DOI: 10.1128/jb.183.17.5001-5007.2001. Proteolysis of the <i>Caulobacter</i> McpA Chemoreceptor Is Cell Cycle Regulated by a ClpX-Dependent Pathway

Proteolysis of the Caulobacter McpA Chemoreceptor Is Cell Cycle Regulated by a ClpX-Dependent Pathway

10.1128/jb.183.17.5001-5007.2001

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT Proteolysis is involved in cell differentiation and the progression through the cell cycle in Caulobacter crescentus . We have constitutively expressed the transmembrane chemoreceptor McpA from a multicopy plasmid to demonstrate that McpA degradation is modulated during the cell cycle. The level of McpA protein starts to decrease only when the swarmer cells differentiate into stalked cells. The reduction in McpA protein levels is maintained until the stalked cells develop into predivisional cells, at which point the level returns to that observed in swarmer cells. The cell-cycle-regulated degradation of McpA does not require the last 12 C-terminal amino acids, but it does require three amino acids (AAL) located 15 residues away from the C terminus. The ClpXP protease is essential in C . crescentus for viability, and thus, we tested McpA degradation in xylose conditional mutants. The effect on McpA degradation occurred within two generations from the start of ClpX depletion. The conditional mutants' growth rate was only slightly affected, suggesting that ClpX is directly involved in McpA proteolysis.

Bibliography

Tsai, J.-W., & Alley, M. R. K. (2001). Proteolysis of the Caulobacter McpA Chemoreceptor Is Cell Cycle Regulated by a ClpX-Dependent Pathway. Journal of Bacteriology, 183(17), 5001â5007.

Authors 2

Jeng-Wen Tsai (first)
M. R. K. Alley (additional)

