Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation

Journal of Bacteriology

Volumn 188, Issue 2, 2006, Pages 487-498

  Bongiorni, Cristina ^a   Stoessel, Ricarda ^a   Shoemaker, Dorinda ^a   Perego, Marta ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PENTAPEPTIDE; PHOSPHATASE; PROTEIN SPOOF; RAP PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL CHROMOSOME; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; DEPHOSPHORYLATION; ENVIRONMENTAL FACTOR; GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; PXO1 GENE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPOROGENESIS;

AMINO ACID SEQUENCE; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; PLASMIDS; SEQUENCE ALIGNMENT; SPORES, BACTERIAL; VIRULENCE;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

EID: 30744446776     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.2.487-498.2006     Document Type: Article

References (60)

1. Anagnostopoulos, C., and J. Spizizen. 1961. Requirements for transformation in Bacillus subtilis. J. Bacteriol. 81:741-746.
2. Arantes, O., and D. Lereclus. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119.
3. Aronson, A. I., C. Bell, and B. Fulroth. 2005. Plasmid-encoded regulator of extracellular proteases in Bacillus anthracis. J. Bacteriol. 187:3133-3138.
4. Auchtung, J. M., C. A. Lee, R. E. Monson, A. P. Lehman, and A. D. Grossman. 2005. Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc. Natl. Acad. Sci. USA 102:12554-12559.
5. Bongiorni, C., S. Ishikawa, S. Stephenson, N. Ogasawara, and M. Perego. 2005. Synergistic regulation of competence development in Bacillus subtilis by two Rap-Phr systems. J. Bacteriol. 187:4353-4361.
6. Brunsing, R. L., C. La Clair, S. Tang, C. Chiang, L. E. Hancock, M. Perego, and J. A. Hoch. 2005. Characterization of sporulation histidine kinases of Bacillus anthracis. J. Bacteriol. 187:6972-6981.
7. Burbulys, D., K. A. Trach, and J. A. Hoch. 1991. The initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552.
8. Carter, H. L., K. M. Tatti, and C. P. Moran. 1990. Cloning of a promoter used by sigma H RNA polymerase in Bacillus subtilis. Gene 96:101-105.
9. Dai, Z., J. C. Sirard, M. Mock, and T. M. Koehler. 1995. The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence. Mol. Microbiol. 16:1171-1181.
10. D'Andrea, L. D., and L. Regan. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28:655-662.
11. Das, A. K., P. T. W. Cohen, and D. Barford. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192-1199.
12. Easterday, W. R., M. N. Van Ert, T. S. Simonson, D. M. Wagner, L. J. Kenefic, C. J. Allender, and P. Keim. 2005. Use of single nucleotide polymorphisms in the plcR gene for specific identification of Bacillus anthracis. J. Clin. Microbiol. 43:1995-1997.
13. Ferrari, E., S. M. H. Howard, and J. A. Hoch. 1985. Effect of sporulation mutations on subtilisin expression, assayed using a subtilisin-β- galactosidase gene fusion, p. 180-184. In J. A. Hoch and P. Setlow (ed.), Molecular biology of microbial differentiation. American Society for Microbiology, Washington, D.C.
14. Groves, M. R., and D. Barford. 1999. Topological characteristics of helical repeat proteins. Curr. Opin. Struct. Biol. 9:383-389.
15. Guidi-Rontani, C., and M. Mock. 2002. Macrophage interactions. Curr. Top. Microbiol. Immunol. 271:115-141.
16. Hoffmaster, A. R., J. Ravel, D. A. Rasko, G. D. Chapman, M. D. Chute, C. K. Marston, B. K. De, C. T. Sacchi, C. Fitzgerald, L. W. Mayer, M. C. J. Maiden, F. G. Priest, M. Barker, L. Jiang, R. Z. Cer, J. Rilstone, S. N. Peterson, R. S. Weyant, D. R. Galloway, T. D. Read, T. Popovic, and C. M. Fraser. 2004. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc. Natl. Acad. Sci. USA 101:8449-8454.
