Role of Clp protease subunits in degradation of carbon starvation proteins in Escherichia coli
10.1128/jb.175.1.53-63.1993
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

When deprived of a carbon source, Escherichia coli induces the synthesis of a group of carbon starvation proteins. The degradation of proteins labeled during starvation was found to be an energy-dependent process which was inhibited by the addition of KCN and accelerated when cells were resupplied with a carbon source. The degradation of the starvation proteins did not require the ATP-dependent Lon protease or the energy-independent proteases protease I, protease IV, OmpT, and DegP. During starvation, mutants lacking either the ClpA or ClpP subunit of the ATP-dependent Clp protease showed a partial reduction in the degradation of starvation proteins. Strains lacking ClpP failed to increase degradation of starvation proteins when glucose was added to starving cells. The clpP mutants showed a competitive disadvantage compared with wild-type cells when exposed to repeated cycles of carbon starvation and growth. Surprisingly, the glucose-stimulated, ClpP-dependent degradation of starvation proteins did not require either the ClpA or ClpB protein. The patterns of synthesis of starvation proteins were similar in clpP+ and clpP cells. The clpP mutants had reduced rates of degradation of certain starvation proteins in the membrane fraction when a carbon source was resupplied to the starved cells.

Bibliography

Damerau, K., & St John, A. C. (1993). Role of Clp protease subunits in degradation of carbon starvation proteins in Escherichia coli. Journal of Bacteriology, 175(1), 53–63.

Authors 2
  1. K Damerau (first)
  2. A C St John (additional)
References 41 Referenced 53
  1. Alexander D. M. and A. C. St. John. 1992. Identification and characterization of a carbon starvation inducible gene in E. coli abstr. H-131 p. 205. Abstr. 92nd Gen. Meet. Am. Soc. Microbiol. 1992. American Society for Microbiology Washington D.C.
  2. Ames , G. F. - L. , and K. Nikaido . 1976 . Two-dimensional gel electrophoresis of membrane proteins . Biochemistry 15 : 616 - 623 . (10.1021/bi00648a026) / Biochemistry / Two-dimensional gel electrophoresis of membrane proteins by Ames G. F. (1976)
  3. Brunschede , H. , and H. Bremer . 1971 . Synthesis and breakdown of proteins in Escherichia coli during amino acid starvation . J. Mol. Biol. 57 : 35 - 57 . (10.1016/0022-2836(71)90118-5) / J. Mol. Biol. / Synthesis and breakdown of proteins in Escherichia coli during amino acid starvation by Brunschede H. (1971)
  4. Damerau , K. , and A. C. St. John . 1988 . Changes in the synthesis of membrane proteins in response to carbon starvation . J. Cell Biol. 107 : 561a . / J. Cell Biol. / Changes in the synthesis of membrane proteins in response to carbon starvation by Damerau K. (1988)
  5. Goff , S. A. , L. P. Casson , and A. L. Goldberg . 1984 . Heat shock regulatory gene htpR influences rates of protein degradation and expression of the Ion gene in Escherichia coil . Proc. Natl. Acad. Sci. USA 81 : 6647 - 6651 . (10.1073/pnas.81.21.6647) / Proc. Natl. Acad. Sci. USA / Heat shock regulatory gene htpR influences rates of protein degradation and expression of the Ion gene in Escherichia coil by Goff S. A. (1984)
  6. Goff , S. A. , and A. L. Goldberg . 1985 . Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes . Cell 41 : 587 - 595 . (10.1016/S0092-8674(85)80031-3) / Cell / Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes by Goff S. A. (1985)
