chromosome organization through DNA bending, bridging and extrusion

Current Opinion in Microbiology

Volumn 22, Issue , 2014, Pages 102-110

  Gruber, Stephan ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; BACTERIAL PROTEIN; DNA; DNA BINDING PROTEIN; PROTEIN BINDING;

BACTERIUM; CHROMOSOME STRUCTURE; COMPLEX FORMATION; DNA BINDING; DNA HELIX; MACROMOLECULAR CROWDING; NONHUMAN; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; BACTERIAL GENOME; CHEMISTRY; CHROMOSOME; GENETICS; METABOLISM;

BACTERIAL PROTEINS; CHROMOSOMES; DNA; DNA-BINDING PROTEINS; GENOME, BACTERIAL; PROTEIN BINDING;

EID: 84910095543     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.09.018     Document Type: Review

References (74)

1. Pelletier J., Halvorsen K., Ha B.Y., Paparcone R., Sandler S.J., Woldringh C.L., Wong W.P., Jun S. Physical manipulation of the Escherichia coli chromosome reveals its soft nature. Proc Natl Acad Sci U S A 2012, 109:E2649-E2656.
2. Wang X., Montero Llopis P., Rudner D.Z. Organization and segregation of bacterial chromosomes. Nat Rev Genet 2013, 14:191-203.
3. Wu L.J., Ishikawa S., Kawai Y., Oshima T., Ogasawara N., Errington J. Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 2009, 28:1940-1952.
4. Cho H., McManus H.R., Dove S.L., Bernhardt T.G. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci U S A 2011, 108:3773-3778.
5. Tonthat N.K., Arold S.T., Pickering B.F., Van Dyke M.W., Liang S., Lu Y., Beuria T.K., Margolin W., Schumacher M.A. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 2011, 30:154-164.
6. Rovinskiy N., Agbleke A.A., Chesnokova O., Pang Z., Higgins N.P. Rates of gyrase supercoiling and transcription elongation control supercoil density in a bacterial chromosome. PLoS Genet 2012, 8:e1002845.
7. Vinograd J., Lebowitz J., Radloff R., Watson R., Laipis P. The twisted circular form of polyoma viral DNA. Proc Natl Acad Sci U S A 1965, 53:1104-1111.
8. Swinger K.K., Lemberg K.M., Zhang Y., Rice P.A. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J 2003, 22:3749-3760.
9. Ali Azam T., Iwata A., Nishimura A., Ueda S., Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 1999, 181:6361-6370.
10. Stella S., Cascio D., Johnson R.C. The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev 2010, 24:814-826.
11. Dillon S.C., Dorman C.J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 2010, 8:185-195.
12. Browning D.F., Grainger D.C., Busby S.J. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 2010, 13:773-780.
13. Koch C., Vandekerckhove J., Kahmann R. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene. Proc Natl Acad Sci U S A 1988, 85:4237-4241.
14. Friedman D.I. Integration host factor: a protein for all reasons. Cell 1988, 55:545-554.
15. Gupta M., Sajid A., Sharma K., Ghosh S., Arora G., Singh R., Nagaraja V., Tandon V., Singh Y. HupB, a nucleoid-associated protein of Mycobacterium tuberculosis, is modified by serine/threonine protein kinases in vivo. J Bacteriol 2014, 196:2646-2657.
16. Macek B., Mijakovic I., Olsen J.V., Gnad F., Kumar C., Jensen P.R., Mann M. The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 2007, 6:697-707.
17. Sobetzko P., Travers A., Muskhelishvili G. Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci U S A 2012, 109:E42-E50.
18. Valens M., Penaud S., Rossignol M., Cornet F., Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J 2004, 23:4330-4341.
19. Le T.B., Imakaev M.V., Mirny L.A., Laub M.T. High-resolution mapping of the spatial organization of a bacterial chromosome. Science 2013, 342:731-734.
20. Postow L., Hardy C.D., Arsuaga J., Cozzarelli N.R. Topological domain structure of the Escherichia coli chromosome. Genes Dev 2004, 18:1766-1779.
21. Umbarger M.A., Toro E., Wright M.A., Porreca G.J., Bau D., Hong S.H., Fero M.J., Zhu L.J., Marti-Renom M.A., McAdams H.H., et al. The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol Cell 2011, 44:252-264.
22. Niki H., Yamaichi Y., Hiraga S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 2000, 14:212-223.
