Advertisement

Experientia

, Volume 48, Issue 2, pp 178–201 | Cite as

Proteases and protein degradation inEscherichia coli

  • M. R. Maurizi
Multi-Author Review Proteases as Biological Regulators

Abstract

InE. coli, protein degradation plays important roles in regulating the levels of specific proteins and in eliminating damaged or abnormal proteins.E. coli possess a very large number of proteolytic enzymes distributed in the cytoplasm, the inner membrane, and the periplasm, but, with few exceptions, the physiological functions of these proteases are not known. More than 90% of the protein degradation occurring in the cytoplasm is energy-dependent, but the activities of mostE. coli proteases in vitro are not energy-dependent. Two ATP-dependent proteases, Lon and Clp, are responsible for 70–80% of the energy-dependent degradation of proteins in vivo. In vitro studies with Lon and Clp indicate that both proteases directly interact with substrates for degradation. ATP functions as an allosteric effector promoting an active conformation of the proteases, and ATP hydrolysis is required for rapid catalytic turnover of peptide bond cleavage in proteins. Lon and Clp show virtually no homology at the amino acid level, and thus it appears that at least two families of ATP-dependent proteases have evolved independently.

Key words

ATP-dependent degradation protease Lon Clp 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Amerik, A. Y., Antonov, V. K., Gorbalenya, A. E., Kotova, S. A., Rotanova, T. V., and Shimbarevich, E. V., Site-directed mutagenesis of La protease. FEBS Lett.287 (1991) 211–214.CrossRefPubMedGoogle Scholar
  2. 2.
    Bachmair, A., Finley, D., and Varshavsky, A., In vivo half-life of a protein is a function of its amino-terminal residue. Science234 (1986) 179–186.PubMedGoogle Scholar
  3. 3.
    Bachmair, A., and Varshavsky, A., The degradation signal in a short-lived protein. Cell56 (1989) 1019–1032.CrossRefPubMedGoogle Scholar
  4. 4.
    Bahl, H., Echols, H., Straus, D. B., Court, D., Crowl, R., and Georgopoulos, C. P., Induction of the heat shock response ofE. coli through stabilization of sigma 32 by the phage lambda cIII protein. Genes Development1 (1987) 57–64.PubMedGoogle Scholar
  5. 5.
    Baker, T. A., Grossman, A. D., and Gross, C. A., A gene regulating the heat shock response inEscherichia coli also affects proteolysis. Proc. natl Acad. Sci. USA81 (1984) 6779–6783.PubMedGoogle Scholar
  6. 6.
    Baneyx, F., and Georgiou, G., In vivo degradation of secreted fusion proteins by theEscherichia coli outer membrane protease OmpT. J. Bact.172 (1990) 491–494.PubMedGoogle Scholar
  7. 7.
    Banuett, F., Hoyt, M. A., McFarlane, L., Echols, H., and Herskowitz, I.,hflB, a newEscherichia coli locus regulating lysogeny and the level of bacteriophage lambda cII protein. J. molec. Biol.187 (1986) 213–224.PubMedGoogle Scholar
  8. 8.
    Ben-Bassat, A., Bauer, K., Chang, S. Y., Myambo, K., Bossman, A., and Chang, S., Processing of the initiation methionine from proteins: properties of theEscherichia coli methionine peptidase and its structure. J. Bact.169 (1987) 751–757.PubMedGoogle Scholar
  9. 9.
    Bond, J. S., and Butler, P. E., Intracellular proteases. A. Rev. Biochem.56 (1987) 333–364.CrossRefGoogle Scholar
  10. 10.
    Bonnefoy, E., Almeida, A., and Rouviere-Yaniv, J., Lon-dependent regulation of the DNA-binding protein HU inEscherichia coli. Proc. natl Acad. Sci. USA86 (1990) 7691–7695.Google Scholar
  11. 11.
    Bowie, J. U., and Sauer, R. T., Identification of C-terminal extensions that protect proteins from intracellular proteolysis. J. biol. Chem.264 (1989) 7596–7602.PubMedGoogle Scholar
  12. 12.
    Bukhari, A. I., and Zipser, D., Mutants ofEscherichia coli with a defect in the degradation of nonsense fragments. Nature243 (1973) 238–241.PubMedGoogle Scholar
  13. 13.
    Burckhardt, S. E., Woodgate, R., Scheuermann, R. H., and Echols, H., UmuD mutagenesis protein ofEscherichia coli: Overproduction, purification, and cleavage by RecA. Proc. natl Acad. Sci. USA85 (1988) 1811–1815.PubMedGoogle Scholar
  14. 14.
    Canceill, D., Dervyn, E., and Huisman, O., Proteolysis and modulation of the activity of the cell division inhibitor SulA inEscherichia coli Ion mutants. J. Bact.172 (1990) 7297–7300.PubMedGoogle Scholar
  15. 15.
    Caron, P. R., and Grossman, L., Potential role of proteolysis in the control of UvrABC incision. Nucl. Acids Res.16 (1988) 10903–10912.PubMedGoogle Scholar
  16. 16.
    Cavard, D., and Lazdunski, C., Colicin cleavage by OmpT protease during both entry into and release fromEscherichia coli cells. J. Bact.172 (1990) 648–652.PubMedGoogle Scholar
  17. 17.
    Cavard, D., Lazdunski, C., and Howard, S. P., The acylated precursor form of the Colicin A lysis protein is a natural substrate of the DegP protease. J. Bact.171 (1989) 6316–6322.PubMedGoogle Scholar
  18. 18.
    Charette, M., Henderson, G. W., and Markovitz, A., ATP hydrolysis-dependent activity of thelon(capR) protein ofE. coli K12. Proc. natl Acad. Sci. USA78 (1981) 4728–4732.PubMedGoogle Scholar
  19. 19.
    Charette, M. F., Henderson, G. W., Doane, L. L., and Markovitz, A., DNA Stimulated ATPase Activity of the Lon (CapR) Protein. J. Bact.158 (1984) 195–201.PubMedGoogle Scholar
  20. 20.