17. Ishikawa, S., L. Core, and M. Perego. 2002. Biochemical characterization of aspartyl phosphate phosphatase interaction with a phosphorylated response regulator and its inhibition by a pentapeptide. J. Biol. Chem. 277:20483-20489.
18. Jiang, M., R. Grau, and M. Perego. 2000. Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J. Bacteriol. 182:303-310.
19. Jiang, M., W. Shao, M. Perego, and J. A. Hoch. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38:535-542.
20. 2 and a trans-acting element activate transcription from one of two promoters. J. Bacteriol. 176:586-595.
21. Koetje, E. J., A. Hajdo-Milasinovic, R. Kiewiet, S. Bron, and H. Tjalsma. 2003. A plasmid-borne Rap-Phr system of Bacillus subtilis can mediate cell-density controlled production of extracellular proteases. Microbiology 149:19-28.
22. Lazazzera, B. A., J. M. Solomon, and A. D. Grossman. 1997. An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis. Cell 89:917-925.
23. McQuade, R. S., N. Comella, and A. D. Grossman. 2001. Control of a family of phosphatase regulatory genes (phr) by the alternate sigma factor sigma-H of Bacillus subtilis. J. Bacteriol. 183:4905-4909.
24. Meijer, W. J., G. B. Wisman, P. Terpstra, P. B. Thorsted, C. M. Thomas, S. Holsappel, G. Venema, and S. Bron. 1998. Rolling-circle plasmids from Bacillus subtilis: complete nucleotide sequences and analyses of genes of pTA1015, pTA1040, pTA1050 and pTA1060, and comparisons with related plasmids from gram-positive bacteria. FEMS Microbiol. Rev. 21:337-368.
25. Mignot, T., M. Mock, D. Robichon, A. Landier, D. Lereclus, and A. Fouet. 2001. The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis. Mol. Microbiol. 42:1189-1198.
26. Miller, J. H. 1972. Experiments in molecular genetics, p. 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
27. Mock, M., and A. Fouet. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671.
28. Molle, V., M. Fujita, S. T. Jensen, P. Eichenberger, J. E. Gonzalez-Pastor, J. S. Liu, and R. Losick. 2003. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 50:1683-1701.
29. Mueller, J. P., G. Bukusoglu, and A. L. Sonenshein. 1992. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J. Bacteriol. 174:4361-4373.
30. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
31. Ogura, M., K. Shimane, K. Asai, N. Ogasawara, and T. Tanaka. 2003. Binding of response regulator DegU to the aprE promoter is inhibited by RapG, which is counteracted by extracellular PhrG in Bacillus subtilis. Mol. Microbiol. 49:1685-1697.
32. Okinaka, R. T., K. Cloud, O. Hampton, A. R. Hoffmaster, K. K. Hill, P. Keim, T. M. Koehler, G. Lamke, S. Kumano, J. Mahillon, D. Manter, Y. Martinez, D. Ricke, R. Svensson, and P. J. Jackson. 1999. Sequence and organization of pXO1, the large Bacillus anthracis plasmid harboring the anthrax toxin genes. J. Bacteriol. 181:6509-6515.
33. Pannucci, J., R. T. Okinaka, R. Sabin, and C. R. Kuske. 2002. Bacillus anthracis pXO1 plasmid sequence conservation among closely related bacterial species. J. Bacteriol. 184:134-141.
34. Perego, M. 1993. Integrational vectors for genetic manipulation in Bacillus subtilis, p. 615-624. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
35. Perego, M. 1997. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc. Natl. Acad. Sci. USA 94:8612-8617.
36. Perego, M. 2001. A new family of aspartyl-phosphate phosphatases targeting the sporulation transcription factor Spo0A of Bacillus subtilis. Mol. Microbiol. 42:133-144.
37. Perego, M., and J. A. Brannigan. 2001. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22:1541-1547.
