Identification of ClpP substrates in Caulobacter crescentus reveals a role for regulated proteolysis in bacterial development

Molecular Microbiology

Volumn 88, Issue 6, 2013, Pages 1083-1092

  Bhat, Nowsheen H ^a   Vass, Robert H ^a   Stoddard, Patrick R ^a   Shin, Dong K ^a   Chien, Peter ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CPDR PROTEIN; CTRA PROTEIN; ENDOPEPTIDASE CLP; ENDOPEPTIDASE CLPX; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TACA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; CAULOBACTER CRESCENTUS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SUBSTRATE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING;

BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL CYCLE; ENDOPEPTIDASE CLP; GENE EXPRESSION REGULATION, BACTERIAL; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CAULOBACTER; CAULOBACTER VIBRIOIDES;

EID: 84879014705     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12241     Document Type: Article

References (42)

1. Abdelhakim, A.H., Oakes, E.C., Sauer, R.T., and Baker, T.A. (2008) Unique contacts direct high-priority recognition of the tetrameric Mu transposase-DNA complex by the AAA+ unfoldase ClpX. Mol Cell 30: 39-50.
2. Abel, S., Chien, P., Wassmann, P., Schirmer, T., Kaever, V., Laub, M.T., etal. (2011) Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 43: 550-560.
3. Biondi, E.G., Reisinger, S.J., Skerker, J.M., Arif, M., Perchuk, B.S., Ryan, K.R., and Laub, M.T. (2006a) Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444: 899-904.
4. Biondi, E.G., Skerker, J.M., Arif, M., Prasol, M.S., Perchuk, B.S., and Laub, M.T. (2006b) A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 59: 386-401.
5. Bissonnette, S.A., Rivera-Rivera, I., Sauer, R.T., and Baker, T.A. (2010) The IbpA and IbpB small heat-shock proteins are substrates of the AAA+ Lon protease. Mol Microbiol 75: 1539-1549.
6. Britos, L., Abeliuk, E., Taverner, T., Lipton, M., McAdams, H., and Shapiro, L. (2011) Regulatory response to carbon starvation in Caulobacter crescentus. PLoS ONE 6: e18179.
7. Camberg, J.L., Hoskins, J.R., and Wickner, S. (2009) ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc Natl Acad Sci USA 106: 10614-10619.
8. Chien, P., Grant, R.A., Sauer, R.T., and Baker, T.A. (2007a) Structure and substrate specificity of an SspB ortholog: design implications for AAA+ adaptors. Structure 15: 1296-1305.
9. Chien, P., Perchuk, B.S., Laub, M.T., Sauer, R.T., and Baker, T.A. (2007b) Direct and adaptor-mediated substrate recognition by an essential AAA+ protease. Proc Natl Acad Sci USA 104: 6590-6595.
10. Curtis, P.D., and Brun, Y.V. (2010) Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol Mol Biol Rev 74: 13-41.
11. Domian, I.J., Quon, K.C., and Shapiro, L. (1997) Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90: 415-424.
12. Domian, I.J., Reisenauer, A., and Shapiro, L. (1999) Feedback control of a master bacterial cell-cycle regulator. Proc Natl Acad Sci USA 96: 6648-6653.
13. Flynn, J.M., Neher, S.B., Kim, Y.I., Sauer, R.T., and Baker, T.A. (2003) Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell 11: 671-683.
14. Gerth, U., Kock, H., Kusters, I., Michalik, S., Switzer, R.L., and Hecker, M. (2008) Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis. J Bacteriol 190: 321-331.
15. Goley, E.D., Toro, E., McAdams, H.H., and Shapiro, L. (2009) Dynamic chromosome organization and protein localization coordinate the regulatory circuitry that drives the bacterial cell cycle. Cold Spring Harb Symp Quant Biol 74: 55-64.
16. Gorbatyuk, B., and Marczynski, G.T. (2005) Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol Microbiol 55: 1233-1245.
17. Gottesman, S., Clark, W.P., de Crecy-Lagard, V., and Maurizi, M.R. (1993) ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J Biol Chem 268: 22618-22626.
