Chapter 9 : Periplasmic Proteases and Protease Inhibitors

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Periplasmic Proteases and Protease Inhibitors, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815806/9781555813987_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555815806/9781555813987_Chap09-2.gif


In general, proteases are involved in diverse functions; the most notable include digestive, protective, and regulatory processes. Digestive proteases are involved in protein degradation for nutritional purposes. About 35% of all entries in the MEROPS database are classified as serine proteases. Two other periplasmic serine proteases containing PDZ domains, DegP and DegQ, are also part of this family. Buchanan and Sowell recognized a considerable rise in expression level of PBP6 in stationary- phase cells compared with exponentially growing cells . While sbmC is a stationary-phase-induced SOS gene involved in MccB17 susceptibility, sbcB encodes for exonuclease I. PBP6b has a molecular mass of 43 kDa and was classified as belonging to the family S11 (clan SE) because it shares several molecular features of this group. The 50 families and 16 clans of metalloproteases recognized to date indicate that they are the most diverse of the four main types of proteases. For the peptidases discussed in this chapter there are two relevant mechanisms of catalysis. The first mechanism involves the catalytic His His Glu/Asp sites for zinc binding. Structural and kinetic studies allow proposing the following mechanism for CPD A. This chapter provides a summary of the information available for pitrilysin, MepA, alkaline phosphatase iso-zyme conversion protein, YebA, YfgC, and YhjT. The chapter talks about cysteine proteases, Proteases of unknown classification, and protease inhibitor.

Citation: Nicolette K, Michael M, Michael E. 2007. Periplasmic Proteases and Protease Inhibitors, p 150-170. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch9
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Affholter, J. A.,, V. A. Fried, and, R.A. Roth. 1988. Human insulin-degrading enzyme shares structural and functional homologies with E. coli protease III. Science 242: 14151418.
2. Amanuma, H., and, J. L. Strominger. 1980. Purification and properties of penicillin-binding proteins 5 and 6 from Escherichia coli membranes. J. Biol. Chem. 255: 1117311180.
3. Anantharaman, V., and, L. Aravind. 2003. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4: R11.
4. Anastasi, A., and, A. J. Barrett. 1995. Pitrilysin. Methods Enzymol. 248: 684692.
5. Anastasi, A.,, C. G. Knight, and, A. J. Barrett. 1993. Characterization of the bacterial metalloendopepti-dase pitrilysin by use of a continuous fluorescence assay. Biochem. J. 290: 601607.
6. Asboth, B.,, E. Stokum,, I. U. Khan, and, L. Pol-gar. 1985. Mechanism of action of cysteine pro-teinases: oxyanion binding site is not essential in the hydrolysis of specific substrates. Biochemistry 24: 606609.
7. Auld, D. S., 1987. Acyl group transfer—metallopro—teinases, p. 241258. In M. I. Page., and, A. Williams (ed.) Enzyme Mechanisms. Royal Society of Chemistry, London, United Kingdom.
8. Auld, D. S., 1997. Zinc catalysis in metalloproteases. Struct. Bonding (Berlin) 89: 2950.
9. Authier, F.,, J. J. Bergeron,, W. J. Ou,, R. A. Rachu-binski,, B. I. Posner, and, P. A. Walton. 1995. Degradation of the cleaved leader peptide of thio-lase by a peroxisomal proteinase. Proc. Natl. Acad. Sci. USA 92: 38593863.
10. Baneyx, F., and, G. Georgiou. 1991. Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecular-weight substrates in vivo. J. Bacteriol. 173: 26962703.
11. Baquero, M. R.,, M. Bouzon,, J. C. Quintela,, J. A. Ayala, and, F. Moreno. 1996. dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with DD-carboxypeptidase activity. J. Bacteriol. 178: 71067111.
12. Baquero, M. R.,, M. Bouzon,, J. Varea, and, F. Moreno. 1995. sbmC, a stationary-phase induced SOS Escherichia coli gene, whose product protects cells from the DNA replication inhibitor microcin B17. Mol. Microbiol. 18: 301311.
13. Barrett, A. J.,, N. D. Rawlings, and, J. F. Woessner. 2004. Handbook of Proteolytic Enzymes. Elsevier, London, United Kingdom.
14. Bass, S.,, Q. Gu, and, A. Christen. 1996. Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated R1pA. J. Bacteriol. 178: 11541161.
15. Baumeister, H.,, D. Müller,, M. Rehbein, and, D. Richter. 1993. The rat insulin-degrading enzyme. Molecular cloning and characterization of tissue-specific transcripts. FEBS Lett. 317: 250254.
16. Becker, A. B., and, R. A. Roth. 1992. An unusual active site identified in a family of zinc metalloen-dopeptidases. Proc. Natl. Acad. Sci. USA 89: 38353839.