    Cheng, H. H., Muhlrad, P. J., Hoyt, A., and Echols, H., Cleavage of the cII protein of phage lambda purified HflA protease: control of the switch between lysis and lysogeny. Proc. natl Acad. Sci. USA85 (1988) 7882–7886.PubMedGoogle Scholar
  21. 21.
    Cheng, Y. S., and Zipser, D., Purification and characterization of protease III fromEscherichia coli. J. biol. Chem.254 (1979) 4698–4706.PubMedGoogle Scholar
  22. 22.
    Cheng, Y.-S. E., Zipser, D., Cheng, C.-Y., and Roiseth, S. J., Isolation and characterization of mutations in the structural gene for protease III (ptr). J. Bact.140 (1979) 125–130.PubMedGoogle Scholar
  23. 23.
    Chin, D. T., Goff, S. A., Webster, T., Smith, T., and Goldberg, A. L., Sequence of theIon gene inEscherichia coli: A heat-shock gene which encodes the ATP-dependent protease La. J. biol. Chem.263 (1988) 11718–11728.PubMedGoogle Scholar
  24. 24.
    Chung, C. H., and Goldberg, A. L., DNA stimulates ATP-dependent proteolysis and protein-dependent ATPase activity of protease La fromEscherichia coli. Proc. natl Acad. Sci. USA79 (1982) 795–799.PubMedGoogle Scholar
  25. 25.
    Chung, C. H., and Goldberg, A. L., The product of theIon(capR) gene inEscherichia coli is the ATP-dependent protease, protease La. Proc. natl Acad. Sci. USA78 (1981) 4931–4935.PubMedGoogle Scholar
  26. 26.
    Chung, C. H., and Goldberg, A. L., Purification and characterization of protease So, a cytoplasmic serine protease inEscherichia coli. J. Bact.154 (1983) 231–238.PubMedGoogle Scholar
  27. 27.
    Chung, C. H., Ives, H. E., Almeda, S., and Goldberg, A. L., Purification fromEscherichia coli of a periplasmic protein that is a potent inhibitor of pancreatic proteases. J. biol. Chem.258 (1983) 11032–11038.PubMedGoogle Scholar
  28. 28.
    Claverie-Martin, F., Diaz-Torres, M. R., Kushner, S. R., Analysis of the regulatory region of the protease III (ptr) gene ofEscherichia coli K12. Gene54 (1987) 185–195.CrossRefPubMedGoogle Scholar
  29. 29.
    Craig, N. L., and Roberts, J. W., Function of nucleoside triphosphate and polynucleotide inEscherichia coli recA protein directed cleavage of phage lambda repressor. J. biol. Chem.256 (1981) 8039–8044.PubMedGoogle Scholar
  30. 30.
    Davies, K. J. A., and Lin, S. W., Degradation of oxidatively denatured protein inEscherichia coli. Free Radic. Biol. Med.5 (1988) 215–223.CrossRefPubMedGoogle Scholar
  31. 31.
    Dennis, P. P., Synthesis and stability of individual ribosomal proteins in the presence of rifampicin. Mol. gen. Genet.134 (1974) 39–47.CrossRefPubMedGoogle Scholar
  32. 32.
    Derbyshire, C., Kramer, M., and Grindley, N. D. F., Role of instability in the cis action of the insertion sequence IS903 transposase. Proc. natl Acad. Sci. USA87 (1990) 4048–4052.PubMedGoogle Scholar
  33. 33.
    Dervyn, E., Canceill, D., and Huisman, O., Saturation and specificity of the Lon protease ofEscherichia coli. J. Bact.172 (1990) 7098–7103.PubMedGoogle Scholar
  34. 34.
    Desautels, M., and Goldberg, A. L., Liver mitochondria contain an ATP-dependent, vanadate-sensitive pathway for the degradation of proteins. Proc. natl Acad. Sci. USA79 (1982) 1869–1873.PubMedGoogle Scholar
  35. 35.
    Donch, J., and Greenberg, J., Genetic analysis oflon mutants of strain K-12 ofEscherichia coli. Mol. gen. Genet.103 (1968) 105–115.CrossRefPubMedGoogle Scholar
  36. 36.
    Downs, D., Waxman, L., Goldberg, A. L., and Roth, J., Isolation and characterization oflon mutants inSalmonella typhimurium. J. Bact.167 (1986) 193–197.40.Google Scholar
  37. 37.
    Dykstra, C. C., and Kushner, S. R., Physical Characterization of the cloned Protease III gene fromEscherichia coli K-12 J. Bact.163 (1985) 1055–1059.PubMedGoogle Scholar
  38. 38.
    Edmunds, T., and Goldberg, A. L., Role of ATP hydrolysis in the degradation of proteins by protease La fromEscherichia coli. J. cell. Biochem.32 (1986) 187–191.CrossRefPubMedGoogle Scholar
  39. 39.
    Eytan, E., Ganoth, D., Armon, T., and Hershko, A., ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. Proc. natl Acad. Sci. USA86 (1989) 7751–7755.PubMedGoogle Scholar
  40. 40.
    Falkenburg, P. E., Haass, C., Kloetzel, P. M., Niedel, B., Kopp, F., Kuehn, L., and Dahlmann, B., Drosophila small cytoplasmic 19S ribonucleoprotein is homologous to the rat multicatalytic proteinase. Nature331 (1988) 190–192.CrossRefPubMedGoogle Scholar
  41. 41.
    Finley, D., Ciechanover, A., and Varshavsky, A., Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutantts85. Cell37 (1984) 43–55.CrossRefGoogle Scholar
  42. 42.
    Finch, P. W., Wilson, R. R., Brown, K., Hickson, I. D., and Emmerson, P. T., Complete nucleotide sequence of theEscherichia coli ptr gene encoding Protease III. Nucl. Acids Res.14 (1986) 7695–7703.PubMedGoogle Scholar
  43. 43.
