Septal localization of forespore membrane proteins during engulfment in Bacillus subtilis

EMBO Journal

Volumn 23, Issue 7, 2004, Pages 1636-1646

  Rubio, Aileen ^a   Pogliano, Kit ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Forespore septal membrane; Membrane protein localization; SpoIIQ; SpoIIR; Sporulation

Indexed keywords

MEMBRANE PROTEIN; PROTEIN SPOIIQ; PROTEIN SPOIIR; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CELL MEMBRANE; CONTROLLED STUDY; GENE EXPRESSION; GENOTYPE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; SPOROGENESIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL MEMBRANE; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; RECOMBINANT FUSION PROTEINS; SIGMA FACTOR; SPORES, BACTERIAL; TRANSCRIPTION FACTORS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); INSERTION SEQUENCES; POSIBACTERIA;

EID: 2342640965     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600171     Document Type: Article

References (57)

1. Abanes-De Mello A, Sun YL, Aung S, Pogliano K (2002) A cytoskeleton-like role for the bacterial cell wall during engulfment of the Bacillus subtilis forespore. Genes Dev 16: 3253-3264
2. Addinall SG, Holland B (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318: 219-236
3. Anderson AJ, Green RS, Sturman AJ, Archibald AR (1978) Cell wall assembly in Bacillus subtilis: location of wall material incorporated during pulsed release of phosphate limitation, its accessibility to bacteriophages and concanavalin A, and its susceptibility to turnover. J Bacteriol 136: 886-899
4. Arigoni F, Guerout-Fleury AM, Barak 1, Stragier P (1999) The SpoIIE phosphatase, the sporulation septum and the establishment of forespore-specific transcription in Bacillus subtilis: a reassessment. Mol Microbiol 31: 1407-1415
5. Ausmees N, Jacobs-Wagner C (2003) Spatial and temporal control of differentiation and cell cycle progression in Caulobacter 'crescentus. Annu Rev Microbiol 57: 225-247
6. Bath J, Wu LJ, Errington J, Wang JC (2000) Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290: 995-997
7. Ben-Yehuda S, Losick R (2002) Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109: 257-266
8. Brandon LD, Goehring N, Janakiraman A, Yan AW, Wu T, Beckwith J, Goldberg MB (2003) IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially circumferentially distributed. Mol Microbiol 50: 45-60
9. Carballido-Lopez R, Errington J (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4: 19-28
10. Clarke-Sturman AJ, Archibald AR, Hancock IC, Harwood CR, Merad T, Hobot JA (1989) Cell wall assembly in Bacillus subtilis: partial conservation of polar wall material and the effect of growth conditions on the pattern of incorporation of new material at the polar caps. J Gen Microbiol 135 (Part 3): 657-665
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. Driks A (2002) Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol 10: 251-254
13. Dubnau D, Davidoff-Abelson R (1971) Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex. J Mol Biol 56: 209-221
14. Eichenberger P, Jensen ST, Conlon EM, van Ooij C, Silvaggi J, Gonzalez-Pastor JE, Fujita M, Ben-Yehuda S, Stragier P, Liu JS, Losick R (2003) The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. J Mol Biol 327: 945-972
15. Evans L, Clarkson J, Yudkin MD, Errington J, Feucht A (2003) Analysis of the interaction between the transcription factor sigmaG and the anti-sigma factor SpolIAB of Bacillus subtilis. J Bacteriol 185: 4615-4619
16. Fawcett P, Eichenberger P, Losick R, Youngman P (2000) The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 97: 8063-8068
17. Frandsen N, Stragier P (1995) Identification and characterization of the Bacillus subtilis spoIIP locus. J Bacteriol 177: 716-722
18. Fujita M, Losick R (2002) An investigation into the compartmentalization of the sporulation transcription factor sigmaE in Bacillus subtilis. Mol Microbiol 43: 27-38
19. Hofmeister AE, Londono-Vallejo A, Harry E, Stragier P, Losick R (1995) Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. subtilis. Cell 83: 219-226
20. Illing N, Errington J (1991) The spoIIIA operon of Bacillus subtilis defines a new temporal class of mother-cell-specific sporulation genes under the control of the sigma E form of RNA polymerase. Mol Microbiol 5: 1927-1940
21. Jacobs C, Hung D, Shapiro L (2001) Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc Natl Acad Sci USA 98: 4095-4100
22. Johnson JE, Lackner LL, de Boer PA (2002) Targeting of (D)MinC/MinD and (D)MinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J Bacteriol 184: 2951-2962
23. Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104: 913-922
24. 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
25. Karow ML, Glaser P, Piggot PJ (1995) Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 92: 2012-2016