18. Grunenfelder, B., Rummel, G., Vohradsky, J., Roder, D., Langen, H., and Jenal, U. (2001) Proteomic analysis of the bacterial cell cycle. Proc Natl Acad Sci USA 98: 4681-4686.
19. Hong, S.J., Lessner, F.H., Mahen, E.M., and Keiler, K.C. (2007) Proteomic identification of tmRNA substrates. Proc Natl Acad Sci USA 104: 17128-17133.
20. Iniesta, A.A., McGrath, P.T., Reisenauer, A., McAdams, H.H., and Shapiro, L. (2006) 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: 10935-10940.
21. Jenal, U., and Fuchs, T. (1998) An essential protease involved in bacterial cell-cycle control. EMBO J 17: 5658-5669.
22. Katayama, Y., Gottesman, S., Pumphrey, J., Rudikoff, S., Clark, W.P., and Maurizi, M.R. (1988) The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J Biol Chem 263: 15226-15236.
23. Kock, H., Gerth, U., and Hecker, M. (2004) The ClpP peptidase is the major determinant of bulk protein turnover in Bacillus subtilis. J Bacteriol 186: 5856-5864.
24. Laub, M.T., McAdams, H.H., Feldblyum, T., Fraser, C.M., and Shapiro, L. (2000) Global analysis of the genetic network controlling a bacterial cell cycle. Science 290: 2144-2148.
25. Lesley, J.A., and Shapiro, L. (2008) SpoT regulates DnaA stability and initiation of DNA replication in carbon-starved Caulobacter crescentus. J Bacteriol 190: 6867-6880.
26. Marques, M.V., Gomes, S.L., and Gober, J.W. (1997) A gene coding for a putative sigma 54 activator is developmentally regulated in Caulobacter crescentus. J Bacteriol 179: 5502-5510.
27. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., etal. (1992) Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360: 597-599.
28. Neher, S.B., Villen, J., Oakes, E.C., Bakalarski, C.E., Sauer, R.T., Gygi, S.P., and Baker, T.A. (2006) Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol Cell 22: 193-204.
29. Osteras, M., Stotz, A., Schmid Nuoffer, S., and Jenal, U. (1999) Identification and transcriptional control of the genes encoding the Caulobacter crescentus ClpXP protease. J Bacteriol 181: 3039-3050.
30. Potocka, I., Thein, M., ØSterås, M., Jenal, U., and Alley, M.R. (2002) Degradation of a Caulobacter soluble cytoplasmic chemoreceptor is ClpX dependent. J Bacteriol 184: 6635-6641.
31. Quon, K.C., Marczynski, G.T., and Shapiro, L. (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84: 83-93.
32. Radhakrishnan, S.K., Thanbichler, M., and Viollier, P.H. (2008) The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev 22: 212-225.
33. Radhakrishnan, S.K., Pritchard, S., and Viollier, P.H. (2010) Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev Cell 18: 90-101.
34. Rood, K.L., Clark, N.E., Stoddard, P.R., Garman, S.C., and Chien, P. (2012) Adaptor-dependent degradation of a cell-cycle regulator uses a unique substrate architecture. Structure 20: 1223-1232.
35. Rosenfeld, N., Elowitz, M.B., and Alon, U. (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323: 785-793.
36. Sauer, R.T., and Baker, T.A. (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80: 587-612.
37. Skerker, J.M., Prasol, M.S., Perchuk, B.S., Biondi, E.G., and Laub, M.T. (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 3: e334.
38. Sommer, J.M., and Newton, A. (1989) Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus. J Bacteriol 171: 392-401.
39. Tsai, J.W., and Alley, M.R. (2001) Proteolysis of the Caulobacter McpA chemoreceptor is cell cycle regulated by a ClpX-dependent pathway. J Bacteriol 183: 5001-5007.
40. Tsokos, C.G., Perchuk, B.S., and Laub, M.T. (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev Cell 20: 329-341.
41. Wang, K.H., Sauer, R.T., and Baker, T.A. (2007) ClpS modulates but is not essential for bacterial N-end rule degradation. Genes Dev 21: 403-408.
42. Wojtyra, U.A., Thibault, G., Tuite, A., and Houry, W.A. (2003) The N-terminal zinc binding domain of ClpX is a dimerization domain that modulates the chaperone function. J Biol Chem 278: 48981-48990.