38. Perego, M., C. G. Hanstein, K. M. Welsh, T. Djavakhishvili, P. Glaser, and J. A. Hoch. 1994. Multiple protein aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in Bacillus subtilis. Cell 79:1047-1055.
39. Perego, M., and J. A. Hoch. 1996. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 93:1549-1553.
40. Perego, M., and J. A. Hoch. 2002. Two-component systems, phosphorelays and regulation of their activities by phosphatases, p. 473-481. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, D.C.
41. Piggot, P. J., and D. W. Hilbert. 2004. Sporulation of Bacillus subtilis. Curr. Opin. Microbiol. 7:579-586.
42. Poyart, C., and P. Trieu-Cuot. 1997. A broad-host-range mobilizable shuttle vector for the construction of transcriptional fusions to β-galactosidase in Gram-positive bacteria. FEMS Microbiol. Lett. 156:193-198.
43. Saile, E., and T. M. Koehler. 2002. Control of anthrax toxin gene expression by the transition state regulator abrB. J. Bacteriol. 184:370-380.
44. Schaeffer, P., J. Millet, and J. P. Aubert. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. USA 54:704-711.
45. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
46. Scheufler, C., A. Brinker, G. Bourenkov, S. Pegoraro, L. Moroder, H. Bartunik, F. U. Hartl, and I. Moarefi. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199-210.
47. Slamti, L., and D. Lereclus. 2002. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 21:4550-4559.
48. Slamti, L., and D. Lereclus. 2005. Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J. Bacteriol. 187:1182-1187.
49. Stephenson, K., and J. A. Hoch. 2002. Evolution of signaling in the sporulation phosphorelay. Mol. Microbiol. 46:297-304.
50. Stephenson, S., and M. Perego. 2002. Interaction surface of the Spo0A response regulator with the Spo0E phosphatase. Mol. Microbiol. 44:1455-1467.
51. Strauch, M. A. 1993. AbrB, a transition state regulator, p. 757-764. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology and molecular genetics. American Society for Microbiology, Washington, D.C.
52. Strauch, M. A., P. Ballar, A. J. Rowshan, and K. L. Zoller. 2005. The DNA-binding specificity of the Bacillus anthracis AbrB protein. Microbiology 151:1751-1759.
53. Strauch, M. A., V. Webb, G. Spiegelman, and J. A. Hoch. 1990. The Spo0A protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. USA 87:1801-1805.
54. Tzeng, Y.-L., V. A. Feher, J. Cavanagh, M. Perego, and J. A. Hoch. 1998. Characterization of interactions between a two-component response regulator, Spo0F, and its phosphatase, RapB. Biochemistry 37:16538-16545.
55. Tzeng, Y.-L., and J. A. Hoch. 1997. Molecular recognition in signal transduction: the interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. J. Mol. Biol. 272:200-212.
56. Uchida, I., J. M. Hornung, C. B. Thorne, K. R. Klimpel, and S. H. Leppla. 1993. Cloning and characterization of a gene whose product is a trans-activator of anthrax toxin synthesis. J. Bacteriol. 175:5329-5338.
57. van Dijl, J. M., A. Bolhuis, H. Tjalsma, J. D. H. Jongbloed, A. de Jong, and S. Bron. 2002. Protein transport pathways in Bacillus subtilis: a genome-based road map, p. 337-355. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, D.C.
58. Zapf, J., U. Sen, Madhusudan, J. A. Hoch, and K. I. Varughese. 2000. A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure (Cambridge) 8:851-862.
59. Zapf, J. W., J. A. Hoch, and J. M. Whiteley. 1996. A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates. Biochemistry 35:2926-2933.
60. Zhao, H., T. Msadek, J. Zapf, Madhusudan, J. A. Hoch, and K. I. Varughese. 2002. DNA complexed structure of the key transcription factor initiating development in sporulating bacteria. Structure (Cambridge) 10:1041-1050.