17. Betton, J.-M.,, N. Sassoon,, M. Hofnung, and, M. Laurent. 1998. Degradation versus aggregation of misfolded maltose-binding protein in the peri-plasm of Escherichia coli. J. Biol. Chem. 273: 88978902.
18. Bode, W.,, F. X. Gomis-Ruth, and, W. Stocker. 1993. Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett. 331: 134140.
19. Broome-Smith, J. K., 1985. Construction of a mutant of Escherichia coli that has deletions of both the penicillin-binding protein 5 and 6 genes. J. Gen. Microbiol. 131: 21152118.
20. Broome-Smith, J. K.,, I. Ioannidis,, A. Edelman, and, B. G. Spratt. 1988. Nucleotide sequences of the penicillin-binding protein 5 and 6 genes of Es-cherichia coli. Nucleic Acids Res. 16: 1617.
21. Buchanan, C. E., and, M. O. Sowell. 1982. Synthesis of penicillin-binding protein 6 by stationary-phase Escherichia coli.J. Bacteriol. 151: 491494.
22. Buelow, D. R., and, T. L. Raivio. 2005. Cpx signal transduction is influenced by a conserved N-termi-nal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J. Bacteriol. 187: 66226630.
23. Chen, C.,, B. Snedecor,, J. C. Nishihara,, J. C. Joly,, N. McFarland,, D. C. Andersen,, J. E. Battersby, and, K. M. Champion. 2004. High-level accumulation of a recombinant antibody fragment in the periplasm of Escherichia coli requires a triple-mutant (degP prc spr) host strain. Biotechnol. Bioeng. 85: 463474.
24. Cheng, Y. S., and, D. Zipser. 1979. Purification and characterization of protease III from Escherichia coli. J. Biol. Chem. 254: 46984706.
25. Christianson, D. W., and, W. N. Lipscomb. 1989. Carboxypeptidase A. Acc. Chem. Res. 22: 6269.
26. Clausen, T.,, C. Southan, and, M. Ehrmann. 2002. The HtrA family of proteases. Implications for protein composition and cell fate. Mol. Cell 10: 443455.
27. Cornista, J.,, S. Ikeuchi,, M. Haruki,, A. Kohara,, K. Takano,, M. Morikawa, and, S. Kanaya. 2004. Cleavage of various peptides with pitrilysin from Escherichia coli: kinetic analyses using beta-endor-phin and its derivatives. Biosci. Biotechnol. Biochem. 68: 21282137.
28. Davies, C.,, S. W. White, and, R. A. Nicholas. 2001. Crystal structure of a deacylation-defective mutant of penicillin-binding protein 5 at 2.3-A resolution. J. Biol. Chem. 276: 616623.
29. Denome, S. A.,, P. K. Elf,, T. A. Henderson,, D. E. Nelson, and, K. D. Young. 1999. Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J. Bacteriol. 181: 39813993.
30. Ding, L.,, A. B. Becker,, A. Suzuki, and, R. A. Roth. 1992. Comparison of the enzymatic and biochemical properties of human insulin-degrading enzyme and Escherichia coli protease III. J. Biol. Chem. 267: 24142420.
31. Dodson, G., and, A. Wlodawer. 1998. Catalytic triads and their relatives. Trends Biochem. Sci. 23: 347352.
32. Drenth, J.,, J. N. Jansonius,, R. Koekoek, and, B. G. Wolthers. 1971a. Papain X-ray structure, p. 485499. In P. D. Boyer (ed.), The Enzymes, vol., 3. Academic Press, New York, N.Y.
33. Drenth, J.,, J. N. Jansonius,, R. Koekoek, and, B. G. Wolthers. 1971b. The structure of papain. Adv. Protein Chem. 25: 79115.
34. Dykstra, C. C.,, D. Prasher, and, S. R. Kushner. 1984. Physical and biochemical analysis of the cloned recB and recC genes of Escherichia coli K-12. J. Bacteriol. 157: 2127.
35. Edwards, D., and, W. Donachie. 1993. Construction of a triple deletion of penicillin-binding proteins 4, 5 and 6 in Escherichia coli, p. 369374. In M. de Pedro,, J.-V. Holttje, and, W. Loffelhardt (ed.), Bacterial Growth and Lysis. Plenum Press, NewYork, N.Y.
36. Eggers, C. T.,, I. A. Murray,, V. A. Delmar,, A. G. Day, and, C. S. Craik. 2004. The periplasmic ser-ine protease inhibitor ecotin protects bacteria against neutrophil elastase. Biochem. J. 379: 107118.
37. Ehrmann, M., and, T. Clausen. 2004. Proteolysis as a regulatory mechanism. Annu. Rev. Genet. 38: 709724.
38. Fanning, A. S., and, J. M. Anderson. 1996. Protein-protein interactions: PDZ domain networks. Curr. Biol 6: 13851388.