  7. Goldberg , A. L. , and A. C. St. John . 1976 . Intracellular protein degradation in mammalian and bacterial cells: part 2. Annu . Rev. Biochem. 45 : 747 - 803 . (10.1146/annurev.bi.45.070176.003531) / Rev. Biochem. / Intracellular protein degradation in mammalian and bacterial cells: part 2. Annu by Goldberg A. L. (1976)
  8. Gottesman , S. 1989 . Genetics of proteolysis in Escherichia coli. Annu . Rev. Genet. 23 : 163 - 198 . (10.1146/annurev.ge.23.120189.001115) / Rev. Genet. / Genetics of proteolysis in Escherichia coli. Annu by Gottesman S. (1989)
  9. Gottesman , S. , W. P. Clark , and M. R. Maurizi . 1990 . The ATP-dependent Clp protease of Escherichia coli. Sequence of cipA and identification of a Clp-specific substrate . J. Biol. Chem. 265 : 7886 - 7893 . (10.1016/S0021-9258(19)39014-3) / J. Biol. Chem. / The ATP-dependent Clp protease of Escherichia coli. Sequence of cipA and identification of a Clp-specific substrate by Gottesman S. (1990)
  10. Gottesman , S. , C. Squires , E. Pichersky , M. Carrington , M. Hobbs , J. S. Mattick , B. Dalrymple , H. Kuramitsu , T. Shiroza , T. Foster , W. P. Clark , B. Ross , C. L. Squires , and M. R. Maurizi . 1990 . Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes . Proc. Natl. Acad. Sci. USA 87 : 3513 - 3517 . (10.1073/pnas.87.9.3513) / Proc. Natl. Acad. Sci. USA / Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes by Gottesman S. (1990)
  11. Groat , R. G. , J. E. Schultz , E. Zychlinshy , A. Bockman , and A. Matin . 1986 . Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival . J. Bacteriol. 168 : 486 - 493 . (10.1128/JB.168.2.486-493.1986) / J. Bacteriol. / Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival by Groat R. G. (1986)
  12. Grodberg , J. , M. D. Lundrigan , D. L. Toledo , W. R. Mangel , and J. J. Dunn . 1988 . Complete nucleotide sequence and deduced amino acid sequence of the ompT gene of Escherichia coli K-12 . Nucleic Acids Res. 16 : 1209 . (10.1093/nar/16.3.1209) / Nucleic Acids Res. / Complete nucleotide sequence and deduced amino acid sequence of the ompT gene of Escherichia coli K-12 by Grodberg J. (1988)
  13. Hwang , B. J. , K. M. Woo , A. L. Goldberg , and C. H. Chung . 1988 . Protease Ti, a new ATP-dependent protease in Escherichia coli, contains protein-activated ATPase and proteolytic functions in distinct subunits . J. Biol. Chem. 263 : 8727 - 8734 . (10.1016/S0021-9258(18)68366-8) / J. Biol. Chem. / Protease Ti, a new ATP-dependent protease in Escherichia coli, contains protein-activated ATPase and proteolytic functions in distinct subunits by Hwang B. J. (1988)
  14. Jenkins , D. E. , E. A. Auger , and A. Matin . 1991 . Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival . J. Bacteriol. 173 : 1992 - 1996 . (10.1128/JB.173.6.1992-1996.1991) / J. Bacteriol. / Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival by Jenkins D. E. (1991)
  15. Jenkins , D. E. , J. E. Schultz , and A. Matin . 1988 . Starvationinduced cross protection against heat or H202 challenge in Escherichia coli . J. Bacteriol. 170 : 3910 - 3914 . (10.1128/JB.170.9.3910-3914.1988) / J. Bacteriol. / Starvationinduced cross protection against heat or H202 challenge in Escherichia coli by Jenkins D. E. (1988)
  16. Katayama , Y. , S. Gottesman , J. Pumphrey , S. Rudikoff , W. P. Clark , and M. R. Maurizi . 1988 . The two-component, ATPdependent Clp protease of Escherichia coli: purification, cloning, and mutational analysis of the ATP-binding component . J. Biol. Chem. 263 : 15226 - 15236 . (10.1016/S0021-9258(18)68168-2) / J. Biol. Chem. / The two-component, ATPdependent Clp protease of Escherichia coli: purification, cloning, and mutational analysis of the ATP-binding component by Katayama Y. (1988)