References 35 Referenced 82

10.1093/genetics/129.2.333
10.1101/gad.6.5.825
Alley M. R. K. Maddock J. R. Shapiro L. Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis.Science259199317541757 (10.1126/science.8456303) / Science / Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis by Alley M. R. K. (1993)
Barnakov A. N. Barnakova L. A. Hazelbauer G. L. Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation.Proc. Natl. Acad. Sci. USA9619991066710672 (10.1073/pnas.96.19.10667) / Proc. Natl. Acad. Sci. USA / Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation by Barnakov A. N. (1999)
Becker G. Klauck E. Hengge-Aronis R. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS.Proc. Natl. Acad. Sci. USA96199964396444 (10.1073/pnas.96.11.6439) / Proc. Natl. Acad. Sci. USA / Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS by Becker G. (1999)
Djordjevic S. Stock A. M. Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine.Structure51997545558 (10.1016/S0969-2126(97)00210-4) / Structure / Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine by Djordjevic S. (1997)
Domian I. J. Quon K. C. Shapiro L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle.Cell901997415424 (10.1016/S0092-8674(00)80502-4) / Cell / Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle by Domian I. J. (1997)
10.1016/0076-6879(91)04019-K
Gonciarz-Swiatek M. Wawrzynow A. Um S. J. Learn B. A. McMacken R. Kelley W. L. Georgopoulos C. Sliekers O. Zylicz M. Recognition, targeting, and hydrolysis of the λO replication protein by the ClpP/ClpX protease.J. Biol. Chem.27419991399914005 (10.1074/jbc.274.20.13999) / J. Biol. Chem. / Recognition, targeting, and hydrolysis of the λO replication protein by the ClpP/ClpX protease by Gonciarz-Swiatek M. (1999)
Gottesman S. Roche E. Zhou Y. Sauer R. T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system.Genes Dev.12199813381347 (10.1101/gad.12.9.1338) / Genes Dev. / The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system by Gottesman S. (1998)
Grünenfelder B. Rummel G. Vohradsky J. Roder D. Langen H. Jenal U. Proteomic analysis of the bacterial cell cycle.Proc. Natl. Acad. Sci. USA98200146814686 (10.1073/pnas.071538098) / Proc. Natl. Acad. Sci. USA / Proteomic analysis of the bacterial cell cycle by Grünenfelder B. (2001)
Herman C. Thévenet D. Bouloc P. Walker G. C. D'Ari R. Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH).Genes Dev.12199813481355 (10.1101/gad.12.9.1348) / Genes Dev. / Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH) by Herman C. (1998)
Jenal U. Fuchs T. An essential protease involved in bacterial cell-cycle control.EMBO J.17199856585669 (10.1093/emboj/17.19.5658) / EMBO J. / An essential protease involved in bacterial cell-cycle control by Jenal U. (1998)
10.1002/j.1460-2075.1996.tb00597.x
10.1128/jb.179.23.7219-7225.1997
Kelly A. J. Sackett M. J. Din N. Quardokus E. Brun Y. V. Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter.Genes Dev.121998880893 (10.1101/gad.12.6.880) / Genes Dev. / Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter by Kelly A. J. (1998)
Kim K. K. Yokota H. Kim S. H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor.Nature4001999787792 (10.1038/23512) / Nature / Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor by Kim K. K. (1999)
Le Moual H. Koshland D. E. Jr. Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis.J. Mol. Biol.2611996568585 (10.1006/jmbi.1996.0483) / J. Mol. Biol. / Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis by Le Moual H. (1996)
Levchenko I. Seidel M. Sauer R. T. Baker T. A. A specificity-enhancing factor for the ClpXP degradation machine.Science289200023542356 (10.1126/science.289.5488.2354) / Science / A specificity-enhancing factor for the ClpXP degradation machine by Levchenko I. (2000)
Levchenko I. Smith C. K. Walsh N. P. Sauer R. T. Baker T. A. PDZ-like domains mediate binding specificity in the Clp/Hsp100 family of chaperones and protease regulatory subunits.Cell911997939947 (10.1016/S0092-8674(00)80485-7) / Cell / PDZ-like domains mediate binding specificity in the Clp/Hsp100 family of chaperones and protease regulatory subunits by Levchenko I. (1997)
10.1128/jb.179.3.592-600.1997
10.1002/j.1460-2075.1996.tb00475.x
Nierman W. C. Feldblyum T. V. Laub M. T. Paulsen I. T. Nelson K. E. Eisen J. Heidelberg J. F. Alley M. R. K. Ohta N. Maddock J. R. Potocka I. Nelson W. C. Newton A. Stephens C. Phadke N. D. Ely B. DeBoy R. T. Dodson R. J. Durkin A. S. Gwinn M. L. Haft D. H. Kolonay J. F. Smit J. Craven M. B. Khouri H. Shetty J. Berry K. Utterback T. Tran K. Wolf A. Vamathevan J. Ermolaeva M. White O. Salzberg S. L. Venter J. C. Shapiro L. Fraser C. M. Complete genome sequence of Caulobacter crescentus.Proc. Natl. Acad. Sci. USA98200141364141 (10.1073/pnas.061029298) / Proc. Natl. Acad. Sci. USA / Complete genome sequence of Caulobacter crescentus by Nierman W. C. (2001)
10.1128/JB.180.7.1862-1868.1998
Quardokus E. Din N. Brun Y. V. Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter.Proc. Natl. Acad. Sci. USA93199663146319 (10.1073/pnas.93.13.6314) / Proc. Natl. Acad. Sci. USA / Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter by Quardokus E. (1996)
Quon K. C. Yang B. Domian I. J. Shapiro L. 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. USA951998120125 (10.1073/pnas.95.1.120) / Proc. Natl. Acad. Sci. USA / Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin by Quon K. C. (1998)
10.1128/jb.178.2.470-476.1996
Sharma S. B. Signer E. R. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA.Genes Dev.41990344356 (10.1101/gad.4.3.344) / Genes Dev. / Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA by Sharma S. B. (1990)
Shaw P. Gomes S. L. Sweeney K. Ely B. Shapiro L. Methylation involved in chemotaxis is regulated during Caulobacter differentiation.Proc. Natl. Acad. Sci. USA80198352615265 (10.1073/pnas.80.17.5262) / Proc. Natl. Acad. Sci. USA / Methylation involved in chemotaxis is regulated during Caulobacter differentiation by Shaw P. (1983)
Silber K. R. Keiler K. C. Sauer R. T. Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini.Proc. Natl. Acad. Sci. USA891992295299 (10.1073/pnas.89.1.295) / Proc. Natl. Acad. Sci. USA / Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini by Silber K. R. (1992)
Simon R. Priefer U. Puhler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria.Bio/Technology11983784791 (10.1038/nbt1183-784) / Bio/Technology / A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria by Simon R. (1983)
10.1128/JB.182.2.504-507.2000
10.1016/S0021-9258(18)41572-4
Wright R. Stephens C. Zweiger G. Shapiro L. Alley M. R. K. Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation.Genes Dev.10199615321542 (10.1101/gad.10.12.1532) / Genes Dev. / Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation by Wright R. (1996)
Wu J. Li J. Li G. Long D. G. Weis R. M. The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation.Biochemistry35199649844993 (10.1021/bi9530189) / Biochemistry / The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation by Wu J. (1996)

Dates

Type	When
Created	23 years ago (July 27, 2002, 6:01 a.m.)
Deposited	4 years ago (July 29, 2021, 1:59 p.m.)
Indexed	1 year ago (Aug. 3, 2024, 4:17 p.m.)
Issued	23 years, 11 months ago (Sept. 1, 2001)
Published	23 years, 11 months ago (Sept. 1, 2001)
Published Print	23 years, 11 months ago (Sept. 1, 2001)

Funders 0

None

BibTeX

@article{Tsai_2001, title={Proteolysis of the Caulobacter McpA Chemoreceptor Is Cell Cycle Regulated by a ClpX-Dependent Pathway}, volume={183}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.183.17.5001-5007.2001}, DOI={10.1128/jb.183.17.5001-5007.2001}, number={17}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Tsai, Jeng-Wen and Alley, M. R. K.}, year={2001}, month=sep, pages={5001–5007} }

