Bacillus subtilis RapA phosphatase domain interaction with its substrate, phosphorylated Spo0F, and its inhibitor, the PhrA peptide

Journal of Bacteriology

Volumn 194, Issue 6, 2012, Pages 1378-1388

  Diaz, Alejandra R ^a,b,c   Core, Leighton J ^a,d   Jiang, Min ^a   Morelli, Michela ^a   Chiang, Christina H ^a   Szurmant, Hendrik ^a   Perego, Marta ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

^c National University of the South   (Argentina)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; COMA PROTEIN; PENTAPEPTIDE; PHOSPHATASE; PHRA PEPTIDE; RAP PROTEIN; RAPA PROTEIN; SPO0F PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BIOCHEMISTRY; CHIMERA; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPOROGENESIS;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; ENZYME INHIBITORS; GENES, REPORTER; MICROBIAL VIABILITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; SPORES, BACTERIAL; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS; EUKARYOTA; PROKARYOTA;

EID: 84857934007     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06747-11     Document Type: Article

References (43)

1. Anagnostopoulos C, Spizizen J. 1961. Requirements for transformation in Bacillus subtilis. J. Bacteriol. 81:741-746.
2. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD. 2005. Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc. Natl. Acad. Sci. U. S. A. 102:12554 -12559.
3. Baker MD, Neiditch MB. 2011. Structural basis of response regulator inhibition by a bacterial anti-activator protein. PLoS Biol. 9:e1001226.
4. Bongiorni C, Ishikawa S, Stephenson S, Ogasawara N, Perego M. 2005. Synergistic regulation of competence development in Bacillus subtilis by two Rap-Phr systems. J. Bacteriol. 187:4353- 4361.
5. Bongiorni C, Stoessel R, Shoemaker D, Perego M. 2006. Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation. J. Bacteriol. 188:487- 498.
6. Bouillaut L, et al. 2008. Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res. 36:3791-3801.
7. Burbulys D, Trach KA, Hoch JA. 1991. The initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552.
8. Core LJ, Perego M. 2003. TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol. Microbiol. 49:1509 -1522.
9. Cortajarena AL, Kajander T, Pan W, Cocco MJ, Regan L. 2004. Protein design to understand peptide ligand recognition by tetratricopeptide repeat proteins. Protein Eng. Des. Sel. 17:399-409.
10. Cortajarena AL, Wang J, Regan L. 2010. Crystal structure of a designed tetratricopeptide repeat module in complex with its peptide ligand. FEBS J. 277:1058 -1066.
11. D'Andrea LD, Regan L. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28:655- 662.
12. Das AK, Cohen PTW, Barford D. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192-1199.
13. Declerck N, et al. 2007. Structure of PlcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc. Natl. Acad. Sci. U. S. A. 104:18490 -18495.
14. Diaz AR, et al. 2008. Functional role for a conserved aspartate in the Spo0E signature motif involved in the dephosphorylation of the Bacillus subtilis sporulation regulator Spo0A. J. Biol. Chem. 283:2962-2972.
15. Fujita M, Losick R. 2005. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19:2236 -2244.
16. Gatto GJ, Jr, Geisbrecht BV, Gould SJ, Berg JM. 2000. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 7:1091-1095.
17. Horton RM, Cai ZL, Ho SN, Pease LR. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528 -535.
18. Ishikawa S, Core LJ, Perego M. 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.
19. Jaroszewski L, Li Z, Cai XH, Weber C, Godzik A. 2011. FFAS server: novel features and applications. Nucleic Acids Res. 39:W38-W44.
20. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A. 2005. FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33: W284-W288.
21. Jiang M, Grau R, Perego M. 2000. Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J. Bacteriol. 182:303- 310.
22. Jiang M, Shao W, Perego M, Hoch JA. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38:535-542.
23. LeDeaux JR, Yu N, Grossman AD. 1995. Different roles for KinA, KinB and KinC in the initiation of sporulation in Bacillus subtilis. J. Bacteriol. 177:861- 863.
24. Mirouze N, Parashar V, Baker MD, Dubnau DA, Neiditch MB. 2011. An atypical Phr peptide regulates the developmental switch protein RapH. J. Bacteriol. 193:6197- 6206.
25. Ogura M, Shimane K, Asai K, Ogasawara N, Tanaka T. 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.
26. Ohlsen KL, Grimsley JK, Hoch JA. 1994. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc. Natl. Acad. Sci. U. S. A. 91:1756 -1760.
27. Parashar V, Mirouze N, Dubnau DA, Neiditch MB. 2011. Structural basis of response regulator dephosphorylation by Rap phosphatases. PLoS Biol. 9:e1000589.
28. Perego M. 1993. Integrational vectors for genetic manipulation in Bacillus subtilis, p 615-624. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, DC.
29. Perego M. 1997. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc. Natl. Acad. Sci. U. S. A. 94:8612- 8617.
30. Perego M. 2001. A new family of aspartyl-phosphate phosphatases targeting the sporulation transcription factor Spo0A of Bacillus subtilis. Mol. Microbiol. 42:133-144.
31. Perego M, Brannigan JA. 2001. Pentapeptide regulation of aspartylphosphate phosphatases. Peptides 22:1541-1547.
32. Perego M, Glaser P, Hoch JA. 1996. Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis. Mol. Microbiol. 19:1151-1157.
33. Perego M, et al. 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.
34. Perego M, Hoch JA. 1987. Isolation and sequence of the spo0E gene: its role in initiation of sporulation in Bacillus subtilis. Mol. Microbiol. 1:125- 132.
35. Perego M, Hoch JA. 1996. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 93:1549 -1553.
36. Schaeffer P, Millet J, Aubert JP. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. U. S. A. 54:704 -711.
37. Scheufler C, et al. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199 -210.
38. Shi K, et al. 2005. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Proc. Natl. Acad. Sci. U. S. A. 102:18596 -18601.
39. Slamti L, Lereclus D. 2002. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 21: 4550-4559.
40. Smits WK, et al. 2007. Temporal separation of distinct differentiation pathways by a dual specificity Rap-Phr system in Bacillus subtilis. Mol. Microbiol. 65:103-120.
41. Tortosa P, Dubnau D. 1999. Competence for transformation: a matter of taste. Curr. Opin. Microbiol. 2:588 -592.
42. Tzeng Y-L, Feher VA, Cavanagh J, Perego M, Hoch JA. 1998. Characterization of interactions between a two-component response regulator, Spo0F, and its phosphatase, RapB. Biochemistry 37:16538 -16545.
43. Zapf JW, Sen U, Madhusudan Hoch JA, Varughese KI. 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 8:851- 862.