Evaluation of the Kinetic Properties of the Sporulation Protein SpoIIE of Bacillus subtilis by Inclusion in a Model Membrane

Journal of Bacteriology

Volumn 186, Issue 10, 2004, Pages 3195-3201

  Searls, Tim ^a   Chen, Xingyong ^b   Allen, Stephanie ^b   Yudkin, Michael D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPID; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2C; PROTEIN; PROTEIN SPOIIE; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL MEMBRANE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VITRO STUDY; LIPID BILAYER; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SPOROGENESIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; KINETICS; LIPID BILAYERS; MICROSCOPY, ATOMIC FORCE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 2342498650     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.10.3195-3201.2004     Document Type: Article

References (71)

1. Adler, E., A. Donella-Deana, F. Arigoni, L. A. Pinna, and P. Stragier. 1997. Structural relationship between a bacterial developmental protein and eukaryotic PP2C protein phosphatases. Mol. Microbiol. 23:57-62.
2. Allen, S., M. C. Davies, C. J. Roberts, S. J. B. Tendler, and P. M. Williams. 1997. Atomic force microscopy in analytical biotechnology. Trends Biotechnol. 15:101-105.
3. Alper, S., L. Duncan, and R. Losick. 1994. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell 77:195-205.
4. F during sporulation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 93: 3238-3242.
5. Arigoni, F., A. M. Guerout-Fleury, I. Barak, and P. Stragier. 1999. The SpoIIE phosphatase, the sporulation septum and the establishment of fore-spore-specific transcription in Bacillus subtilis: a reassessment. Mol. Microbiol. 31:1407-1415.
6. Arigoni, F., K. Pogliano, C. D. Webb, P. Stragier, and R. Losick. 1995. Localization of protein implicated in establishment of cell type to sites of asymmetric division. Science 270:637-640.
7. Aubry, L., and R. A. Firtel. 1998. Spalten, a protein containing Ga-protein-like and PP2C domains, is essential for cell-type differentiation in Dictyostelium. Genes Dev. 12:1525-1538.
8. Barak, I., J. Behari, G. Olmedo, P. Guzman, D. P. Brown, E. Castro, D. Walker, J. Westpheling, and P. Youngman. 1996. Structure and function of the Bacillus SpoIIE protein and its localization to sites of sporulation septum assembly. Mol. Microbiol. 19:1047-1060.
9. Barak, I., and P. Youngman. 1996. SpoIIE mutants of Bacillus subtilis comprise two distinct phenotypic classes consistent with a dual functional role for the SpoIIE protein. J. Bacteriol. 178:4984-4989.
10. Beall, B., and J. Lutkenhaus. 1991. FtsZ in Bacillus subtilis is required for vegetative septation and for asymmetric septation during sporulation. Genes Dev. 5:447-455.
11. Ben-Yehuda, S., and R. Losick. 2002. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109: 257-266.
12. Bonomi, F., and D. M. Kurtz, Jr. 1984. Chromatographic separation of extruded iron-sulphur cores from the apoproteins of Clostridium pasteurianum and spinach ferredoxins in aqueous Triton X-100/urea. Anal. Biochem. 142:226-231.
13. Daniel, R. A., E. J. Harry, V. L. Katis, R. G. Wake, and J. Errington. 1998. Characterization of the essential cell division gene FtsL (yllD) of Bacillus subtilis and its role in assembly of the division apparatus. Mol. Microbiol. 29:593-604.
14. Das, A. K., N. R. Helps, P. T. W. Cohen, and D. Barford. 1996. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0A resolution. EMBO J. 15:6798-6809.
15. DeLain, E., A. Fourcade, J.-C. Poulin, A. Barbin, D. Coulaud, E. LeCam, and E. Paris. 1992. Comparative observations of biological specimens, especially DNA and filamentous actin molecules in atomic force, tunnelling and electron microscopes. Microsc. Microanal. Microstruct. 3:457-470.
16. Diederich, B., J. F. Wilkinson, T. Magnin, M. Najafi, J. Errington, and M. D. Yudkin. 1994. Role of interactions between SpoIIAA and SpoIIAB in regulating cell-specific transcription factor sigma F of Bacillus subtilis. Genes Dev. 8:2653-2663.
17. Duncan, L., S. Alper, F. Arigoni, R. Losick, and P. Stragier. 1995. Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division. Science 279:641-644.
18. F from its anti-sigma factor SpoIIAB. J. Mol. Biol. 260:147-164.