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      "article-title": "Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis",
      "volume": "259",
      "author": "Alley M. R. K.",
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      "unstructured": "Alley M. R. K. Maddock J. R. Shapiro L. Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis.Science259199317541757",
      "journal-title": "Science"
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      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "10667",
      "DOI": "10.1073/pnas.96.19.10667",
      "article-title": "Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation",
      "volume": "96",
      "author": "Barnakov A. N.",
      "year": "1999",
      "unstructured": "Barnakov A. N. Barnakova L. A. Hazelbauer G. L. Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation.Proc. Natl. Acad. Sci. USA9619991066710672",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "6439",
      "DOI": "10.1073/pnas.96.11.6439",
      "article-title": "Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS",
      "volume": "96",
      "author": "Becker G.",
      "year": "1999",
      "unstructured": "Becker G. Klauck E. Hengge-Aronis R. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS.Proc. Natl. Acad. Sci. USA96199964396444",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "545",
      "DOI": "10.1016/S0969-2126(97)00210-4",
      "article-title": "Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine",
      "volume": "5",
      "author": "Djordjevic S.",
      "year": "1997",
      "unstructured": "Djordjevic S. Stock A. M. Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine.Structure51997545558",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "415",
      "DOI": "10.1016/S0092-8674(00)80502-4",
      "article-title": "Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle",
      "volume": "90",
      "author": "Domian I. J.",
      "year": "1997",
      "unstructured": "Domian I. J. Quon K. C. Shapiro L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle.Cell901997415424",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
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      "first-page": "13999",
      "DOI": "10.1074/jbc.274.20.13999",
      "article-title": "Recognition, targeting, and hydrolysis of the \u03bbO replication protein by the ClpP/ClpX protease",
      "volume": "274",
      "author": "Gonciarz-Swiatek M.",
      "year": "1999",
      "unstructured": "Gonciarz-Swiatek M. Wawrzynow A. Um S. J. Learn B. A. McMacken R. Kelley W. L. Georgopoulos C. Sliekers O. Zylicz M. Recognition, targeting, and hydrolysis of the \u03bbO replication protein by the ClpP/ClpX protease.J. Biol. Chem.27419991399914005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1101/gad.12.9.1338",
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      "volume": "12",
      "author": "Gottesman S.",
      "year": "1998",
      "unstructured": "Gottesman S. Roche E. Zhou Y. Sauer R. T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system.Genes Dev.12199813381347",
      "journal-title": "Genes Dev."
    },
    {
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      "first-page": "4681",
      "DOI": "10.1073/pnas.071538098",
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      "volume": "98",
      "author": "Gr\u00fcnenfelder B.",
      "year": "2001",
      "unstructured": "Gr\u00fcnenfelder B. Rummel G. Vohradsky J. Roder D. Langen H. Jenal U. Proteomic analysis of the bacterial cell cycle.Proc. Natl. Acad. Sci. USA98200146814686",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
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      "volume": "12",
      "author": "Herman C.",
      "year": "1998",
      "unstructured": "Herman C. Th\u00e9venet D. Bouloc P. Walker G. C. D'Ari R. Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH).Genes Dev.12199813481355",
      "journal-title": "Genes Dev."
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      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "5658",
      "DOI": "10.1093/emboj/17.19.5658",
      "article-title": "An essential protease involved in bacterial cell-cycle control",
      "volume": "17",
      "author": "Jenal U.",
      "year": "1998",
      "unstructured": "Jenal U. Fuchs T. An essential protease involved in bacterial cell-cycle control.EMBO J.17199856585669",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1996.tb00597.x"
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      "volume": "12",
      "author": "Kelly A. J.",
      "year": "1998",
      "unstructured": "Kelly A. J. Sackett M. J. Din N. Quardokus E. Brun Y. V. Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter.Genes Dev.121998880893",
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    },
    {
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      "first-page": "787",
      "DOI": "10.1038/23512",
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      "volume": "400",
      "author": "Kim K. K.",
      "year": "1999",
      "unstructured": "Kim K. K. Yokota H. Kim S. H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor.Nature4001999787792",
      "journal-title": "Nature"
    },
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      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "568",
      "DOI": "10.1006/jmbi.1996.0483",
      "article-title": "Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis",
      "volume": "261",
      "author": "Le Moual H.",
      "year": "1996",
      "unstructured": "Le Moual H. Koshland D. E. Jr. Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis.J. Mol. Biol.2611996568585",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "2354",
      "DOI": "10.1126/science.289.5488.2354",
      "article-title": "A specificity-enhancing factor for the ClpXP degradation machine",
      "volume": "289",
      "author": "Levchenko I.",
      "year": "2000",
      "unstructured": "Levchenko I. Seidel M. Sauer R. T. Baker T. A. A specificity-enhancing factor for the ClpXP degradation machine.Science289200023542356",
      "journal-title": "Science"
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