23. Mercier R., Petit M.A., Schbath S., Robin S., El Karoui M., Boccard F., Espeli O. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 2008, 135:475-485.
24. Dupaigne P., Tonthat N.K., Espeli O., Whitfill T., Boccard F., Schumacher M.A. Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell 2012, 48:560-571.
25. Espeli O., Borne R., Dupaigne P., Thiel A., Gigant E., Mercier R., Boccard F. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 2012, 31:3198-3211.
26. Ben-Yehuda S., Fujita M., Liu X.S., Gorbatyuk B., Skoko D., Yan J., Marko J.F., Liu J.S., Eichenberger P., Rudner D.Z., et al. Defining a centromere-like element in Bacillus subtilis by identifying the binding sites for the chromosome-anchoring protein RacA. Mol Cell 2005, 17:773-782.
27. van Baarle S., Celik I.N., Kaval K.G., Bramkamp M., Hamoen L.W., Halbedel S. Protein-protein interaction domains of Bacillus subtilis DivIVA. J Bacteriol 2013, 195:1012-1021.
28. Ben-Yehuda S., Rudner D.Z., Losick R. RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 2003, 299:532-536.
29. Kahramanoglou C., Seshasayee A.S., Prieto A.I., Ibberson D., Schmidt S., Zimmermann J., Benes V., Fraser G.M., Luscombe N.M. Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res 2011, 39:2073-2091.
30. Lang B., Blot N., Bouffartigues E., Buckle M., Geertz M., Gualerzi C.O., Mavathur R., Muskhelishvili G., Pon C.L., Rimsky S., et al. High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 2007, 35:6330-6337.
31. Noom M.C., Navarre W.W., Oshima T., Wuite G.J., Dame R.T. H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 2007, 17:R913-R914.
32. Dame R.T., Noom M.C., Wuite G.J. Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 2006, 444:387-390.
33. Dame R.T., Wyman C., Goosen N. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res 2000, 28:3504-3510.
34. Wang W., Li G.W., Chen C., Xie X.S., Zhuang X. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 2011, 333:1445-1449.
35. Smits W.K., Grossman A.D. The transcriptional regulator Rok binds A+T-rich DNA and is involved in repression of a mobile genetic element in Bacillus subtilis. PLoS Genet 2010, 6:e1001207.
36. Leonard T.A., Butler P.J., Lowe J. Structural analysis of the chromosome segregation protein Spo0J from Thermus thermophilus. Mol Microbiol 2004, 53:419-432.
37. Schumacher M.A., Mansoor A., Funnell B.E. Structure of a four-way bridged ParB-DNA complex provides insight into P1 segrosome assembly. J Biol Chem 2007, 282:10456-10464.
38. Schumacher M.A., Funnell B.E. Structures of ParB bound to DNA reveal mechanism of partition complex formation. Nature 2005, 438:516-519.
39. Breier A.M., Grossman A.D. 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 2007, 64:703-718.
40. Graham T.G., Wang X., Song D., Etson C.M., van Oijen A.M., Rudner D.Z., Loparo J.J. ParB spreading requires DNA bridging. Genes Dev 2014, 28:1228-1238.
41. Rodionov O., Lobocka M., Yarmolinsky M. Silencing of genes flanking the P1 plasmid centromere. Science 1999, 283:546-549.
42. Murray H., Ferreira H., Errington J. The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 2006, 61:1352-1361.
43. Vecchiarelli A.G., Neuman K.C., Mizuuchi K. A propagating ATPase gradient drives transport of surface-confined cellular cargo. Proc Natl Acad Sci U S A 2014, 111:4880-4885.
44. Sherratt D.J., Arciszewska L.K., Crozat E., Graham J.E., Grainge I. The Escherichia coli DNA translocase FtsK. Biochem Soc Trans 2010, 38:395-398.
45. Wu L.J., Errington J. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 1994, 264:572-575.
46. Bigot S., Saleh O.A., Lesterlin C., Pages C., El Karoui M., Dennis C., Grigoriev M., Allemand J.F., Barre F.X., Cornet F. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 2005, 24:3770-3780.
47. Pease P.J., Levy O., Cost G.J., Gore J., Ptacin J.L., Sherratt D., Bustamante C., Cozzarelli N.R. Sequence-directed DNA translocation by purified FtsK. Science 2005, 307:586-590.
48. Ptacin J.L., Nollmann M., Bustamante C., Cozzarelli N.R. Identification of the FtsK sequence-recognition domain. Nat Struct Mol Biol 2006, 13:1023-1025.
