Mutations that Alter RcdA Surface Residues Decouple Protein Localization and CtrA Proteolysis in Caulobacter crescentus

Journal of Molecular Biology

Volumn 394, Issue 1, 2009, Pages 46-60

  Taylor, James A ^a   Wilbur, Jeremy D ^b   Smith, Stephen C ^a   Ryan, Kathleen R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Caulobacter; cell cycle; ClpXP; protein localization; proteolysis

Indexed keywords

ESSENTIAL RESPONSE REGULATOR PROTEIN; PEPTIDE; PROTEIN; RCDA PROTEIN; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CAULOBACTER CRESCENTUS; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA REPLICATION; ENZYME SUBSTRATE; EPISTASIS; IN VITRO STUDY; IN VIVO STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN VARIANT;

CAULOBACTER; CAULOBACTER VIBRIOIDES;

AMINO ACIDS; BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL POLARITY; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; G1 PHASE; HALF-LIFE; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; S PHASE; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PROPERTIES; TRANSCRIPTION FACTORS;

EID: 70350196362     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.08.076     Document Type: Article

References (53)

1. Collier J., and Shapiro L. Spatial complexity and control of a bacterial cell cycle. Curr. Opin. Biotechnol. 18 (2007) 333-340
2. Quon K.C., Marczynski G.T., and Shapiro L. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84 (1996) 83-93
3. Domian I.J., Quon K.C., and Shapiro L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90 (1997) 415-424
4. Laub M.T., Chen S.L., Shapiro L., and McAdams H.H. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc. Natl Acad. Sci. USA 99 (2002) 4632-4637
5. Quon K.C., Yang B., Domian I.J., Shapiro L., and Marczynski G.T. Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc. Natl Acad. Sci. USA 95 (1998) 120-125
6. Jenal U., and Fuchs T. An essential protease involved in bacterial cell-cycle control. EMBO J. 17 (1998) 5658-5669
7. Licht S., and Lee I. Resolving individual steps in the operation of ATP-dependent proteolytic molecular machines: from conformational changes to substrate translocation and processivity. Biochemistry 47 (2008) 3595-3605
8. Biondi E.G., Reisinger S.J., Skerker J.M., Arif M., Perchuk B.S., Ryan K.R., and Laub M.T. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444 (2006) 899-904
9. Iniesta A.A., McGrath P.T., Reisenauer A., McAdams H.H., and Shapiro L. A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc. Natl Acad. Sci. USA 103 (2006) 10935-10940
10. McGrath P.T., Iniesta A.A., Ryan K.R., Shapiro L., and McAdams H.H. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124 (2006) 535-547
11. Kainth P., and Gupta R.S. Signature proteins that are distinctive of alpha proteobacteria. BMC Genomics 6 (2005) 94
12. Ryan K.R., Judd E.M., and Shapiro L. The CtrA response regulator essential for Caulobacter crescentus cell-cycle progression requires a bipartite degradation signal for temporally controlled proteolysis. J. Mol. Biol. 324 (2002) 443-455
13. Ryan K.R., Huntwork S., and Shapiro L. Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis. Proc. Natl Acad. Sci. USA 101 (2004) 7415-7420
14. Iniesta A.A., and Shapiro L. A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade. Proc. Natl Acad. Sci. USA 105 (2008) 16602-16607
15. Duerig A., Abel S., Folcher M., Nicollier M., Schwede T., Amiot N., et al. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23 (2009) 93-104
16. Jenal U., and Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40 (2006) 385-407
17. Ades S.E. Proteolysis: adaptor, adaptor, catch me a catch. Curr. Biol. 12 (2004) R924-926
18. Keiler K.C., Waller P.R., and Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271 (1996) 990-993
19. Gottesman S., Roche E., Zhou Y., and Sauer R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12 (1998) 1338-1347
20. Levchenko I., Seidel M., Sauer R.T., and Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 289 (2000) 2354-2356
21. Wah D.A., Levchenko I., Baker T.A., and Sauer R.T. Characterization of a specificity factor for an AAA+ ATPase: assembly of SspB dimers with ssrA-tagged proteins and the ClpX hexamer. Chem. Biol. 9 (2002) 1237-1245
22. Chien P., Perchuk B.S., Laub M.T., Sauer R.T., and Baker T.A. Direct and adaptor-mediated substrate recognition by an essential AAA+ protease. Proc. Natl Acad. Sci. USA 104 (2007) 6590-6595
23. Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J., Evans P.R., and McMahon H.T. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303 (2004) 495-499
24. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2256-2268
25. Meisenzahl A.C., Shapiro L., and Jenal U. Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus. J. Bacteriol. 179 (1997) 592-600
26. Gruber J., Zawaira A., Saunders R., Barrett C.P., and Noble M.E. Computational analyses of he surface properties of protein-protein interfaces. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 (2007) 50-57
27. Laub M.T., and Goulian M. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41 (2007) 121-145
28. Viollier P.H., Sternheim N., and Shapiro L. Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins. Proc. Natl Acad. Sci. USA 99 (2002) 13831-13836
29. Hinz A.J., Larson D.E., Smith C.S., and Brun Y.V. The Caulobacter crescentus polar organelle development protein PodJ is differentially localized and is required for polar targeting of the PleC development regulator. Mol. Microbiol. 47 (2003) 929-941
30. Osteras M., Stotz A., Schmid Nuoffer S., and Jenal U. Identification and transcriptional control of the genes encoding the Caulobacter crescentus ClpXP protease. J. Bacteriol. 181 (1999) 3039-3050
31. Judd E.M., Ryan K.R., Moerner W.E., Shapiro L., and McAdams H.H. Fluorescence bleaching reveals asymmetric compartment formation prior to cell division in Caulobacter. Proc. Natl Acad. Sci. USA 100 (2003) 8235-8240
32. Farrell C.M., Grossman A.D., and Sauer R.T. Cytoplasmic degradation of ssrA-tagged proteins. Mol. Microbiol. 57 (2005) 1750-1761
33. Lies M., and Maurizi M.R. Turnover of endogenous SsrA-tagged proteins mediated by ATP-dependent proteases in Escherichia coli. J. Biol. Chem. 283 (2008) 22918-22929
34. Moore S.D., and Sauer R.T. Ribosome rescue: tmRNA tagging activity and capacity in Escherichia coli. Mol. Microbiol. 58 (2005) 456-466
35. Hong S.-J., Lessner F.H., Mahen E.M., and Keiler K.C. Proteomic identification of tmRNA substrates. Proc. Natl Acad. Sci. USA 104 (2007) 17128-17133
36. Keiler K.C., and Shapiro L. tmRNA is required for correct timing of DNA replication in Caulobacter crescentus. J. Bacteriol. 185 (2003) 573-580
37. Wah D.A., Levchenko I., Rieckhof G.E., Bolon D.N., Baker T.A., and Sauer R.T. Flexible linkers leash the substrate binding domain of SspB to a peptide module that stabilizes delivery complexes with the AAA+ ClpXP protease. Mol. Cell 12 (2003) 355-363
38. Dougan D.A., Weber-Ban E., and Bukau B. Targeted delivery of an ssrA-tagged substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol. Cell 12 (2003) 373-380
39. Levchenko I., Grant R.A., Wah D.A., Sauer R.T., and Baker T.A. Structure of a delivery protein for an AAA+ protease in complex with a peptide degradation tag. Mol. Cell 12 (2003) 365-372
40. Flynn J.M., Neher S.B., Kim Y.I., Sauer R.T., and Baker T.A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 11 (2003) 671-683
41. Dougan D.A., Reid B.G., Horwich A.L., and Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 9 (2002) 673-683
42. Crymes Jr. W.B., Zhang D., and Ely B. Regulation of podJ expression during the Caulobacter crescentus cell cycle. J. Bacteriol. 181 (1999) 3967-3973
43. Laub M.T., McAdams H.H., Feldblyum T., Fraser C.M., and Shapiro L. Global analysis of the genetic network controlling a bacterial cell cycle. Science 290 (2000) 2144-2148
44. Ely B. Genetics of Caulobacter crescentus. Methods Enzymol. 204 (1991) 372-384
45. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., and Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229 (1993) 105-124
46. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
47. Sheldrick G.M. A short history of SHELX. Acta Crystallogr., Sect. A: Found. Crystallogr. 64 (2008) 112-122
48. McCoy A.J. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 (2007) 32-41
49. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
50. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
51. Reisinger S.J., Huntwork S., Viollier P.H., and Ryan K.R. DivL performs critical cell cycle functions in Caulobacter crescentus independent of kinase activity. J. Bacteriol. 189 (2007) 8308-8320
52. Alley M.R., Maddock J.R., and Shapiro L. Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis. Science 259 (1993) 1754-1757
53. Sciochetti S.A., Ohta N., and Newton A. The role of polar localization in the function of an essential Caulobacter crescentus tyrosine kinase. Mol. Microbiol. 56 (2005) 1467-1480