19. F from Bacillus subtilis. Proc. Natl. Acad. Sci. USA 90:2325-2329.
20. Engel, A., Y. Lyubchenko, and D. Muller. 1999. Atomic force microscopy; a powerful tool to observe biomolecules at work. Trends Cell Biol. 9:77-80.
21. Errington, J. 1996. Determination of cell fate in Bacillus subtilis. Trends Genet. 12:313-334.
22. Feucht, A., L. Abbotts, and J. Errington. 2003. The cell differentiation protein SpoIIE contains a regulatory site that controls its phosphatase activity in response to asymmetric septation. Mol. Microbiol. 45:1119-1132.
23. Feucht, A., R. A. Daniel, and J. Errington. 1999. Characterization of a morphological checkpoint coupling cell-specific transcription to septation in Bacillus subtilis. Mol. Microbiol. 33:1015-1026.
24. Feucht, A., T. Magnin, M. D. Yudkin, and J. Errington. 1996. Bifunctional protein required for asymmetric cell division and cell-specific transcription in Bacillus subtilis. Genes Dev. 10:794-803.
25. Gholamhoseinian, A., and P. J. Piggot. 1989. Timing of spoIIE gene expression relative to septum formation during sporulation of Bacillus subtilis. J. Bacteriol. 171:5747-5749.
26. Gregoriadis, G. 1995. Engineering liposomes for drug delivery: progress and problems. Trends Biotechnol. 13:527-537.
27. Gregoriadis, G. 1993. Liposome technology, 2nd ed., vol. I. CRC Press, Inc., Boca Raton, Fla.
28. Hagting, A., J. Knol, B. Hasemeier, M. R. Streutker, G. Fang, B. Poolman, and W. N. Konings. 1997. Amplified expression, purification and functional reconstitution of the dipeptide and tripeptide transport protein of Lactococcus lactis. Eur. J. Biochem. 247:581-587.
29. Hansma, P. K., J. P. Cleveland, M. Radmacher, D. A. Walters, P. Hillner, M. Bezanilla, M. Fritz, D. Vie, and H. G. Hansma. 1994. Tapping mode atomic force microscopy in liquids. Appl. Phys. Lett. 64:1738-1740.
30. F activation in Bacillus subtilis. J. Bacteriol. 185: 1590-1598.
31. Holloway, P. W. 1973. A simple procedure for removal of Triton X-100 from protein samples. Anal. Biochem. 53:304-308.
32. F in prespore engulfment. J. Bacteriol. 173:3159-3169.
33. Kang, C. M., K. Vijay, and C. W. Price. 1998. Serine kinase activity of a Bacillus subtilis switch protein is required to transduce environmental stress signals but not to activate its target PP2C phosphatase. Mol. Microbiol. 30:189-196.
34. F during sporulation in Bacillus subtilis. Genes Dev. 13:1156-1167.
35. Knol, J., K. Sjollema, and B. Poolman. 1998. Detergent-mediated reconstitution of membrane proteins. Biochemistry 37:16410-16415.
36. Knol, J., L. Veenhoff, W.-J. Liang, P. J. F. Henderson, G. Leblanc, and B. Poolman. 1996. Unidirectional reconstitution into detergent-destabilized liposomes of the purified lactose transport system of Streptococcus thermophilus. J. Biol. Chem. 271:15358-15366.
37. Kroos, L., and Y. T. Yu. 2000. Regulation of sigma factor activity during Bacillus subtilis development. Curr. Opin. Microbiol. 3:553-560.
38. Lawson, J. E., S. H. Park, A. R. Mattison, J. Yan, and L. J. Reed. 1997. Cloning, expression, and properties of the regulatory subunit of bovine pyruvate dehydrogenase phosphatase. J. Biol. Chem. 272:31625-31629.
39. LeCam, E., D. Frechon, M. Barray, A. Fourcade, and E. DeLain. 1994. Observing of binding and polymerization of Fur repressor onto operator-containing DNA with electron and atomic force microscopes. Proc. Natl. Acad. Sci. USA 91:11816-11820.
40. Leung, J., M. Biouvier-Durand, P. C. Morris, D. Guerrier, F. Chefdor, and J. Giraudat. 1994. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448-1452.
41. Levin, P. A., and R. Losick. 1994. Characterization of cell division gene from Bacillus subtilis that is required for vegetative and sporulation septum formation. J. Bacteriol. 176:1451-1459.
42. Levin, P. A., and R. Losick. 1996. Transcription factor SpoOA switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes Dev. 10:478-488.
43. Levin, P. A., R. Losick, P. Stragier, and F. Arigoni. 1997. Localization of the sporulation protein SpoIIE in Bacillus subtilis is dependent upon the cell division protein FtsZ. Mol. Microbiol. 25:839-846.
44. Losick, R., and J. Dworkin. 1999. Linking symmetric division to cell fate: teaching an old microbe new tricks. Genes Dev. 13:377-381.