49. Sivanathan V., Allen M.D., de Bekker C., Baker R., Arciszewska L.K., Freund S.M., Bycroft M., Lowe J., Sherratt D.J. The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol 2006, 13:965-972.
50. Ptacin J.L., Nollmann M., Becker E.C., Cozzarelli N.R., Pogliano K., Bustamante C. Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat Struct Mol Biol 2008, 15:485-493.
51. Cattoni D.I., Chara O., Godefroy C., Margeat E., Trigueros S., Milhiet P.E., Nollmann M. SpoIIIE mechanism of directional translocation involves target search coupled to sequence-dependent motor stimulation. EMBO Rep 2013, 14:473-479.
52. Yates J., Zhekov I., Baker R., Eklund B., Sherratt D.J., Arciszewska L.K. Dissection of a functional interaction between the DNA translocase FtsK, and the XerD recombinase. Mol Microbiol 2006, 59:1754-1766.
53. Nolivos S., Sherratt D. The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes. FEMS Microbiol Rev 2014, 38:380-392.
54. Melby T.E., Ciampaglio C.N., Briscoe G., Erickson H.P. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 1998, 142:1595-1604.
55. Lammens A., Schele A., Hopfner K.P. Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases. Curr Biol 2004, 14:1778-1782.
56. Bürmann F., Shin H.C., Basquin J., Soh Y.M., Gimenez-Oya V., Kim Y.G., Oh B.H., Gruber S. An asymmetric SMC-kleisin bridge in prokaryotic condensin. Nat Struct Mol Biol 2013, 20:371-379.
57. Kamada K., Miyata M., Hirano T. Molecular basis of SMC ATPase activation: role of internal structural changes of the regulatory subcomplex ScpAB. Structure 2013, 21:581-594.
58. Danilova O., Reyes-Lamothe R., Pinskaya M., Sherratt D., Possoz C. MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 2007, 65:1485-1492.
59. Gruber S., Errington J. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 2009, 137:685-696.
60. Minnen A., Attaiech L., Thon M., Gruber S., Veening J.W. SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol 2011, 81:676-688.
61. Sullivan N.L., Marquis K.A., Rudner D.Z. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 2009, 137:697-707.
62. Kleine Borgmann L.A., Ries J., Ewers H., Ulbrich M.H., Graumann P.L. The bacterial SMC complex displays two distinct modes of interaction with the chromosome. Cell Rep 2013, 3:1483-1492.
63. Woo J.S., Lim J.H., Shin H.C., Suh M.K., Ku B., Lee K.H., Joo K., Robinson H., Lee J., Park S.Y., et al. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 2009, 136:85-96.
64. Wang X., Tang O.W., Riley E.P., Rudner D.Z. The SMC condensin complex is required for origin segregation in Bacillus subtilis. Curr Biol 2014, 24:287-292.
65. Gruber S., Veening J.W., Bach J., Blettinger M., Bramkamp M., Errington J. Interlinked sister chromosomes arise in the absence of condensin during fast replication in B. subtilis. Curr Biol 2014, 24:293-298.
66. Badrinarayanan A., Reyes-Lamothe R., Uphoff S., Leake M.C., Sherratt D.J. In vivo architecture and action of bacterial structural maintenance of chromosome proteins. Science 2012, 338:528-531.
67. Losada A., Hirano T. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev 2005, 19:1269-1287.
68. Gruber S., Haering C.H., Nasmyth K. Chromosomal cohesin forms a ring. Cell 2003, 112:765-777.
69. Haering C.H., Farcas A.M., Arumugam P., Metson J., Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 2008, 454:297-301.
70. Petrushenko Z.M., Cui Y., She W., Rybenkov V.V. Mechanics of DNA bridging by bacterial condensin MukBEF in vitro and in singulo. EMBO J 2010, 29:1126-1135.
71. Vallet-Gely I., Boccard F. Chromosomal organization and segregation in Pseudomonas aeruginosa. PLoS Genet 2013, 9:e1003492.
72. Alipour E., Marko J.F. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res 2012, 40:11202-11212.
73. Lengronne A., Katou Y., Mori S., Yokobayashi S., Kelly G.P., Itoh T., Watanabe Y., Shirahige K., Uhlmann F. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 2004, 430:573-578.
74. D'Ambrosio C., Schmidt C.K., Katou Y., Kelly G., Itoh T., Shirahige K., Uhlmann F. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 2008, 22:2215-2227.