Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32)
10.1128/jb.173.14.4247-4253.1991
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Escherichia coli K-12 produces at least two ATP-dependent proteases, Lon (La) and Clp (Ti), the latter consisting of a regulatory subunit (ClpA) and a proteolytic subunit (ClpP). The gene clpB encoding an analog of ClpA had been found at 57 min on the E. coli chromosome. Cloning and examination of novel heat shock promoters led us to identify a major clpB promoter specifically controlled by a heat shock sigma factor, sigma 32 (the rpoH [= htpR] gene product). beta-Galactosidase synthesis from a PclpB-lacZ operon fusion was transiently induced upon temperature shift from 30 to 42 degrees C, and the induction depended on the rpoH function. Chromosomal clpB transcripts also increased upon temperature upshift and were totally absent in the rpoH deletion strain. In the in vitro transcription experiments, the clpB promoter was specifically recognized and transcribed by RNA polymerase-sigma 32. Nucleotide sequencing and determination of mRNA start sites permitted us to identify a major heat shock promoter located upstream of the clpB coding sequence. The results clearly indicate that clpB expression is under direct control of sigma 32. Since ClpP was recently shown to be a sigma 32-dependent heat shock protein, the present finding suggests the possibility that a potential ATP-dependent protease, ClpB-ClpP complex, plays an important role against thermal stress in E. coli.

Bibliography

Kitagawa, M., Wada, C., Yoshioka, S., & Yura, T. (1991). Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). Journal of Bacteriology, 173(14), 4247–4253.

