The ATPase SpoIIIE Transports DNA across Fused Septal Membranes during Sporulation in Bacillus subtilis

Cell

Volumn 131, Issue 7, 2007, Pages 1301-1312

  Burton, Briana M ^a   Marquis, Kathleen A ^a   Sullivan, Nora L ^a   Rapoport, Tom A ^a   Rudner, David Z ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CELLCYCLE; MICROBIO; PROTEINS

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA; PROTEIN SPOIIIE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BIOASSAY; CELL SEPARATION; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINESIS; ELECTRON MICROSCOPY; LIPID BILAYER; NONHUMAN; PRIORITY JOURNAL; SPOROGENESIS;

BACILLUS SUBTILIS;

EID: 37349090734     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.11.009     Document Type: Article

References (51)

1. Aussel L., Barre F.X., Aroyo M., Stasiak A., Stasiak A.Z., and Sherratt D. FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108 (2002) 195-205
2. Bartosik A.A., and Jagura-Burdzy G. Bacterial chromosome segregation. Acta Biochim. Pol. 52 (2005) 1-34
3. Bath J., Wu L.J., Errington J., and Wang J.C. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290 (2000) 995-997
4. Ben-Yehuda S., Rudner D.Z., and Losick R. Assembly of the SpoIIIE DNA translocase depends on chromosome trapping in Bacillus subtilis. Curr. Biol. 13 (2003) 2196-2200
5. Bernhardt T.G., and de Boer P.A. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18 (2005) 555-564
6. Bigot S., Saleh O.A., Cornet F., Allemand J.F., and Barre F.X. Oriented loading of FtsK on KOPS. Nat. Struct. Mol. Biol. 13 (2006) 1026-1028
7. Bigot S., Sivanathan V., Possoz C., Barre F.X., and Cornet F. FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64 (2007) 1434-1441
8. Britton R.A., and Grossman A.D. Synthetic lethal phenotypes caused by mutations affecting chromosome partitioning in Bacillus subtilis. J. Bacteriol. 181 (1999) 5860-5864
9. Broder D.H., and Pogliano K. Forespore engulfment mediated by a ratchet-like mechanism. Cell 126 (2006) 917-928
10. Cabezon E., and de la Cruz F. TrwB: an F(1)-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Res. Microbiol. 157 (2006) 299-305
11. Chary V.K., and Piggot P.J. Postdivisional synthesis of the Sporosarcina ureae DNA translocase SpoIIIE either in the mother cell or in the prespore enables Bacillus subtilis to translocate DNA from the mother cell to the prespore. J. Bacteriol. 185 (2003) 879-886
12. Chen I., Christie P.J., and Dubnau D. The ins and outs of DNA transfer in bacteria. Science 310 (2005) 1456-1460
13. Christie P.J., Atmakuri K., Krishnamoorthy V., Jakubowski S., and Cascales E. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59 (2005) 451-485
14. Corre J., and Louarn J.M. Extent of the activity domain and possible roles of FtsK in the Escherichia coli chromosome terminus. Mol. Microbiol. 56 (2005) 1539-1548
15. Dworkin J., and Losick R. Differential gene expression governed by chromosomal spatial asymmetry. Cell 107 (2001) 339-346
16. Errington J. Septation and chromosome segregation during sporulation in Bacillus subtilis. Curr. Opin. Microbiol. 4 (2001) 660-666
17. Errington J., Bath J., and Wu L.J. DNA transport in bacteria. Nat. Rev. Mol. Cell Biol. 2 (2001) 538-545
18. Frandsen N., Barák I., Karmazyn-Campelli C., and Stragier P. Transient gene asymmetry during sporulation and establishment of cell specificity in Bacillus subtilis. Genes Dev. 13 (1999) 394-399
19. Gomis-Rüth F.X., and Coll M. Structure of TrwB, a gatekeeper in bacterial conjugation. Int. J. Biochem. Cell Biol. 33 (2001) 839-843
20. Gomis-Rüth F.X., Moncalián G., Pérez-Luque R., González A., Cabezón E., de la Cruz F., and Coll M. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409 (2001) 637-641
21. Gunton J.E., Gilmour M.W., Baptista K.P., Lawley T.D., and Taylor D.E. Interaction between the co-inherited TraG coupling protein and the TraJ membrane-associated protein of the H-plasmid conjugative DNA transfer system resembles chromosomal DNA translocases. Microbiology 153 (2007) 428-441
22. Harwood C.R., and Cutting S.M. Molecular Biological Methods for Bacillus (1990), Wiley, New York
23. Hilbert D.W., Chary V.K., and Piggot P.J. Contrasting effects of sigmaE on compartmentalization of sigmaF activity during sporulation of Bacillus subtilis. J. Bacteriol. 186 (2004) 1983-1990
24. Hillen W., and Berens C. Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu. Rev. Microbiol. 48 (1994) 345-369
25. Iyer L.M., Makarova K.S., Koonin E.V., and Aravind L. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 32 (2004) 5260-5279