26. Kellner EM, Decatur A, Moran Jr CP (1996) Two-stage regulation of an anti-sigma factor determines developmental fate during bacterial endospore formation. Mol Microbiol 21: 913-924
27. Kenney TJ, Moran Jr CP (1987) Organization and regulation of an operon that encodes a sporulation-essential sigma factor in Bacillus subtilis. J Bacteriol 169: 3329-3339
28. Koch AL, Burdett ID (1986) Biophysics of pole formation of Gram-positive rods. J Gen Microbiol 132 (Part 12): 3451-3457
29. Levin PA, Losick R (1994) Characterization of a cell division gene from Bacillus subtilis that is required for vegetative and sporulation septum formation. J Bacteriol 176: 1451-1459
30. Londono-Vallejo JA, Frehel C, Stragier P (1997) SpoIIQ, a forespore-expressed gene required for engulfment in Bacillus subtilis. Mol Microbiol 24: 29-39
31. Lopez-Diaz I, Clarke S, Mandelstam J (1986) spolID operon of Bacillus subtilis: cloning and sequence. J Gen Microbiol 132 (Part 2): 341-354
32. Lutkenhaus J (2002) Unexpected twist to the Z ring. Dev Cell 2: 519-521
33. Margolin W (2002) Bacterial sporulation: FtsZ rings do the twist. Curr Biol 12: R391-R392
34. Marston AL, Errington J (1999) Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol 33: 84-96
35. Merad T, Archibald AR, Hancock IC, Harwood CR, Hobot JA (1989) Cell wall assembly in Bacillus subtilis: visualization of old and new wall material by electron microscopic examination of samples stained selectively for teichoic acid and teichuronic acid. J Gen Microbiol 135 (Part 3): 645-655
36. Mobley HL, Koch AL, Doyle RJ, Streips UN (1984) Insertion and fate of the cell wall in Bacillus subtilis. J Bacteriol 158: 169-179
37. Murakami T, Haga K, Takeuchi M, Sato T (2002) Analysis of the Bacillus subtilis spoIIIJ gene and its paralogue gene, yqjG. J Bacteriol 184: 1998-2004
38. Oke V, Losick R (1993) Multilevel regulation of the sporulation transcription factor sigma K in Bacillus subtilis. J Bacteriol 175: 7341-7347
39. Perez AR, Abanes-De Mello A, Pogliano K (2000) SpoIIB localizes to active sites of septal biogenesis and spatially regulates septal thinning during engulfment in Bacillus subtilis. J Bacteriol 182: 1096-1108
40. Pichoff S, Lutkenhaus J (2001) Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J Bacteriol 183: 6630-6635
41. Pogliano J, Osborne N, Sharp MD, Abanes-De Mello A, Perez A, Sun YL, Pogliano K (1999) A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol Microbiol 31: 1149-1159
42. Pogliano J, Sharp MD, Pogliano K (2002) Partitioning of chromosomal DNA during establishment of cellular asymmetry in Bacillus subtilis. J Bacteriol 184: 1743-1749
43. Pogliano K, Harry E, Losick R (1995) Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol Microbiol 18: 459-470
44. Pogliano K, Hofmeister AE, Losick R (1997) 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: 3331-3341
45. Rudner DZ, Losick R (2002) A sporulation membrane protein tethers the pro-sigmaK processing enzyme to its inhibitor and dictates its subcellular localization. Genes Dev 16: 1007-1018
46. Rudner DZ, Pan Q, Losick RM (2002) Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc Natl Acad Sci USA 99: 8701-8706
47. Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria [see comments]. Nature 406: 637-641
48. Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G, van der Does C, Driessen AJ, Oudega B, Luirink J (2000) YidC, the Escherichia coli homologue of mitochondrial Oxalp, is a component of the Sec translocase. EMBO J 19: 542-549
49. Serrano M, Corte L, Opdyke J, Moran Jr CP, Henriques AO (2003) Expression of spolllJ in the prespore is sufficient for activation of sigma G and for sporulation in Bacillus subtilis. J Bacteriol 185: 3905-3917
50. Sharp MD, Pogliano K (1999) An in vivo membrane fusion assay implicates SpolIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc Natl Acad Sci USA 96: 14553-14558
51. Sharp MD, Pogliano K (2002) Role of cell-specific SpoIIIE in polarity of DNA transfer. Science 295: 137-139
52. Smith K, Bayer ME, Youngman P (1993) Physical and functional characterization of the Bacillus subtilis spoIIM gene. J Bacteriol 175: 3607-3617
53. Sterlini JM, Mandelstam J (1969) Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance. Biochem J 113: 29-37
54. Stragier P, Losick R (1996) Molecular genetics of sporulation in Bacillus subtilis. Annu Rev Genet 30: 241-297
55. Sun YL, Sharp MD, Pogliano K (2000) A dispensable role for forespore-specific gene expression in engulfment of the forespore during sporulation of Bacillus subtilis. J Bacteriol 182: 2919-2927
56. Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850
57. Youngman P, Perkins JB, Losick R (1984) A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions. Mol Gen Genet 195: 424-433