Authors 4
  1. M Kitagawa (first)
  2. C Wada (additional)
  3. S Yoshioka (additional)
  4. T Yura (additional)
References 36 Referenced 94
  1. Aiba , H. , S. Adhya , and B. de Crombrugghe . 1981 . Evidence for two functional gal promoters in intact Escherichia coli cells . J. Biol. Chem. 256 : 11905 - 11910 . (10.1016/S0021-9258(19)68491-7) / J. Biol. Chem. / Evidence for two functional gal promoters in intact Escherichia coli cells by Aiba H. (1981)
  2. Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. G. Seidman J. A. Smith and K. Struhl. 1987. Primer extension p. 4.8.1.-4.8.3. In Current protocols in molecular biology. Wiley Interscience New York.
  3. Baker , T. A. , A. D. Grossman , and C. A. Gross . 1984 . A gene regulating the heat shock response in Escherichia coli also affects proteolysis . Proc. Natl. Acad. Sci. USA 81 : 6779 - 6783 . (10.1073/pnas.81.21.6779) / Proc. Natl. Acad. Sci. USA / A gene regulating the heat shock response in Escherichia coli also affects proteolysis by Baker T. A. (1984)
  4. Casadaban , M. J. 1976 . Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu . J. Mol. Biol. 104 : 541 - 556 . (10.1016/0022-2836(76)90119-4) / J. Mol. Biol. / Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu by Casadaban M. J. (1976)
  5. Cowing , D. W. , J. C. A. Bardwell , E. A. Craig , C. Woolford , R. W. Hendrix , and C. A. Gross . 1985 . Consensus sequence for Escherichia coli heat shock gene promoters . Proc. Natl. Acad. Sci. USA 82 : 2679 - 2683 . (10.1073/pnas.82.9.2679) / Proc. Natl. Acad. Sci. USA / Consensus sequence for Escherichia coli heat shock gene promoters by Cowing D. W. (1985)
  6. Erickson , J. W. , and C. A. Gross . 1989 . Identification of the CuE subunit of Escherichia coli RNA polymerase: a second alternate u factor involved in high temperature gene expression . Genes Dev. 3 : 1462 - 1471 . (10.1101/gad.3.9.1462) / Genes Dev. / Identification of the CuE subunit of Escherichia coli RNA polymerase: a second alternate u factor involved in high temperature gene expression by Erickson J. W. (1989)
  7. Georgopoulos C. D. Ang K. Liberek and M. Zylicz. 1990. Properties of the Escherichia coli heat shock proteins and their role in bacteriophage X growth p. 191-221. In R. I. Morimoto A. Tissieres and C. Georgopoulos (ed.) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  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. , 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)
  10. Gross C. A. D. B. Straus J. W. Erickson and T. Yura. 1990. The function and regulation of heat shock proteins in Escherichia coli p. 167-189. In R. I. Morimoto A. Tissieres and C. Georgopoulos (ed.) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  11. Grossman , A. D. , J. W. Erickson , and C. A. Gross . 1984 . The htpR gene product of E. coli is a sigma factor for heat-shock promoters . Cell 38 : 383 - 390 . (10.1016/0092-8674(84)90493-8) / Cell / The htpR gene product of E. coli is a sigma factor for heat-shock promoters by Grossman A. D. (1984)
  12. Hirano , M. , K. Shigesada , and M. Imai . 1987 . Construction and characterization of plasmid and lambda phage vector systems for study of transcriptional control of Escherichia coli . Gene 57 : 89 - 99 . (10.1016/0378-1119(87)90180-6) / Gene / Construction and characterization of plasmid and lambda phage vector systems for study of transcriptional control of Escherichia coli by Hirano M. (1987)
  13. Hwang , B. J. , W. J. Park , C. H. Chung , and A. L. Goldberg . 1987 . Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La . Proc. Natl. Acad. Sci. USA 84 : 5550 - 5554 . (10.1073/pnas.84.16.5550) / Proc. Natl. Acad. Sci. USA / Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La by Hwang B. J. (1987)
  14. Katayama , Y. , S. Gottesman , J. Pumphrey , S. Rudikoff , W. P. Clark , and M. R. Maurizi . 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 . (10.1016/S0021-9258(18)68168-2) / J. Biol. Chem. / The two-component, ATP dependent Clp protease of Escherichia coli: purification, cloning, and mutational analysis of the ATP-binding component by Katayama Y. (1988)
  15. Katayama-Fujimura , Y. , S. Gottesman , and M. R. Maurizi . 1987 . A multiple-component, ATP-dependent protease from Escherichia coli . J. Biol. Chem. 262 : 4477 - 4485 . (10.1016/S0021-9258(18)61217-7) / J. Biol. Chem. / A multiple-component, ATP-dependent protease from Escherichia coli by Katayama-Fujimura Y. (1987)
  16. Kohara , Y. , K. Akiyama , and K. Isono . 1987 . The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library . Cell 50 : 495 - 508 . (10.1016/0092-8674(87)90503-4) / Cell / The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library by Kohara Y. (1987)
  17. Kroh , H. E. , and L. D. Simon . 1990 . The ClpP component of Clp protease is the 32-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 32-dependent heat shock protein F21.5 by Kroh H. E. (1990)
  18. Kusukawa , N. , and T. Yura . 1988 . Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress . Genes Dev. 2 : 874 - 882 . (10.1101/gad.2.7.874) / Genes Dev. / Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress by Kusukawa N. (1988)
  19. Lipinska , B. , S. Sharma , and C. Georgopoulos . 1988 . Sequence analysis and regulation of the htrA gene of Escherichia coli: cr 2-independent mechanism of heat-inducible transcription . Nucleic Acids Res. 16 : 10053 - 10066 . (10.1093/nar/16.21.10053) / Nucleic Acids Res. / Sequence analysis and regulation of the htrA gene of Escherichia coli: cr 2-independent mechanism of heat-inducible transcription by Lipinska B. (1988)