  17. Kitagawa , M. , C. Wada , S. Yochioka , and T. Yura . 1991 . Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Eschenchia coli, is controlled by a heat shock v factor, C&2 . J. Bacteriol. 173 : 4247 - 4253 . (10.1128/JB.173.14.4247-4253.1991) / J. Bacteriol. / Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Eschenchia coli, is controlled by a heat shock v factor, C&2 by Kitagawa M. (1991)
  18. Kroh , H. E. , and L. D. Simon . 1990 . The ClpP component of Clp protease is the c2-dependent heat shock protein F21.5 . J. Bacteriol. 172 : 6026 - 6034 . (10.1128/JB.172.10.6026-6034.1990) / J. Bacteriol. / The ClpP component of Clp protease is the c2-dependent heat shock protein F21.5 by Kroh H. E. (1990)
  19. Lange , R. , and R. Hengge-Aronis . 1991 . Identification of a central regulator of stationary-phase gene expression in Escherichia coli . Mol. Microbiol. 5 : 49 - 59 . (10.1111/j.1365-2958.1991.tb01825.x) / Mol. Microbiol. / Identification of a central regulator of stationary-phase gene expression in Escherichia coli by Lange R. (1991)
  20. Lee , Y. S. , S. C. Park , A. L. Goldberg , and C. H. Chung . 1988 . Protease So from Escherichia coti preferentially degrades oxidatively damaged glutamine synthetase . J. Biol. Chem. 263 : 6643 - 6646 . (10.1016/S0021-9258(18)68690-9) / J. Biol. Chem. / Protease So from Escherichia coti preferentially degrades oxidatively damaged glutamine synthetase by Lee Y. S. (1988)
  21. Matin , A. 1990 . Molecular analysis of the starvation stress in Escherichia coli . FEMS Microbiol. Ecol. 74 : 185 - 196 . (10.1111/j.1574-6968.1990.tb04064.x) / FEMS Microbiol. Ecol. / Molecular analysis of the starvation stress in Escherichia coli by Matin A. (1990)
  22. Matin , A. 1991 . The molecular basis of carbon-starvationinduced general resistance in Escherichia coli . Mol. Microbiol. 5 : 3 - 10 . (10.1111/j.1365-2958.1991.tb01819.x) / Mol. Microbiol. / The molecular basis of carbon-starvationinduced general resistance in Escherichia coli by Matin A. (1991)
  23. Matin , A. , E. A. Auger , P. H. Blum , and J. E. Schultz . 1989 . Genetic basis of starvation survival in "nondifferentiating " bacteria. Annu. Rev. Microbiol. 43 : 293 - 316 . (10.1146/annurev.mi.43.100189.001453) / bacteria. Annu. Rev. Microbiol. / Genetic basis of starvation survival in "nondifferentiating by Matin A. (1989)
  24. Maurizi , M. R. , W. P. Clark , Y. Katayama , S. Rudikoff , J. Pumphrey , B. Bowers , and S. Gottesman . 1990 . Sequence and structure of ClpP, the proteolytic Component of the ATPdependent Clp protease of Eschenchia coli . J. Biol. Chem. 265 : 12536 - 12545 . (10.1016/S0021-9258(19)38378-4) / J. Biol. Chem. / Sequence and structure of ClpP, the proteolytic Component of the ATPdependent Clp protease of Eschenchia coli by Maurizi M. R. (1990)
  25. Maurizi , M. R. , W. P. Clark , S. -H. Kim , and S. Gottesman . 1990 . ClpP represents a unique family of serine proteases . J. Biol. Chem. 265 : 12546 - 12552 . (10.1016/S0021-9258(19)38379-6) / J. Biol. Chem. / ClpP represents a unique family of serine proteases by Maurizi M. R. (1990)
  26. McCann , M. P. , J. P. Kidwell , and A. Matin . 1991 . The putative a factor KatF has a central role in development of starvationmediated general resistance in Escherichia coli . J. Bacteriol. 173 : 4188 - 4194 . (10.1128/JB.173.13.4188-4194.1991) / J. Bacteriol. / The putative a factor KatF has a central role in development of starvationmediated general resistance in Escherichia coli by McCann M. P. (1991)
  27. Miller C. G. 1987. Protein degradation and proteolytic modification p. 680-691. In F. C. Neidhardt J. L. Ingraham K. B. Low B. Magasanik M. Schaechter and H. E. Umbarger (ed.) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology Washington D.C.