26. Khvorova A., Chary V.K., Hilbert D.W., and Piggot P.J. The chromosomal location of the Bacillus subtilis sporulation gene spoIIR is important for its function. J. Bacteriol. 182 (2000) 4425-4429
27. Lau I.F., Filipe S.R., Søballe B., Økstad O.A., Barre F.X., and Sherratt D.J. Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol. Microbiol. 49 (2003) 731-743
28. Levy O., Ptacin J.L., Pease P.J., Gore J., Eisen M.B., Bustamante C., and Cozzarelli N.R. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc. Natl. Acad. Sci. USA 102 (2005) 17618-17623
29. Li Z., and Piggot P.J. Development of a two-part transcription probe to determine the completeness of temporal and spatial compartmentalization of gene expression during bacterial development. Proc. Natl. Acad. Sci. USA 98 (2001) 12538-12543
30. Liu N.J., Dutton R.J., and Pogliano K. Evidence that the SpoIIIE DNA translocase participates in membrane fusion during cytokinesis and engulfment. Mol. Microbiol. 59 (2006) 1097-1113
31. Massey T.H., Mercogliano C.P., Yates J., Sherratt D.J., and Löwe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell 23 (2006) 457-469
32. Michaelis C., Ciosk R., and Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91 (1997) 35-45
33. Nesmeyanova M.A. On the possible participation of acid phospholipids in the translocation of secreted proteins through the bacterial cytoplasmic membrane. FEBS Lett. 142 (1982) 189-193
34. Pease P.J., Levy O., Cost G.J., Gore J., Ptacin J.L., Sherratt D., Bustamante C., and Cozzarelli N.R. Sequence-directed DNA translocation by purified FtsK. Science 307 (2005) 586-590
35. Pogliano K., Hofmeister A.E., and Losick R. Disappearance of the sigma E transcription factor from the forespore and the SpoIIE phosphatase from the mother cell contributes to establishment of cell-specific gene expression during sporulation in Bacillus subtilis. J. Bacteriol. 179 (1997) 3331-3341
36. Pogliano J., Osborne N., Sharp M.D., Abanes-De Mello A., Perez A., Sun Y.L., and Pogliano K. A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol. Microbiol. 31 (1999) 1149-1159
37. Preble A.M., Giddings T.H., and Dutcher S.K. Extragenic bypass suppressors of mutations in the essential gene BLD2 promote assembly of basal bodies with abnormal microtubules in Chlamydomonas reinhardtii. Genetics 157 (2001) 163-181
38. Rudner D.Z., and Losick R. A sporulation membrane protein tethers the pro-sigmaK processing enzyme to its inhibitor and dictates its subcellular localization. Genes Dev. 16 (2002) 1007-1018
39. Rudner D.Z., Pan Q., and Losick R.M. Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc. Natl. Acad. Sci. USA 99 (2002) 8701-8706
40. Sharp M.D., and Pogliano K. An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc. Natl. Acad. Sci. USA 96 (1999) 14553-14558
41. Sharp M.D., and Pogliano K. Role of cell-specific SpoIIIE assembly in polarity of DNA transfer. Science 295 (2002) 137-139
42. Sharp M.D., and Pogliano K. The membrane domain of SpoIIIE is required for membrane fusion during Bacillus subtilis sporulation. J. Bacteriol. 185 (2003) 2005-2008
43. Sharpe M.E., and Errington J. Postseptational chromosome partitioning in bacteria. Proc. Natl. Acad. Sci. USA 92 (1995) 8630-8634
44. Wang S.T., Setlow B., Conlon E.M., Lyon J.L., Imamura D., Sato T., Setlow P., Losick R., and Eichenberger P. The forespore line of gene expression in Bacillus subtilis. J. Mol. Biol. 358 (2006) 16-37
45. Wu L.J., and Errington J. Bacillus subtilis spoIIIE protein required for DNA segregation during asymmetric cell division. Science 264 (1994) 572-575
46. Wu L.J., and Errington J. Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis. EMBO J. 16 (1997) 2161-2169
47. Wu L.J., and Errington J. Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Mol. Microbiol. 27 (1998) 777-786
48. Wu L.J., Lewis P.J., Allmansberger R., Hauser P.M., and Errington J. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev. 9 (1995) 1316-1326
49. Youngman P.J., Perkins J.B., and Losick R. Genetic transposition and insertional mutagenesis in Bacillus subtilis with Streptococcus faecalis transposon Tn917. Proc. Natl. Acad. Sci. USA 80 (1983) 2305-2309
50. Yu X.C., Tran A.H., Sun Q., and Margolin W. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180 (1998) 1296-1304
51. Zupancic M.L., Tran H., and Hofmeister A.E. Chromosomal organization governs the timing of cell type-specific gene expression required for spore formation in Bacillus subtilis. Mol. Microbiol. 39 (2001) 1471-1481