45. Lucet, I., R. Borriss, and M. D. Yudkin. 1999. Purification, kinetic properties, and intracellular concentration of SpoIIE, an integral membrane protein that regulates sporulation in Bacillus subtilis. J. Bacteriol. 181:3242-3245.
46. Lucet, I., A. Feucht, M. D. Yudkin, and J. Errington. 2000. Direct interaction between the cell division protein FtsZ and the cell differentiation protein SpoIIE. EMBO J. 19:1467-1475.
47. F activity in sporulating Bacillus subtilis. J. Bacteriol. 179:3922-3927.
48. Mayer, L. D., M. J. Hope, and P. R. Cullis. 1986. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta 858:161-168.
49. Meijberg, W., and P. J. Booth. 2002. The activation energy for insertion of transmembrane alpha-helices is dependent on membrane composition. J. Mol. Biol. 319:839-853.
50. Meyer, K., M. P. Leube, and E. Grill. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455.
51. Min, K. T., C. M. Hilditch, B. Diederich, J. Errington, and M. D. Yudkin. 1993. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell 74:735-742.
52. F of Bacillus subtilis. J. Bacteriol. 177:2912-2913.
53. Newman, J. D., and A. P. F. Turner. 1994. Biosensors: the analyst's dream? Chem. Ind. 10:374-378.
54. Pan, Q., D. A. Garsin, and R. Losick. 2001. Self-reinforcing activation of a cell-specific transcription factor by proteolysis of an anti-sigma factor in B. subtilis. Mol. Cell 8:873-883.
55. Pan, Q., and R. Losick. 2003. Unique degradation signal for ClpCP in Bacillus subtilis. J. Bacteriol. 185:5275-5278.
56. Partridge, S. R., and J. Errington. 1993. The importance of morphological events and intercellular interactions in the regulation of prespore-specific gene expression during sporulation in Bacillus subtilis. Mol. Microbiol. 8:945-955.
57. Paternostre, M. T., M. Roux, and J. L. Rigaud. 1988. Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. I. Solubilization of large unilamellar liposomes (prepared by reverse-phase evaporation) by Triton X-100, octyl glucoside, and sodium cholate. Biochemistry 27:2668-2677.
58. Piggot, P. J. 1973. Mapping of asporogenous mutations of Bacillus subtilis: a minimum estimate of the number of sporulation operons. J. Bacteriol. 114: 1241-1253.
59. Ren, J., S. Lew, J. Wang, and E. London. 1999. Control of the transmembrane orientation and interhelical interactions within membranes by hydrophobic helix length. Biochemistry 38:5905-5912.
60. Ren, J., S. Lew, Z. Wang, and E. London. 1997. Transmembrane orientation of hydrophobic alpha-helices is regulated both by the relationship of helix length to bilayer thickness and by the cholesterol concentration. Biochemistry 36:10213-10220.
61. Rigaud, J.-L., D. Levy, G. Mosser, and O. Lambert. 1998. Detergent removal by non-polar polystyrene beads. Eur. Biophys. J. 27:305-319.
62. Rigaud, J. L., B. Pitard, and D. Levy. 1995. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins. Biochim. Biophys. Acta 1231:223-246.
63. Rudner, D. Z., and R. Losick. 2001. Morphological coupling in development: lessons from prokaryotes. Dev. Cell 1:733-742.
64. Schabert, F. A., C. Henn, and A. Engel. 1995. Native Escherichia coli OmpF porin surfaces probed by the atomic force microscope. Science 268:92-94.
65. Stone, J. M., M. A. Collinge, R. D. Smith, M. A. Horn, and J. C. Walker. 1994. Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science 266:793-795.
66. Stragier, P., C. Bonamy, and C. Karmazyn-Campelli. 1988. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell 52:697-704.
67. Stragier, P., and R. Losick. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 30:297-341.
68. Taylor, M. A., M. N. Jones, P. M. Vadgama, and S. P. J. Higson. 1997. The effect of lipid bilayer manipulation on the response of the glucose oxidase-liposome electrode. Biosens. Bioelectron. 21:467-477.
69. Weiner, M. C., and S. H. White. 1992. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61:437-447.
70. Wu, L. J., A. Feucht, and J. Errington. 1998. Prespore-specific gene expression in Bacillus subtilis is driven by sequestration of SpoIIE phosphatase to the prespore side of the asymmetric septum. Genes Dev. 12:1371-1380.
71. Yang, X., C. M. Kang, M. S. Brody, and C. W. Price. 1996. Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 10:2265-2275.