  28. O'Farrell , P. H. 1975 . High resolution two-dimensional electrophoresis of proteins . J. Biol. Chem. 250 : 4007 - 4021 . (10.1016/S0021-9258(19)41496-8) / J. Biol. Chem. / High resolution two-dimensional electrophoresis of proteins by O'Farrell P. H. (1975)
  29. Pine , M. J. 1965 . Heterogeneity of protein turnover in Escherichia coli . Biochim. Biophys. Acta 104 : 439 - 456 . (10.1016/0304-4165(65)90349-1) / Biochim. Biophys. Acta / Heterogeneity of protein turnover in Escherichia coli by Pine M. J. (1965)
  30. Reeve , C. A. , A. T. Bockman , and A. Matin . 1984 . Role of protein degradation in the survival of carbon-starved Escherichia coli and Salmonella typhimuium . J. Bacteriol. 157 : 758 - 763 . (10.1128/JB.157.3.758-763.1984) / J. Bacteriol. / Role of protein degradation in the survival of carbon-starved Escherichia coli and Salmonella typhimuium by Reeve C. A. (1984)
  31. Roseman , J. E. , and R. L. Levine . 1987 . Purification of a protease from E. coli with specificity for oxidized glutamine synthetase . J. Biol. Chem. 262 : 2101 - 2110 . (10.1016/S0021-9258(18)61623-0) / J. Biol. Chem. / Purification of a protease from E. coli with specificity for oxidized glutamine synthetase by Roseman J. E. (1987)
  32. Schroer , D. W. , and A. C. St. John . 1981 . Relative stability of membrane proteins in Eschenichia coli . J. Bacteriol. 146 : 476 - 483 . (10.1128/jb.146.2.476-483.1981) / J. Bacteriol. / Relative stability of membrane proteins in Eschenichia coli by Schroer D. W. (1981)
  33. Schultz , J. E. , G. I. Latter , and A. Matin . 1988 . Differential regulation by cyclic AMP of starvation protein synthesis in Escherichia coli . J. Bacteriol. 170 : 3903 - 3909 . (10.1128/JB.170.9.3903-3909.1988) / J. Bacteriol. / Differential regulation by cyclic AMP of starvation protein synthesis in Escherichia coli by Schultz J. E. (1988)
  34. Schultz , J. E. , and A. Matin . 1991 . Molecular and functional characterization of a carbon starvation gene of Escherichia coli . J. Mol. Biol. 218 : 129 - 140 . (10.1016/0022-2836(91)90879-B) / J. Mol. Biol. / Molecular and functional characterization of a carbon starvation gene of Escherichia coli by Schultz J. E. (1991)
  35. Spence , J. , A. Cegielska , and C. Georgopoulos . 1990 . Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation . J. Bacteriol. 172 : 7157 - 7166 . (10.1128/JB.172.12.7157-7166.1990) / J. Bacteriol. / Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation by Spence J. (1990)
  36. Squires , C. , and C. L. Squires . 1992 . The Clp proteins: proteolysis regulators or molecular chaperones ? J. Bacteriol. 174 : 1081 - 1085 . (10.1128/JB.174.4.1081-1085.1992) / J. Bacteriol. / The Clp proteins: proteolysis regulators or molecular chaperones by Squires C. (1992)
  37. Squires , C. L. , S. Pedersen , B. M. Ross , and C. Squires . 1991 . ClpB is the Eschenichia coli heat shock protein F84.1 . J. Bacteriol. 173 : 4254 - 4262 . (10.1128/JB.173.14.4254-4262.1991) / J. Bacteriol. / ClpB is the Eschenichia coli heat shock protein F84.1 by Squires C. L. (1991)
  38. St. John , A. C. , L. Cannavacciuolo , and D. W. Schroer . 1981 . Relative stability of intracellular proteins in bacterial cells . Acta Biol. Med. Ger. 40 : 1375 - 1384 . / Acta Biol. Med. Ger. / Relative stability of intracellular proteins in bacterial cells by St. John A. C. (1981)
  39. Strauch , K. L. , and J. Beckwith . 1988 . An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins . Proc. Natl. Acad. Sci. USA 85 : 1576 - 1580 . (10.1073/pnas.85.5.1576) / Proc. Natl. Acad. Sci. USA / An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins by Strauch K. L. (1988)
  40. Wickner , W. , A. J. M. Driessen , and F. -U. Hartl . 1991 . The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu . Rev. Biochem. 60 : 101 - 124 . (10.1146/annurev.bi.60.070191.000533) / Rev. Biochem. / The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu by Wickner W. (1991)
  41. Woo , K. M. , W. J. Chung , D. B. Ha , A. L. Goldberg , and C. J. Chung . 1989 . Protease Ti from Escherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides . J. Biol. Chem. 264 : 2088 - 2091 . (10.1016/S0021-9258(18)94145-1) / J. Biol. Chem. / Protease Ti from Escherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides by Woo K. M. (1989)
Dates
Type When
Created 8 years, 9 months ago (Nov. 7, 2016, 10:39 a.m.)
Deposited 4 years ago (July 29, 2021, 1:52 p.m.)
Indexed 1 year, 1 month ago (June 30, 2024, 2:29 p.m.)
Issued 32 years, 7 months ago (Jan. 1, 1993)
Published 32 years, 7 months ago (Jan. 1, 1993)
Published Print 32 years, 7 months ago (Jan. 1, 1993)
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@article{Damerau_1993, title={Role of Clp protease subunits in degradation of carbon starvation proteins in Escherichia coli}, volume={175}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.175.1.53-63.1993}, DOI={10.1128/jb.175.1.53-63.1993}, number={1}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Damerau, K and St John, A C}, year={1993}, month=jan, pages={53–63} }