  20. 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 Escherichia 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 Escherichia coli by Maurizi M. R. (1990)
  21. Miller J. H. 1972. Experiments in molecular genetics p. 352-355. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  22. Neidhardt , F. C. , and R. A. VanBogelen . 1981 . Positive regulatory gene for temperature-controlled proteins in Escherichia coli . Biochem. Biophys. Res. Commun. 100 : 894 - 900 . (10.1016/S0006-291X(81)80257-4) / Biochem. Biophys. Res. Commun. / Positive regulatory gene for temperature-controlled proteins in Escherichia coli by Neidhardt F. C. (1981)
  23. Neidhardt F. C. and R. A. VanBogelen. 1987. Heat shock response p. 1334-1345. 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 vol. 2. American Society for Microbiology Washington D.C.
  24. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  25. Shen , W. - F. , C. Squires , and C. L. Squires . 1982 . Nucleotide sequence of the rrnG ribosomal RNA promoter region of Escherichia coli . Nucleic Acids Res. 10 : 3303 - 3313 . (10.1093/nar/10.10.3303) / Nucleic Acids Res. / Nucleotide sequence of the rrnG ribosomal RNA promoter region of Escherichia coli by Shen W. (1982)
  26. Squires C. B. M. Ross and C. L. Squires. 1990. GenBank access no. M29364.
  27. . Squires , C. L. , S. Pedersen , B. M. Ross , and C. Squires . 1991 . ClpB is the Escherichia coli heat shock protein F84.1 . J. Bacteriol. 173 : 4254 - 4262 . (10.1128/jb.173.14.4254-4262.1991) / J. Bacteriol. / ClpB is the Escherichia coli heat shock protein F84.1 by Squires C. L. (1991)
  28. Straus , D. , W. Walter , and C. A. Gross . 1990 . DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of a2 . Genes Dev. 4 : 2202 - 2209 . (10.1101/gad.4.12a.2202) / Genes Dev. / DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of a2 by Straus D. (1990)
  29. Straus , D. B. , W. A. Walter , and C. A. Gross . 1988 . Escherichia coli heat shock gene mutants are defective in proteolysis . Genes Dev. 2 : 1851 - 1858 . (10.1101/gad.2.12b.1851) / Genes Dev. / Escherichia coli heat shock gene mutants are defective in proteolysis by Straus D. B. (1988)
  30. Taylor , W. E. , D. B. Straus , A. D. Grossman , Z. F. Burton , C. A. Gross , and R. R. Burgess . 1984 . Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase . Cell 38 : 371 - 381 . (10.1016/0092-8674(84)90492-6) / Cell / Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase by Taylor W. E. (1984)
  31. Tobe , T. , K. Ito , and T. Yura . 1984 . Isolation and physical mapping of temperature-sensitive mutants defective in heatshock induction of proteins in Escherichia coli . Mol. Gen. Genet. 195 : 10 - 16 . (10.1007/BF00332716) / Mol. Gen. Genet. / Isolation and physical mapping of temperature-sensitive mutants defective in heatshock induction of proteins in Escherichia coli by Tobe T. (1984)
  32. Wada , C. , M. Imai , and T. Yura . 1987 . Host control of plasmid replication: requirement for the a factor C32 in transcription of mini-F replication initiator gene . Proc. Natl. Acad. Sci. USA 84 : 8849 - 8853 . (10.1073/pnas.84.24.8849) / Proc. Natl. Acad. Sci. USA / Host control of plasmid replication: requirement for the a factor C32 in transcription of mini-F replication initiator gene by Wada C. (1987)
  33. Wang , Q. , and J. M. Kaguni . 1989 . A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli . J. Bacteriol. 171 : 4248 - 4253 . (10.1128/jb.171.8.4248-4253.1989) / J. Bacteriol. / A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli by Wang Q. (1989)
  34. Yamamori , T. , and T. Yura . 1980 . Temperature-induced synthesis of specific proteins in Escherichia c61i: evidence for transcriptional control . J. Bacteriol. 142 : 843 - 851 . (10.1128/jb.142.3.843-851.1980) / J. Bacteriol. / Temperature-induced synthesis of specific proteins in Escherichia c61i: evidence for transcriptional control by Yamamori T. (1980)
  35. Yamamonr , T. , and T. Yura . 1982 . Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12 . Proc. Natl. Acad. Sci. USA 79 : 860 - 864 . (10.1073/pnas.79.3.860) / Proc. Natl. Acad. Sci. USA / Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12 by Yamamonr T. (1982)
  36. Yano , R. , M. Imna , and T. Yura . 1987 . The use of operon fusions in studies of the heat-shock promoter function in Escherichia coli . Mol. Gen. Genet. 207 : 24 - 28 . (10.1007/BF00331486) / Mol. Gen. Genet. / The use of operon fusions in studies of the heat-shock promoter function in Escherichia coli by Yano R. (1987)
Dates
Type When
Created 8 years, 9 months ago (Nov. 7, 2016, 11:33 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:52 p.m.)
Indexed 1 year ago (Aug. 6, 2024, 12:20 p.m.)
Issued 34 years, 2 months ago (July 1, 1991)
Published 34 years, 2 months ago (July 1, 1991)
Published Print 34 years, 2 months ago (July 1, 1991)
Funders 0

None

@article{Kitagawa_1991, title={Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32)}, volume={173}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.173.14.4247-4253.1991}, DOI={10.1128/jb.173.14.4247-4253.1991}, number={14}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Kitagawa, M and Wada, C and Yoshioka, S and Yura, T}, year={1991}, month=jul, pages={4247–4253} }