    Fujiwara, T., Tanaka, K., Orino, E., Hoshimura, T., Kumatori, A., Tamura, T., Chung, C. H., Nakai, T., Yamaguchi, K., Shin, S., Kakizuka, A., Nakanishi, S., and Ichihara, A., Proteasomes are essential for yeast proliferation. J. biol. Chem.265 (1990) 16604–1663.PubMedGoogle Scholar
  44. 44.
    Ganoth, D., Leshinsky, E., Eytan, E., and Hershko, A., A multicomponent system that degrades proteins conjugated to ubiquitin. J. biol. Chem.263 (1988) 12412–12419.PubMedGoogle Scholar
  45. 45.
    Georgopoulos, C., Ang. D., Libeleric, K., and Zylicz, M., Properties of theEscherichia coli heat shock proteins and their role in bacteriophage λ growth in: Stress Proteins in Biology and Medicine, pp. 191–221. Eds R. Morimoto, A. Tissieres and C. Georgopoulos. Cold Spring Harbor Press 1990.Google Scholar
  46. 46.
    Goff, S. A., and Goldberg, A. L., An increased content of protease La, thelon gene product, increases protein degradation and blocks growth inEscherichia coli. J. biol. Chem.262 (1987) 4508–4515.PubMedGoogle Scholar
  47. 47.
    Goff, S. A., Casson, L. P., and Goldberg, A. L., Heat shock regulatory genehtpR influences rates of protein degradation and expression of thelon gene inEscherichia coli. Proc. natl Acad. Sci. USA81 (1984) 6647–6651.PubMedGoogle Scholar
  48. 48.
    Goff, S. A., and Goldberg, A. L., Production of abnormal proteins inE. coli stimulates transcription oflon and other heat shock genes. Cell41 (1985) 587–595.CrossRefPubMedGoogle Scholar
  49. 49.
    Goldberg, A. L., Degradation of abnormal proteins inEscherichia coli. Proc. natl Acad. Sci. USA69 (1972) 422–426.PubMedGoogle Scholar
  50. 50.
    Goldberg, A. L., and St. John, A. C., Intracellular protein degradation in mammalian and bacterial cells: part 2. A. Rev. Biochem.45 (1976) 747–803.CrossRefGoogle Scholar
  51. 51.
    Goldberg, A. L., Streedhara Swamy, K. H., Chung, C. H., and Larimore, F. S., Proteases ofEscherichia coli. Meth. Enzym.80 (1983) 680–702.Google Scholar
  52. 52.
    Goldberg, A. L., and Waxman, L., The role of ATP hydrolysis in the breakdown of proteins and peptides by protease La fromEscherichia coli. J. biol. Chem.260 (1985) 12029–12034.PubMedGoogle Scholar
  53. 53.
    Goldschmidt, R., In vivo degradation of nonsense fragements inE. coli. Nature (London)228 (1970) 1151–1154.Google Scholar
  54. 54.
    Gottesman, S., Regulation by proteolysis, in:Escherichia coli andSalmonella typhimurium: Cellular and Molecular Biology, pp. 1308–1312. Eds F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaecter and H. E. Umbarger. American Society for Microbiology, Washington, D.C. 1987.Google Scholar
  55. 55.
    Gottesman, S., Genetics of proteolysis inEscherichia coli. A. Rev. Genet.23 (1989) 163–198.CrossRefGoogle Scholar
  56. 56.
    Gottesman, S., Clark, W. P., and Maurizi, M. R., The ATP-dependent Clp protease ofEscherichia coli sequence ofclpA and identification of a Clp-specific substrate. J. Biol. Chem.265 (1990) 7886–7893.PubMedGoogle Scholar
  57. 57.
    Gottesman, S., Gottesman, M., Shaw, J., and Pearson, M. L., Protein degradation inE. coli: thelon mutation and bacteriophage lambda N and cII protein stability. Cell24 (1981) 225–233.CrossRefPubMedGoogle Scholar
  58. 58.
    Gottesman, S., Squires, C., Pichersky, E., Carrington, M., Hobbs, M., Mattick, J. S., Dalrymple, B., Kuramitsu, H., Shiroza, T., Foster, T., Clark, W. P., Ross, B., Squires, C., and Maurizi, M. R., Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc. natl Acad. Sci. USA87 (1990) 3513–3517.PubMedGoogle Scholar
  59. 59.
    Gottesman, S., and Zipser, D., The Deg phenotype ofEscherichia coli lon mutants. J. Bact.133 (1978) 844–851.PubMedGoogle Scholar
  60. 60.
    Grodberg, J., and Dunn, J. J.,ompT Encodes theEscherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bact.170 (1988) 1245–1253.PubMedGoogle Scholar
  61. 61.
    Grossman, A. D., Burgess, R., Walter, W., and Gross, C., Mutations in thelon gene ofE. coli K12 phenotypically suppress a mutation in the sigma subunit of RNA polymerase. Cell32 (1983) 151–159CrossRefPubMedGoogle Scholar
  62. 62.
    Grossman, A. D., Erickson, J. W., and Gross, C. A., ThehtpR gene product ofE. coli is a sigma factor for heat shock promoters. Cell38 (1984) 383–390.CrossRefPubMedGoogle Scholar
  63. 63.
    Grossman, A. D., Straus, D. B., Walter, W. A., and Gross, C. A., Sigma 32 synthesis can regulate the synthesis of heat shock proteins inEscherichia coli. Genes Dev.1 (1987) 179–184.PubMedGoogle Scholar
  64. 63a.
    Heinemeyer, W., Kleinschmidt, J. A., Saidowsky, J., Escher, C., and Wolf, D. H., Proteinase YscE, the yeast proteasome/multicatalyticmultifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J.10 (1991) 555–562.PubMedGoogle Scholar
  65. 64.
    Hershko, A., Ubiquitin-mediated protein degradation. J. biol. Chem.263 (1990) 15237–15240Google Scholar
  66. 65.
    Holck, A., and Kleppe, K., Cloning and sequence of the gene for the DNA-binding 17K protein ofEscherichia coli. Gene67 (1988) 117–124.CrossRefPubMedGoogle Scholar
  67. 66.
    Hopfield, J. J., Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. natl Acad. Sci. USA71 (1974) 4135–4139.PubMedGoogle Scholar
  68. 67.
    Hough, R., Pratt, G., and Rechensteiner, M., Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J. biol. Chem.262 (1987) 8303–8313.PubMedGoogle Scholar
  69. 68.
    Hoyt, M. A., Knight, D. M., Das, A., Miller, H. I., and Echols, H., Control of phage lambda development by stability and synthesis of cII protein: Role of the viral cIII and hosthflA, himA andhimD genes. Cell31 (1982) 565–573.CrossRefPubMedGoogle Scholar
  70. 69.
    Huisman, O., D'Ari, R., and Gottesman, S., Cell division control inEscherichia coli: specific induction of the SOS SfiA protein is sufficient to block septation. Proc. natl Acad. Sci. USA81 (1984) 4490–4494.PubMedGoogle Scholar
  71. 70.
    Hwang, B. J., Park, W. J., Chung, C. H., and Goldberg, A. L.,Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proc. natl Acad. Sci. USA84 (1987) 5550–5554.PubMedGoogle Scholar
  72. 71.
    Hwang, B. J., Woo, K. M., Goldberg, A. L., and Chung, C. H., Protease Ti, a new ATP-dependent protease inEscherichia coli contains protein-activated ATPase and proteolytic functions in distinct subunits. J. biol. Chem.263 (1988) 8727–8734.PubMedGoogle Scholar
  73. 72.
    Ichihara, S., Beppu, N., and Mizushima, S., Protease IV, a cytoplasmic membrane protein ofEscherichia coli, has signal peptide peptidase activity. J. biol. Chem.259 (1984) 9853–9857.PubMedGoogle Scholar
  74. 73.
    Ichihara, S., Suzuki, T., Suzuki, M., and Mizushima, S., Molecular cloning and sequencing of thesppA gene and characterization of the encoded protease IV, a signal peptide peptidase, ofEscherichia coli. J. biol. Chem.261 (1986) 9405–9411.PubMedGoogle Scholar
  75. 74.
    Innis, M. A., Tokunaga, M., Williams, M. E., Loranger, J. M., Chang, S. Y., Chang, S., and Wu, H. C., Nucleotide sequence of theEscherichia coli prolipoprotein signal peptidase (lsp) gene. Proc. natl Acad. Sci. USA81 (1984) 3708–3712.PubMedGoogle Scholar
  76. 75.
    Ishihama, A., Fujita, N., and Glass, R. E., Subunit assembly and metabolic stability ofE. coli RNA polymerase. Prot. Struct. Funct. Gen.2 (1987) 42–53.CrossRefGoogle Scholar
  77. 76.
    Johnson, C., Chandrasekhar, G. N., and Georgopoulos, C.,Escherichia coli DnaK and GrpE heat shock proteins interact both in vivo and in vitro. J. Bact.171 (1989) 1590–1596.PubMedGoogle Scholar
  78. 77.
    Jones, C. A., and Holland, I. B., Role of the SfiB (FtsZ) protein in division inhibition during the SOS response inE. coli: FtsZ stabilizes the inhibitor SfiA in maxicells. Proc. natl Acad. Sci. USA82 (1985) 6045–6049.PubMedGoogle Scholar
  79. 78.
    Katayama, Y., Gottesman, S., Pumphrey, J., Rudikoff, S., Clark, W. P., and Maurizi, M. R., The two-component ATP-dependent Clp Protease ofEscherichia coli: purification, cloning, and mutational analysis of the ATP-binding component. J. biol. Chem.263 (1988) 15226–15236.PubMedGoogle Scholar
  80. 79.
    Katayama-Fujimura, Y., Gottesman, S., and Maurizi, M. R., a multiple-component, ATP-dependent protease fromEscherichia coli. J. biol. Chem.262 (1987) 4477–4485.PubMedGoogle Scholar
  81. 80.
    Keller, J. A., and Simon, L. D., Divergent effects of adnaK mutation on abnormal protein degradation inEscherichia coli. Molec. Microbiol.2 (1988) 31–41.Google Scholar
  82. 80a.
    Kitagawa, M., Wada, C., Yoshioka, S., and Yura, T., Expression of ClpB, an analog of the ATP-dependent protease-regulatory subunit inEscherichia coli is controlled by heat shock σ factor (σ32). J. Bact.173 (1991) 4247–4253.PubMedGoogle Scholar
  83. 81.
    Kornitzer, D., Altuvia, S., and Oppenheim, A. B., The activity of the CIII regulator of lamboid bacteriophages resides within a 24-amino acid protein domain. Proc. natl Acad. Sci. USA88 (1991).Google Scholar
  84. 82.
    Kroh, H. E., and Simon, L. E., The ClpP component of Clp protease is the σ32-dependent heat shock protein F21.5. J. Bact.172 (1990) 6026–6034.PubMedGoogle Scholar
  85. 83.
    Kuhn, A., and Wickner, W., Conserved residues of the leader peptide are essential for cleavage by leader peptidase. J. biol. Chem.260 (1985) 55914–15918.Google Scholar
  86. 84.
    Lazarides, E., and Moon, R. T., Assembly and topogenesis of the spectrin-based membrane skeleton in erythroid development. Cell37 (1984) 354–356.CrossRefPubMedGoogle Scholar
  87. 85.
    Lee, C. S., Hahm, J. K., Hwang, B. J., Park, K. C., Ha, D. B., Park, S. D., and Chung, C. H., Processing of Ada protein by two serine endoproteases Do and So fromEscherichia coli. FEBS Lett.262 (1990) 310–312.CrossRefPubMedGoogle Scholar
  88. 86.
    Lee, Y. S., Park, S. C., Goldberg, A. L., and Chung, C. H., Protease So fromEscherichia coli preferentially degrades oxidatively damaged glutamine synthetase. J. biol. Chem.263 (1988) 6643–6646.PubMedGoogle Scholar
  89. 87.
    Lindahl, T., Sedgwick, B., Sekiguchi, M., and Nakabeppu, Y., Regulation and expression of the adaptive response to alkylating agents. A. Rev. Biochem.57 (1988) 133–157.CrossRefGoogle Scholar
  90. 88.
    Lipinska, B., Fayet, O., Baird, L., and Georgopoulos, C. Identification, characterization, and mapping of theEscherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J. Bact.171 (1989) 1574–1584.PubMedGoogle Scholar
  91. 89.
    Lipinska, B., Zylicz, M., and Georgopoulos, C., The HtrA (DegP) protein, essential forEscherichia coli survival at high temperatures, is an endopeptidase. J. Bact.172 (1990) 1791–1797.PubMedGoogle Scholar
  92. 90.
    Little, J. W., Autodigestion of LexA and phage lambda repressors. Proc. natl Acad. Sci. USA81 (1984) 1375–1379.PubMedGoogle Scholar
  93. 91.
    Little, J. W., Edmiston, S. H., Pacelli, L. Z., and Mount, D. W., Cleavage of theEscherichia coli lexA protein by therecA protease. Proc. natl Acad Sci. USA77 (1980) 3225–3229.PubMedGoogle Scholar
  94. 92.
    Little, J. W., and Mount, D. W., The SOS regulatory system ofEscherichia coli. Cell29 (1982) 11–22.CrossRefPubMedGoogle Scholar
  95. 93.
    Mandelstam, J., Turnover of protein in growing and nongrowing population ofEscherichia coli. Biochem. J.169 (1958) 110–119.Google Scholar
  96. 94.
    Maurizi, M. R., Degradation in vitro of bacteriophage lambda N protein by Lon protease fromEscherichia coli. J. biol. Chem.262 (1987) 2696–2703.PubMedGoogle Scholar
  97. 95.
    Maurizi, M. R., ATP-promoted interaction between ClpA and ClpP in activation of Clp protease fromEscherichia coli. Biochem. Soc. Trans. (1991) in press.Google Scholar
  98. 96.
    Maurizi, M. R., Katayama, Y., and Gottesman, S., Selective ATP-dependent degradation of proteins inEscherichia coli, in: The Ubiquitin System. Current Communications in Molecular Biology, pp. 147–154. Ed. M. J. Schlesinger. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 1988.Google Scholar
  99. 97.
    Maurizi, M. R., Clark, W. P., Katayama, Y., Rudikoff, S., Pumphrey, J., Bowers, B., and Gottesman, S., Sequence and structure of ClpP, the proteolytic component of the ATP-dependent Clp protease ofEscherichia coli. J. biol. Chem.265 (1990) 12536–12545.PubMedGoogle Scholar
  100. 98.
    Maurizi, M. R., Clark, W. P., Kim, S. H., and Gottesman, S. J., ClpP represnts a unique family of serine proteases. Biol. Chem.265 (1990) 12546–12552.Google Scholar
  101. 99.
    Maurizi, M. R., and Switzer, R. L., Proteolysis in bacterial sporulation. Curr. Top. Cell Regul.16 (1979) 163–224.Google Scholar
  102. 100.
    Maurizi, M. R., Trisler, P., and Gottesman, S., Insecrtional mutagenesis of thelon gene inEscherichia coli: lon is dispensable. J. Bact.164 (1985) 1124–1135.PubMedGoogle Scholar
  103. 101.
    mcGrath, M. E., Hines, W. M., Sakanari, J. A., Fletterick, R. J., and Craik, C. S., The sequence and reactive site of Ecotin. J. biol. Chem.266 (1991) 6620–6625.PubMedGoogle Scholar
  104. 102.
    Menon, A. S., and Goldberg, A. L., binding of nucleotides to the ATP-dependent protease La fromEscherichia coli. J. biol. Chem.262 (1987) 14921–14928.PubMedGoogle Scholar
  105. 103.
    Menon, A. S., and Goldberg, A. L., Protein substrates activate the ATP-dependent protease La by promoting nucleotide binding and release of bound ADP. J. biol. Chem.262 (1987) 14929–14934.PubMedGoogle Scholar
  106. 104.
    Menon, A. S., Waxman, L., and Goldberg, A. L., The energy utilized in protein breakdown by the ATP-dependent protease La fromEscherichia coli. J. biol. Chem.262 (1987) 722–726.PubMedGoogle Scholar
  107. 105.
    Michaelis, S., and Beckwith, J., Mechanism of incorporation of cell envelop proteins inEscherichia coli. A. Rev. Microbiol.36 (1982) 435–465.CrossRefGoogle Scholar
  108. 106.
    Miller, C. G., Protein degradation and proteolytic modification in:Escherichia coli andSalmonella typhimurium: Cellular and Molecular Biology, pp. 680–691. Eds F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter and H. E. Umbarger. American Society for Microbiology, Washington, D.C. 1987.Google Scholar
  109. 107.
    Miller, C. G., Genetics and physiological roles ofSalmonella typhimurium peptidases, in: Microbiology 1985, pp. 346–349. Ed. L. Leive. American Society for Microbiology, Washington, D.C. 1985.Google Scholar
  110. 108.
    Miller, C. G., and Schwartz, G., Peptidase-deficient mutants ofEscherichia coli. J. Bact.135 (1978) 603–611.PubMedGoogle Scholar
  111. 109.
    Mizusawa, S., and Gottesman, S., Protein degradation inEscherichia coli: Thelon gene controls the stability of the SulA protein. Proc. natl Acad. Sci. USA80 (1983) 358–362.PubMedGoogle Scholar
  112. 110a.
    Mosteller, R. D., Goldstein, R. V., and Nishimoto, K. R., Metabolism of individual proteins in exponentially growingEscherichia coli. J. biol. Chem.255 (1980) 2524–2532.PubMedGoogle Scholar
  113. 110b.
    Moesteller, R. D., Nishimoto, K. R., and Goldstein, R. V., Inactivation and partial degradation of phosphoribosylanthranilate isomerase-indoleglycerol phosphate synthetase in nongrowing cultures ofEscherichia coli. J. Bact.131 (1977) 153–162.PubMedGoogle Scholar
  114. 111.
    Murray, A. W., Solomon, M. J., and Kirschner, M. W., The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature339 (1989) 280–286.CrossRefPubMedGoogle Scholar
  115. 112.
    Nash, H. A., Robertson, C. A., Flamm, E., Weisberg, R. A., and Miller, H. I., Overproduction ofEscherichia coli: integration host factor, a protein with nonidentical subunits. J. Bact.169 (1987) 4124–4127.PubMedGoogle Scholar
  116. 113.
    Neidhardt, F. C., VanBogelen, R. A., and Vaughn, V., The genetics and regulation of the heat shock proteins. A. Rev. Genet.18 (1984) 295–329.CrossRefGoogle Scholar
  117. 114.
    Neurath, H., Evolution of proteolytic enzymes. Science224 (1984) 350–357.PubMedGoogle Scholar
  118. 115.
    Nishi, K., and Schnier, J., The phenotypic suppression of a mutation in the generplX for ribosomal protein L24 by mutations affecting the lon gene product for protease La inEscherichia coli K12. Molec. gen. Genet.212 (1988) 177–181.CrossRefPubMedGoogle Scholar
  119. 116.
    Nohmi, T., Battista, J. R., Dodson, L. A., and Walker, G. C., RecAmediated cleavage activates UmuD for mutagenesis: Mechanistic relationship between transcriptional derepression and posttranslational activation. Proc. natl Acad. sci. USA85 (1988) 1816–1820.PubMedGoogle Scholar
  120. 117.
    Novak, P., Ray, P. H., and Dev, I. K., Localization and purification of two enzymes fromEscherichia coli capable of hydrolyzing a signal peptide. J. biol. Chem.261 (1986) 420–427.PubMedGoogle Scholar
  121. 118.
    Olden, K., and Goldberg, A. L., Studies on the energy requirement for intracellular protein degradation inEscherichia coli. Biochim. biophys. Acta542 (1978) 385–598.Google Scholar
  122. 119.
    Oliver, D., Protein secretion inEscherichia coli. A. Rev. Microbiol.39, (1985) 615–648CrossRefGoogle Scholar
  123. 120.
    Orlowski, M., The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry29 (1990) 10289–10297.CrossRefPubMedGoogle Scholar
  124. 121.
    Pacaud, M., Sibilli L., and Le Bras, G., Protease I fromEscherichia coli. Eur. J. Biochem.69 (1976) 141–151.CrossRefPubMedGoogle Scholar
  125. 122.
    Pacaud, M., Protease II fromEscherichia coli: substrate specificity and kinetic properties. Eur. J. Biochem.82 (1978) 439–451.CrossRefPubMedGoogle Scholar
  126. 123.
    Pacaud, M., Purification and characterization of two novel proteolytic enzymes in membranes ofEscherichia coli. J. biol. Chem.257 (1982) 4333–4339PubMedGoogle Scholar
  127. 124.
    Pakula, A. A., Young, V. B., and Sauer, R. T., Bacteriophage λ Cro mutations: effects on activity and intracellular degradation. Proc. natl Acad. Sci. USA83 (1986) 8829–8833.PubMedGoogle Scholar
  128. 125.
    Palmer, S. M., and St, John, A. C., Characterization of a membraneassociated serine protease inEscherichia coli. J. Bact.169 (1987) 1474–1479.PubMedGoogle Scholar
  129. 126.
    Park, J. H., Lee, Y. S., Chung, C. H., and goldberg, A. L., Purification and characterization of protease Re, a cytoplasmic endoprotease inEscherichia coli. J. Bact.170 (1988) 921–926.PubMedGoogle Scholar
  130. 126a.
    Parsell, D. A., Sanchez, Y., Stitzel, J. D., and Lindquist, S., Hsp 104 is a highly conserved protein with two essential nucleotide-binding sites. Nature (London)353 (1991) 270–273.CrossRefGoogle Scholar
  131. 127.
    Parsell, D. A., and Sauer, R. T., The structural stability of a protein is an important determinant of its proteolytic susceptibility inE. coli. J. biol. Chem.264 (1989) 7590–7595.PubMedGoogle Scholar
  132. 128.
    Parsell, D. A., Silber, K. R., and Sauer, R. t., Carboxy-terminal determinants of intracellular protein degradation. Genes Devl.4 (1990) 277–286.Google Scholar
  133. 129.
    Pato, M. L., and Reich, C., Instability of transposase activity: evidence from bacteriophage Mu DNA replication. Cell29 (1982) 219–225.CrossRefPubMedGoogle Scholar
  134. 130.
    Pelham, H. R. B., Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell46 (1986) 959–961.CrossRefPubMedGoogle Scholar
  135. 131.
    Perry, K. L., Elledge, S. J., Mitchell, B. B., Marsh, L., and Walker, G. C.,mucDC andmucAB operons whose products are required for UV light-and chemical-induced mutagenesis: umuD, MucA, and LexA proteins share homology. Proc. natl Acad. Sci. USA82 (1985) 4331–4335.PubMedGoogle Scholar
  136. 132.
    Peterson, K. R., Wertman, K. F., Mount, D. W., and Marinus, M. G., Viability ofEscherichia coli K-12 DNA adenine methylase (S) mutants requires increased expression of specific genes in the SOS regulon. Molec. gen. Genet.201 (1985) 14–19.CrossRefPubMedGoogle Scholar
  137. 133.
    Phillips, T. A., VanBogelen, R. A., and Neidhardt, F. C.,lon gene product ofEscherichia coli is a heat shock protein. J. Bact.159 (1984) 283–287.PubMedGoogle Scholar
  138. 134.
    Pine, M. J., Response of intracellular proteolysis to alteration of bacterial protein and the implications in metabolic regulation. J. Bact.93 (1967) 1527–1533.PubMedGoogle Scholar
  139. 135.
    Pine, M. J., Steady-state measurements of the turnover of amino acid in the cellular protein of growingEscherichia coli: existence of two kinetically distinct reactions. J. Bact.103 (1970) 207–215.PubMedGoogle Scholar
  140. 136.
    Pine, M. J., Regulation of intracellular proteolysis inEscherichia coli. J. Bact.115 (1973) 1097–1116.Google Scholar
  141. 137.
    Platt, T., Miller, J. H., and Weber, K., In vivo degradation of mutantlac repressor. Nature (London)228 (1970) 1154–1156.Google Scholar
  142. 138.
    Rawlings, N. D., and Barrett, A. J., Homologues of insulinase, a new superfamily of metallopeptidases. Biochem. J.274 (1991) in press.Google Scholar
  143. 139.
    Rechsteiner, M., Ubiquitin-mediated pathways for intracellular proteolysis. A. Rev. Cell Biol.3 (1987) 1–30.Google Scholar
  144. 139a.
    Regnier, P. The purification of protease IV and the demonstration that it is a proteolytic enzyme. biochem. biophys. Res. Commun.99 (1981) 1369–1376.CrossRefPubMedGoogle Scholar
  145. 140.
    Reiss, Y., Kaim, D., and Hershko, A., Specificity of binding of NH2-terminal residue of proteins to Ubiquitin-protein ligase. J. biol. Chem.263 (1988) 2693–2698.PubMedGoogle Scholar
  146. 141.
    Rivett, A. J., The multicatalytic proteinase of mammalian cells. Archs Biochem. Biophys.268 (1989) 1–8CrossRefGoogle Scholar
  147. 142.
    Roberts, J. W., and Roberts, C. W., Proteolytic cleavage of bacteriophage lanbda repressor in induction. Proc. natl Acad. Sci. USA72 (1975) 147–151.PubMedGoogle Scholar
  148. 143.
    Roland, K., and Little, J. W., Reaction of LexA repressor with diisopropylfluoro phosphate: a test of the serine protease model. J. biol. Chem.265 (1990) 12828–12835.PubMedGoogle Scholar
  149. 144.
    Roseman, J. E., and Levine, R. L., Purification of a protease fromEscherichia coli with specificity for oxidized glutamine synthetase. J. biol. Chem.262 (1987) 2101–2110.PubMedGoogle Scholar
  150. 145.
    Rupprecht, K. R., and Markovitz, A., Conservation ofcapR (lon) DNA ofEscherichia coli K-12 between distantly related species. J. Bact.155 (1983) 910–914.PubMedGoogle Scholar
  151. 146.
    Schroer, D. W., and St. John, A. C., Relative stability of membrane proteins inEscherichia coli. J. Bact.146 (1981) 476–483.PubMedGoogle Scholar
  152. 147.
    Sedgwick, B., in vitro proteolytic cleavage of theEscherichia coli Ada protein by theompT gene product. J. Bact.171 (1989) 2249–2251.PubMedGoogle Scholar
  153. 148.
    Shinagawa, H., Iwasaki, H., Kato, T., and Nakata, A., RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc. natl Acad. Sci. USA85 (1988) 1806–1810.PubMedGoogle Scholar
  154. 149.
    Shineberg, B., and Zipser, D., Thelon gene and degradation of β-galactosidase nonsense fragments. J. Bact.116 (1973) 1469–1471.PubMedGoogle Scholar
  155. 150.
    Simon, L. D., Tomczak, K., and St. John, A. C., Bacteriophages inhibit degradation of abnormal proteins inE coli. Nature275 (1978) 424–428.Google Scholar
  156. 151.
    Skorupski, K., Tomaschewski, J., Ruger, W., and Simon, L. D., A bacteriophage T4 gene which functions to inhibitEscherichia coli Lon protease. J. Bact.170 (1988) 3016–3024.PubMedGoogle Scholar
  157. 152.
    Skowyra, D., Georgopoulos, C., and Zylicz, M., TheE. coli dnaK gene product, the hsp 70 homologg, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell62 (1990) 939–944.CrossRefPubMedGoogle Scholar
  158. 153.
    Slavicek, J. M., Jones, N. C., and Richter, J. D., Rapid turnover of adenovirus E1A is determined through a co-translational mechanism that requires an aminoterminal domain. EMBO J.7 (1988) 171–180Google Scholar
  159. 154.
    Slilaty, S. N., and Little, J. W., Lysine-156 and serine-119 are required for LexA repressor cleavage: A possible mechanism. Proc. natl Acad. Sci. USA84 (1987) 3987–3991.PubMedGoogle Scholar
  160. 154a.
    Squires, C. L., Pedersen, S., Ross, B. M., and Squires, C., ClpB is theEscherichia coli heat shock protein F84.1. J. Bact.173 (1991) 4254–4262.PubMedGoogle Scholar
  161. 154b.
    Squires, C. L., and Squires, C., The Clp proteins-proteolysis regulators or molecular chaperones? J. Bact.174 (1992) in press.Google Scholar
  162. 155.
    St. John, A. C., and Goldberg, A. L., Effects of reduced energy production on protein degradation, guanosine tetraphosphate, and RNA synthesis inEscherichia coli. J. biol. Chem.253 (1978) 2705–2711.PubMedGoogle Scholar
  163. 156.
    St. John, A. C., and Goldberg, A. L., Effects of starvation for potassium and other inorganic ions on protein degradation and ribonucleic acid synthesis inEscherichia coli. J. Bact.143 (1978) 1223–1233.Google Scholar
  164. 157.
    St. John, A. C., Jakubas, K., and Beim, D., Degradation of proteins in steady-state cultures ofEscherichia coli. Biochim. biophys. Acta586 (1979) 537–544.PubMedGoogle Scholar
  165. 158.
    Stout, V., Torres-Cabassa, A., Maurizi, M. R., Gutnick, D., and Gottesman, S., RcsA, an unstable regulator of capsular polysaccharide synthesis. J. Bact.173 (1991) 1738–1747PubMedGoogle Scholar
  166. 159.
    Strauch, K., Johnson, K., and Beckwith, J., Characterization ofdegP, a gene required for proteolysis in the cell envelope and essential for growth ofEscherichia coli at high temperature. J. Bact.171 (1989) 2689–2696.PubMedGoogle Scholar
  167. 160.
    Strauch, K. L., and Beckwith, J., AnEscherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. natl Acad. Sci. USA85 (1988) 1576–1580.PubMedGoogle Scholar
  168. 161.
    Straus, D. B., Walter, W. A., and Gross, C. A., The heat shock response ofE. coli is regulated by changes in the concentration of sigma 32. Nature (London)329 (1987) 348–391.CrossRefGoogle Scholar
  169. 162.
    Straus, D. B., Walter, W. A., and Gross, C. A.,Escherichia coli heat shock gene mutants are defective in proteolysis. Genes Devl.2 (1988) 1851–1858.Google Scholar
  170. 163.
    Straus, D. B., Walter, W., and Gross, C. A., DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of σ32. Genes Devl.4 (1990) 2202–2209.Google Scholar
  171. 164.
    Strongin, A. Y., Gorodetsky, D. I., and Stepanov, V. M., The study ofEscherichia coli proteases. Intracellular serine protease ofE. coli — an analog ofBacillus proteases. J. gen. Microbiol.110 (1979) 443–451.PubMedGoogle Scholar
  172. 165.
    Sugimura, K., and Nishihara, T., Purification, characterization, and primary structure ofEscherichia coli protease VII with specificity for paired basic residues: identity of protease VII and OmpT. J. Bact.170 (1988) 5625–5632.PubMedGoogle Scholar
  173. 166.
    Swamy, K. H. S., Chung, C. H., and Goldberg, A. L., Isolation and characterization of protease Do fromEscherichia coli, a large serine protease containing multiple subunits. Archs Biochem. Biophys.224 (1983) 543–554CrossRefGoogle Scholar
  174. 167.
    Tilly, K., Spence, J., and Georgopoulos, C., Modulation of stability of theEscherichia coli Heat Shock Regulatory Factor sigma 32, J. Bact.171 (1989) 1585–1589.PubMedGoogle Scholar
  175. 168.
    Torres-Cabassa, A. S., and Gottesman, S., Capsule synthesis inEscherichia coli K-12 is regulated by proteolysis. J. Bact.169 (1987) 981–989.PubMedGoogle Scholar
  176. 169.
    Trempy, J. E., and Gottesman, S., Alp: A suppressor of Lon protease mutants inEscherichia coli. J. Bact.171 (1989) 3348–3353.PubMedGoogle Scholar
  177. 170.
    Tokunaga, M., Loranger, J. M., Wolfe, P. B., and Wu, H. C., Prolipoprotein signal peptidase inEscherichia coli is distinct from the M13 precoat protein signal peptidase. J. biol. Chem.257 (1982) 9922–9925.PubMedGoogle Scholar
  178. 171.
    Tokunaga, M., Loranger, J. M., Chang, S. Y., Regue, M., Chang, S., and Wu, H. C., Identification of prolipoprotein signal peptidase and genomic organization of the Isp gene inEscherichia coli. J. biol. Chem.260 (1985) 5610–5616.PubMedGoogle Scholar
  179. 172.
    Tokunaga, M., Tokunaga, H., and Wu, H. C., Post-translational modification and processing ofEscherichia coli prolipoprotein in vitro. Proc. natl. Acad. Sci. USA79 (1982) 2255–2259.PubMedGoogle Scholar
  180. 173.
    Vaithilingam, I., and Cook, R. A., High-molecular-mass proteases (possibly proteasomes) inEscherichia coli K12. Biochem. Int.19 (1989) 1297–1307.PubMedGoogle Scholar
  181. 174.
    Walker, G. C., The SOS Response ofEscherichia coli, in:Escherichia coll andSalmonella typhimurium: Cellular and Molecular Biology pp. 41346–1357. Eds F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger, American Society for Microbiology. Washington, D.C. 1987.Google Scholar
  182. 175.
    Waxman, L., and Goldberg, A. L., Protease La fromEscherichia coli hydrolyzes ATP and proteins in a linked fashion. Proc. natl Acad. Sci. USA79 (1982) 4883–4887.PubMedGoogle Scholar
  183. 176.
    Waxman, L., and Goldberg, A. L., Protease La, thelon gene product, cleaves specific fluorogenic peptides in an ATP-dependent reaction. J. biol. Chem.260 (1985) 12022–12028.PubMedGoogle Scholar
  184. 177.
    Waxman, L., and Goldberg, A. L., Selectivity of intracellular proteolysis: protein substrates activate the ATP-dependent protease (La). Science232 (1986) 500–503.PubMedGoogle Scholar
  185. 178.
    Wolfe, P. B., Silver, P., and Wickner, W., The isolation of homogeneous leader peptidase from a strain ofEscherichia coli which overproduces the enzyme. J. biol. Chem.257 (1982) 7898–7902.PubMedGoogle Scholar
  186. 179.
    Woo, K. M., Chung, W. J., Ha, D. B., Goldberg, A. L., and Chung, C. H., Protease Ti fromEscherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides. J. biol. Chem.264 (1989) 2088–2091.PubMedGoogle Scholar
  187. 180.
    Yen, C., Green, L., and Miller, C. G., Degradation of intracellular protein inSalmonella typhimurium peptidase mutants. J. molec. Biol.143 (1980) 21–33.CrossRefPubMedGoogle Scholar
  188. 181.
    Zehnbauer, B. A., Foley, E. C., Henderson, G. W., and Markovitz, A., Identification and purification of thelon + (capR+) gene product, a DNA-binding protein. Proc. natl Acad. Sci. USA78 (1981) 2043–2047.PubMedGoogle Scholar
  189. 182.
    Zwizinski, C., and Wickner, W., Purification and characterization of leader (signal) peptidase fromEscherichia coli. J. biol. Chem.255 (1980) 7973–7977.PubMedGoogle Scholar
  190. 183.
    Zwizinski, C., Date, T. and Wickner, W., Leader peptidase is found in both the inner and outer membranes ofEscherichia coli. J. biol. Chem.256 (1981) 3593–3597.PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag 1992

Authors and Affiliations

  • M. R. Maurizi
    • 1
  1. 1.Laboratory of Cell BiologyNational Cancer InstituteBethesdaUSA

Personalised recommendations