A DNA damage checkpoint in caulobacter crescentus inhibits cell division through a direct interaction with FtsW

Genes and Development

Volumn 25, Issue 12, 2011, Pages 1328-1343

  Modell, Joshua W ^a   Hopkins, Alexander C ^a   Laub, Michael T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Caulobacter crescentus; Cell division; Checkpoint; Dna damage; Ftsw

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; CTRA PROTEIN; DNA; FTSW PROTEIN; FTSZ PROTEIN; MEMBRANE PROTEIN; REGULATOR PROTEIN; SIDA PROTEIN; SOS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CAULOBACTER CRESCENTUS; CELL CYCLE ARREST; CELL DAMAGE; CELL DIVISION; CONTROLLED STUDY; CYTOKINESIS; DNA DAMAGE; GENE OVEREXPRESSION; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULON;

BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL MEMBRANE; DNA DAMAGE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MUTATION; PEPTIDOGLYCAN; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES;

EID: 79959677792     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.2038911     Document Type: Article

References (54)

1. Adams DW, Errington J. 2009. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7: 642-653.
2. Alexeeva S, Gadella TW Jr, Verheul J, Verhoeven GS, den Blaauwen T. 2010. Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77: 384-398.
3. Bernhardt TG, de Boer PA. 2005. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol Cell 18: 555-564.
4. Biondi EG, Skerker JM, Arif M, Prasol MS, Perchuk BS, Laub MT. 2006. A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 59: 386-401.
5. Briley K Jr, Prepiak P, Dias MJ, Hahn J, Dubnau D. 2011. Maf acts downstream of ComGA to arrest cell division in competent cells of B. subtilis. Mol Microbiol doi: 10.1111/j.1365-2958.2011.07695.x.
6. Burkholder WF, Kurtser I, Grossman AD. 2001. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104: 269-279.
7. Butala M, Zgur-Bertok D, Busby SJ. 2009. The bacterial LexA transcriptional repressor. Cell Mol Life Sci 66: 82-93.
8. Chauhan A, Lofton H, Maloney E, Moore J, Fol M, Madiraju MV, Rajagopalan M. 2006. Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase. Mol Microbiol 62: 132-147.
9. Corbin BD, Geissler B, Sadasivam M, Margolin W. 2004. Z-ringindependent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J Bacteriol 186: 7736-7744.
10. Costa T, Priyadarshini R, Jacobs-Wagner C. 2008. Localization of PBP3 in Caulobacter crescentus is highly dynamic and largely relies on its functional transpeptidase domain. Mol Microbiol 70: 634-651.
11. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113: 767-776.
12. da Rocha RP, Paquola AC, Marques Mdo V, Menck CF, Galhardo RS. 2008. Characterization of the SOS regulon of Caulobacter crescentus. J Bacteriol 190: 1209-1218.
13. Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, Basu J. 2006. Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsWand PBP3 inmycobacteria. MolMicrobiol 62: 1655-1673.
14. Degnen ST, Newton A. 1972. Chromosome replication during development in Caulobacter crescentus. JMol Biol 64: 671-680.
15. Eichenberger P, Fawcett P, Losick R. 2001. A three-protein inhibitor of polar septation during sporulation in Bacillus subtilis. Mol Microbiol 42: 1147-1162.
16. Erill I, Campoy S, Barbe J. 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev 31: 637-656.
17. Errington J, Daniel RA, Scheffers DJ. 2003. Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52-65.
18. Gerding MA, Liu B, Bendezu FO, Hale CA, Bernhardt TG, de Boer PA. 2009. Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J Bacteriol 191: 7383-7401.
19. Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15: R514-R526. doi: 10.1016/j.cub.2005.06.038.
20. Goley ED, Yeh YC, Hong SH, Fero MJ, Abeliuk E, McAdams HH, Shapiro L. 2011. Assembly of the Caulobacter cell division machine. MolMicrobiol doi: 10.1111/j.1365-2958.2011.07677.x.
21. Gottesman S, Halpern E, Trisler P. 1981. Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol 148: 265-273.
22. Handler AA, Lim JE, Losick R. 2008. Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol Microbiol 68: 588-599.
23. Harper JW, Elledge SJ. 2007. The DNA damage response: ten years after. Mol Cell 28: 739-745.