39. Fundoiano-Hershcovitz, Y.,, L. Rabinovitch,, Y. Langut,, V. Reiland,, G. Shoham, and, Y. Shoham. 2004. Identification of the catalytic residues in the double-zinc aminopeptidase from Streptomyces griseus. FEBS Lett. 571: 192196.
40. Gehm, B. D.,, W. L. Kuo,, R. K. Perlman, and, M. R. Rosner. 1993. Mutations in a zinc-binding domain of human insulin-degrading enzyme eliminate catalytic activity but not insulin binding. J. Biol. Chem. 268: 79437948.
41. Georgopapadakou, N. H.,, S. A. Smith,, C. M. Cimarusti, and, R. B. Sykes. 1983. Binding of monobactams to penicillin-binding proteins of Escherichia coli and Staphylococcus aureus: relation to antibacterial activity. Antimicrob. Agents Chemother. 23: 98104.
42. Ghuysen, J. M., 1991. Serine beta-lactamases and penicillin-binding proteins. Annu. Rev. Microbiol. 45: 3767.
43. Ghuysen, J. M., 1994. Molecular structures of penicillin-binding proteins and beta-lactamases. Trends Microbiol. 2: 372380.
44. Goffin, C., and, J. M. Ghuysen. 1998. Multimodu-lar penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62: 10791093.
45. Gottesman, S., 2003. Proteolysis in bacterial regulatory circuits .Annu. Rev. Cell. Dev. Biol. 19: 565587.
46. Granier, B.,, C. Duez,, S. Lepage,, S. Englebert,, J. Dusart,, O. Dideberg,, J. Van Beeumen,, J. M. Frere, and, J. M. Ghuysen. 1992. Primary and predicted secondary structures of the Actinomadura R39 extracellular DD-peptidase, a penicillin-binding protein (PBP) related to the Escherichia coli PBP4. Biochem.J. 282(Pt 3) :781788.
47. Guinand, M., 2004. Dipeptidyl-peptidase VI, p. 13991401. In A. J. Barrett,, N. D. Rawlings, and, J. F. Woessner (ed.), Handbook of Proteolytic Enzymes. Elsevier, London, United Kingdom.
48. Guinand, M.,, G. Michel, and, D. J. Tipper. 1974. Appearance of gamma-D-glutamyl-(L) meso-diaminopimealate peptidoglycan hydrolase during sporulation in Bacillus sphaericus. J. Bacteriol. 120: 173184.
49. Hara, H.,, Y. Yamamoto,, A. Higashitani,, H. Suzuki, and, Y. Nishimura. 1991. Cloning, mapping, and characterization of the Escherichia coli prc gene, which is involved in C-terminal processing of penicillin-binding protein 3. J. Bacteriol. 173: 47994813.
50. Harris, F.,, K. Brandenburg,, U. Seydel, and, D. Phoenix. 2002. Investigations into the mechanisms used by the C-terminal anchors of Escherichia coli penicillin-binding proteins 4, 5, 6 and 6b for membrane interaction. Eur. J. Biochem. 269: 58215829.
51. Harris, F.,, R. Demel,, B. de Kruijff, and, D. A. Phoenix. 1998. An investigation into the lipid interactions of peptides corresponding to the C-terminal anchoring domains of Escherichia coli penicillin-binding proteins 4, 5 and 6. Biochim. Biophys. Acta 1415: 1022.
52. Hedstrom, L., 2002. Serine protease mechanism and specificity. Chem. Rev. 102: 45014524.
53. Henderson, T. A.,, P. M. Dombrosky, and, K. D. Young. 1994. Artifactual processing of penicillin-binding proteins 7 and 1b by the OmpT protease of Escherichia coli. J. Bacteriol. 176: 256259.
54. Henderson, T. A.,, M. Templin, and, K. D. Young. 1995. Identification and cloning of the gene encoding penicillin-binding protein 7 of Escherichia coli. J. Bacteriol. 177: 20742079.
55. Henderson, T. A.,, K. D. Young,, S. A. Denome, and, P. K. Elf. 1997. AmpC and AmpH, proteins related to the class C beta-lactamases, bind penicillin and contribute to the normal morphology of Escherichia coli. J. Bacteriol. 179: 61126121.
56. Hiniker, A., and, J. C. Bardwell. 2004. In vivo substrate specificity of periplasmic disulfide oxidore-ductases. J. Biol. Chem. 279: 1296712973.
57. Holtje, J. V., 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62: 181203.
58. Isaac, D. D.,, J. S. Pinkner,, S. J. Hultgren, and, T. J. Silhavy. 2005. The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. P->roc. Natl. Acad. Sci. USA 102: 1777517779.
59. Ishino, Y.,, H. Shinagawa,, K. Makino,, M. Ame-mura, and, A. Nakata. 1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bac-teriol. 169: 54295433.
60. Jackson, M. E., and, J. M. Pratt. 1987. An 18 amino acid amphiphilic helix forms the membrane-anchoring domain of the Escherichia coli penicillin-binding protein 5. Mol. Microbiol. 1: 2328.
61. Jackson, M. E., and, J. M. Pratt. 1988. Analysis of the membrane-binding domain of penicillin-binding protein 5 of Escherichia coli. Mol. Microbiol. 2: 563568.
62. Johnson, K.,, I. Charles,, G. Dougan,, D. Pickard,, P. O’Gaora,, G. Costa,, T. Ali,, I. Miller, and, C. Hormaeche. 1991. The role of a stress-response protein in Salmonella typhimurium virulence. Mol. Microbiol. 5: 401407.
63. Joris, B.,, J. M. Ghuysen,, G. Dive,, A. Renard,, O. Dideberg,, P. Charlier,, J. M. Frere,, J. A. Kelly,, J. C. Boyington, and, P. C. Moews. 1988. The active-site-serine penicillin-recognizing enzymes as members of the Streptomyces R61 DD-peptidase family. Biochem. J. 250: 313324.
64. Kamphuis, I. G.,, K. H. Kalk,, M. B. Swarte, and, J. Drenth. 1984. Structure of papain refined at 1.65 A resolution. J. Mol. Biol. 179: 233256.
65. Kato, T.,, N. Takahashi, and, H. K. Kuramitsu. 1992. Sequence analysis and characterization of the Porphyromonas gingivalis prtC gene, which expresses a novel collagenase activity. J. Bacteriol. 174: 38893895.
66. Keiler, K. C., and, R. T. Sauer. 1996. Sequence determinants of C-terminal substrate recognition by the Tsp protease. J. Biol. Chem. 271: 25892593.
67. Keiler, K. C.,, K. R. Silber,, K. M. Downard,, I. A. Papayannopoulos,, K. Biemann, and, R. T. Sauer. 1995. C-terminal specific protein degradation: activity and substrate specificity of the Tsp protease. Protein Sci. 4: 15071515.
68. Keiler, K. C.,, P. R. Waller, and, R. T. Sauer. 1996. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990993.
69. Kessler, E., 2004. beta-Lytic metalloendopeptidase, p. 9981000. In A. J. Barrett,, N. D. Rawlings, and, J. F. Woessner (ed.), Handbook of Proteolytic Enzymes. Elsevier, London, United Kingdom.
70. Kessler, E., and, D. E. Ohmann. 2004. Staphy-lolysin, p. 10011003. In A. J. Barrett,, N. D. Rawlings, and, J. F. Woessner (ed.), Handbook of Proteolytic Enzymes. Elsevier, London, United Kingdom.
71. Kolmar, H.,, P. Waller, and, R. Sauer. 1996. The DegP and DegQ periplasmic endoproteases of Es-cherichia coli: specificity for cleavage sites and substrate conformation. J. Bacteriol. 178: 59255929.
72. Korat, B.,, H. Mottl, and, W. Keck. 1991. Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol. Microbiol. 5: 675684.
73. Kraut, J., 1977. Serine proteases: structure and mechanism of catalysis. Annu. Rev. Biochem. 46: 331358.
74. Krojer, T.,, M. Garrido-Franco,, R. Huber,, M. Ehrmann, and, T. Clausen. 2002. Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416: 455459.
75. Kuo, W. L.,, B. D. Gehm, and, M. R. Rosner. 1990. Cloning and expression of the cDNA for a Drosophila insulin-degrading enzyme. Mol. En-docrinol. 4: 15801591.
76. Kurochkin, I. V., 2001. Insulin-degrading enzyme: embarking on amyloid destruction. Trends Biochem. Sci. 26: 421425.
77. Larsen, K. S., and, D. S. Auld. 1989. Carboxypepti-dase A: mechanism of zinc inhibition. Biochemistry 28: 96209625.
78. Lipinska, B.,, O. Fayet,, L. Baird, and, C. Geor-gopoulos. 1989. Identification, characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J. Bacteriol. 171: 15741584.
79. Lipinska, B.,, S. Sharma, and, C. Georgopoulos. 1988. Sequence analysis and regulation of the htrA gene of Escherichia coli: a sigma 32-independent mechanism of heat-inducible transcription. Nucleic Acids Res. 16: 1005310067.
80. Marcyjaniak, M.,, S. G. Odintsov,, I. Sabala, and, M. Bochtler. 2004. Peptidoglycan amidase MepA is a LAS metallopeptidase. J. Biol. Chem. 279: 4398243989.
81. Markiewicz, Z.,, J. K. