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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
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.
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.
Bachmair, A., and Varshavsky, A., The degradation signal in a short-lived protein. Cell56 (1989) 1019–1032.
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.
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.
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.
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.
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.
Bond, J. S., and Butler, P. E., Intracellular proteases. A. Rev. Biochem.56 (1987) 333–364.
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.
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.
Bukhari, A. I., and Zipser, D., Mutants ofEscherichia coli with a defect in the degradation of nonsense fragments. Nature243 (1973) 238–241.
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.
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.
Caron, P. R., and Grossman, L., Potential role of proteolysis in the control of UvrABC incision. Nucl. Acids Res.16 (1988) 10903–10912.
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.
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.
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.
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.
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.
Cheng, Y. S., and Zipser, D., Purification and characterization of protease III fromEscherichia coli. J. biol. Chem.254 (1979) 4698–4706.
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.
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.
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.
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.
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.
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.
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.
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.
Davies, K. J. A., and Lin, S. W., Degradation of oxidatively denatured protein inEscherichia coli. Free Radic. Biol. Med.5 (1988) 215–223.
Dennis, P. P., Synthesis and stability of individual ribosomal proteins in the presence of rifampicin. Mol. gen. Genet.134 (1974) 39–47.
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.
Dervyn, E., Canceill, D., and Huisman, O., Saturation and specificity of the Lon protease ofEscherichia coli. J. Bact.172 (1990) 7098–7103.
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.
Donch, J., and Greenberg, J., Genetic analysis oflon mutants of strain K-12 ofEscherichia coli. Mol. gen. Genet.103 (1968) 105–115.
Downs, D., Waxman, L., Goldberg, A. L., and Roth, J., Isolation and characterization oflon mutants inSalmonella typhimurium. J. Bact.167 (1986) 193–197.40.
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.
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.
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.
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.
Finley, D., Ciechanover, A., and Varshavsky, A., Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutantts85. Cell37 (1984) 43–55.
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.
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.
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.
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.
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.
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.
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.
Goldberg, A. L., Degradation of abnormal proteins inEscherichia coli. Proc. natl Acad. Sci. USA69 (1972) 422–426.
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.
Goldberg, A. L., Streedhara Swamy, K. H., Chung, C. H., and Larimore, F. S., Proteases ofEscherichia coli. Meth. Enzym.80 (1983) 680–702.
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.
Goldschmidt, R., In vivo degradation of nonsense fragements inE. coli. Nature (London)228 (1970) 1151–1154.
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.
Gottesman, S., Genetics of proteolysis inEscherichia coli. A. Rev. Genet.23 (1989) 163–198.
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.
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.
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.
Gottesman, S., and Zipser, D., The Deg phenotype ofEscherichia coli lon mutants. J. Bact.133 (1978) 844–851.
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.
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) 151–159
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.
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.
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.
Hershko, A., Ubiquitin-mediated protein degradation. J. biol. Chem.263 (1990) 15237–15240
Holck, A., and Kleppe, K., Cloning and sequence of the gene for the DNA-binding 17K protein ofEscherichia coli. Gene67 (1988) 117–124.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Katayama-Fujimura, Y., Gottesman, S., and Maurizi, M. R., a multiple-component, ATP-dependent protease fromEscherichia coli. J. biol. Chem.262 (1987) 4477–4485.
Keller, J. A., and Simon, L. D., Divergent effects of adnaK mutation on abnormal protein degradation inEscherichia coli. Molec. Microbiol.2 (1988) 31–41.
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.
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).
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.
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.
Lazarides, E., and Moon, R. T., Assembly and topogenesis of the spectrin-based membrane skeleton in erythroid development. Cell37 (1984) 354–356.
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.
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.
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.
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.
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.
Little, J. W., Autodigestion of LexA and phage lambda repressors. Proc. natl Acad. Sci. USA81 (1984) 1375–1379.
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.
Little, J. W., and Mount, D. W., The SOS regulatory system ofEscherichia coli. Cell29 (1982) 11–22.
Mandelstam, J., Turnover of protein in growing and nongrowing population ofEscherichia coli. Biochem. J.169 (1958) 110–119.
Maurizi, M. R., Degradation in vitro of bacteriophage lambda N protein by Lon protease fromEscherichia coli. J. biol. Chem.262 (1987) 2696–2703.
Maurizi, M. R., ATP-promoted interaction between ClpA and ClpP in activation of Clp protease fromEscherichia coli. Biochem. Soc. Trans. (1991) in press.
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.
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.
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.
Maurizi, M. R., and Switzer, R. L., Proteolysis in bacterial sporulation. Curr. Top. Cell Regul.16 (1979) 163–224.
Maurizi, M. R., Trisler, P., and Gottesman, S., Insecrtional mutagenesis of thelon gene inEscherichia coli: lon is dispensable. J. Bact.164 (1985) 1124–1135.
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.
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.
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.
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.
Michaelis, S., and Beckwith, J., Mechanism of incorporation of cell envelop proteins inEscherichia coli. A. Rev. Microbiol.36 (1982) 435–465.
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.
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.
Miller, C. G., and Schwartz, G., Peptidase-deficient mutants ofEscherichia coli. J. Bact.135 (1978) 603–611.
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.
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.
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.
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.
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.
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.
Neurath, H., Evolution of proteolytic enzymes. Science224 (1984) 350–357.
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.
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.
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.
Olden, K., and Goldberg, A. L., Studies on the energy requirement for intracellular protein degradation inEscherichia coli. Biochim. biophys. Acta542 (1978) 385–598.
Oliver, D., Protein secretion inEscherichia coli. A. Rev. Microbiol.39, (1985) 615–648
Orlowski, M., The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry29 (1990) 10289–10297.
Pacaud, M., Sibilli L., and Le Bras, G., Protease I fromEscherichia coli. Eur. J. Biochem.69 (1976) 141–151.
Pacaud, M., Protease II fromEscherichia coli: substrate specificity and kinetic properties. Eur. J. Biochem.82 (1978) 439–451.
Pacaud, M., Purification and characterization of two novel proteolytic enzymes in membranes ofEscherichia coli. J. biol. Chem.257 (1982) 4333–4339
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.
Palmer, S. M., and St, John, A. C., Characterization of a membraneassociated serine protease inEscherichia coli. J. Bact.169 (1987) 1474–1479.
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.
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.
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.
Parsell, D. A., Silber, K. R., and Sauer, R. t., Carboxy-terminal determinants of intracellular protein degradation. Genes Devl.4 (1990) 277–286.
Pato, M. L., and Reich, C., Instability of transposase activity: evidence from bacteriophage Mu DNA replication. Cell29 (1982) 219–225.
Pelham, H. R. B., Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell46 (1986) 959–961.
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.
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.
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.
Pine, M. J., Response of intracellular proteolysis to alteration of bacterial protein and the implications in metabolic regulation. J. Bact.93 (1967) 1527–1533.
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.
Pine, M. J., Regulation of intracellular proteolysis inEscherichia coli. J. Bact.115 (1973) 1097–1116.
Platt, T., Miller, J. H., and Weber, K., In vivo degradation of mutantlac repressor. Nature (London)228 (1970) 1154–1156.
Rawlings, N. D., and Barrett, A. J., Homologues of insulinase, a new superfamily of metallopeptidases. Biochem. J.274 (1991) in press.
Rechsteiner, M., Ubiquitin-mediated pathways for intracellular proteolysis. A. Rev. Cell Biol.3 (1987) 1–30.
Regnier, P. The purification of protease IV and the demonstration that it is a proteolytic enzyme. biochem. biophys. Res. Commun.99 (1981) 1369–1376.
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.
Rivett, A. J., The multicatalytic proteinase of mammalian cells. Archs Biochem. Biophys.268 (1989) 1–8
Roberts, J. W., and Roberts, C. W., Proteolytic cleavage of bacteriophage lanbda repressor in induction. Proc. natl Acad. Sci. USA72 (1975) 147–151.
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.
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.
Rupprecht, K. R., and Markovitz, A., Conservation ofcapR (lon) DNA ofEscherichia coli K-12 between distantly related species. J. Bact.155 (1983) 910–914.
Schroer, D. W., and St. John, A. C., Relative stability of membrane proteins inEscherichia coli. J. Bact.146 (1981) 476–483.
Sedgwick, B., in vitro proteolytic cleavage of theEscherichia coli Ada protein by theompT gene product. J. Bact.171 (1989) 2249–2251.
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.
Shineberg, B., and Zipser, D., Thelon gene and degradation of β-galactosidase nonsense fragments. J. Bact.116 (1973) 1469–1471.
Simon, L. D., Tomczak, K., and St. John, A. C., Bacteriophages inhibit degradation of abnormal proteins inE coli. Nature275 (1978) 424–428.
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.
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.
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) 171–180
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.
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.
Squires, C. L., and Squires, C., The Clp proteins-proteolysis regulators or molecular chaperones? J. Bact.174 (1992) in press.
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.
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.
St. John, A. C., Jakubas, K., and Beim, D., Degradation of proteins in steady-state cultures ofEscherichia coli. Biochim. biophys. Acta586 (1979) 537–544.
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) 1738–1747
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.
Strauch, K. L., and Beckwith, J., AnEscherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. natl Acad. Sci. USA85 (1988) 1576–1580.
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.
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.
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.
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.
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.
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) 543–554
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.
Torres-Cabassa, A. S., and Gottesman, S., Capsule synthesis inEscherichia coli K-12 is regulated by proteolysis. J. Bact.169 (1987) 981–989.
Trempy, J. E., and Gottesman, S., Alp: A suppressor of Lon protease mutants inEscherichia coli. J. Bact.171 (1989) 3348–3353.
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.
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.
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.
Vaithilingam, I., and Cook, R. A., High-molecular-mass proteases (possibly proteasomes) inEscherichia coli K12. Biochem. Int.19 (1989) 1297–1307.
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.
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.
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.
Waxman, L., and Goldberg, A. L., Selectivity of intracellular proteolysis: protein substrates activate the ATP-dependent protease (La). Science232 (1986) 500–503.
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.
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.
Yen, C., Green, L., and Miller, C. G., Degradation of intracellular protein inSalmonella typhimurium peptidase mutants. J. molec. Biol.143 (1980) 21–33.
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.
Zwizinski, C., and Wickner, W., Purification and characterization of leader (signal) peptidase fromEscherichia coli. J. biol. Chem.255 (1980) 7973–7977.
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.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Maurizi, M.R. Proteases and protein degradation in Escherichia coli. Experientia 48, 178–201 (1992). https://doi.org/10.1007/BF01923511
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01923511