24. Hartwell LH, Weinert TA. 1989. Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629-634.
25. Hemm MR, Paul BJ, Schneider TD, Storz G, Rudd KE. 2008. Small membrane proteins found by comparative genomics and ribosome binding site models. Mol Microbiol 70: 1487-1501.
26. Hemm MR, Paul BJ, Miranda-Rios J, Zhang A, Soltanzad N, Storz G. 2010. Small stress response proteins in Escherichia coli: proteins missed by classical proteomic studies. J Bacteriol 192: 46-58.
27. Hill TM, Sharma B, Valjavec-Gratian M, Smith J. 1997. sfiindependent filamentation in Escherichia coli is lexA dependent and requires DNA damage for induction. J Bacteriol 179: 1931-1939.
28. Holtje JV. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
29. Huisman O, D'Ari R. 1981. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature 290: 797-799.
30. Justice SS, Garcia-Lara J, Rothfield LI. 2000. Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery. Mol Microbiol 37: 410-423.
31. Karimova G, Dautin N, Ladant D. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187: 2233-2243.
32. Kawai Y, Ogasawara N. 2006. Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152: 1129-1141.
33. Kawai Y, Moriya S, Ogasawara N. 2003. Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol Microbiol 47: 1113-1122.
34. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
35. Laub MT, McAdams HH, Feldblyum T, Fraser CM, Shapiro L. 2000. Global analysis of the genetic network controlling a bacterial cell cycle. Science 290: 2144-2148.
36. Laub MT, Chen SL, Shapiro L, McAdams HH. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci 99: 4632-4637.
37. Little JW, Mount DW. 1982. The SOS regulatory system of Escherichia coli. Cell 29: 11-22.
38. Lutkenhaus J. 2007. Assembly dynamics of the bacterialMinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562.
39. Lutkenhaus J, Addinall SG. 1997. Bacterial cell division and the Z ring. Annu Rev Biochem 66: 93-116.
40. Mercer KL, Weiss DS. 2002. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J Bacteriol 184: 904-912.
41. Mo AH, Burkholder WF. 2010. YneA, an SOS-induced inhibitor of cell division in Bacillus subtilis, is regulated posttranslationally and requires the transmembrane region for activity. J Bacteriol 192: 3159-3173.
42. Mohammadi T, van Dam V, Sijbrandi R, Vernet T, Zapun A, Bouhss A, Diepeveen-de Bruin M, Nguyen-Disteche M, de Kruijff B, Breukink E. 2011. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J 30: 1425-1432.
43. Moll A, Thanbichler M. 2009. FtsN-like proteins are conserved components of the cell division machinery in proteobacteria. Mol Microbiol 72: 1037-1053.
44. Mukherjee A, Cao C, Lutkenhaus J. 1998. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci 95: 2885-2890.
45. Ogino H, Teramoto H, Inui M, Yukawa H. 2008. DivS, a novel SOS-inducible cell-division suppressor in Corynebacterium glutamicum. Mol Microbiol 67: 597-608.
46. Opperman T, Murli S, Smith BT, Walker GC. 1999. A model for a umuDC-dependent prokaryotic DNA damage checkpoint. Proc Natl Acad Sci 96: 9218-9223.
47. Quardokus EM, Din N, Brun YV. 2001. Cell cycle and positional constraints on FtsZ localization and the initiation of cell division in Caulobacter crescentus. MolMicrobiol 39: 949-959.
48. Rico AI, Garcia-Ovalle M, Palacios P, Casanova M, Vicente M. 2010. Role of Escherichia coli FtsN protein in the assembly and stability of the cell division ring. Mol Microbiol 76: 760-771.
49. Spratt BG. 1977. Temperature-sensitive cell division mutants of Escherichia coli with thermolabile penicillin-binding proteins. J Bacteriol 131: 293-305.
50. Vicente M, Rico AI, Martinez-Arteaga R, Mingorance J. 2006. Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188: 19-27.
51. Weart RB, Lee AH, Chien AC, Haeusser DP, Hill NS, Levin PA. 2007. A metabolic sensor governing cell size in bacteria. Cell 130: 335-347.
52. White CL, Kitich A, Gober JW. 2010. Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD. Mol Microbiol 76: 616-633.
53. Wortinger M, Sackett MJ, Brun YV. 2000. CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 19: 4503-4512.
54. Wu LJ, Errington J. 2004. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925.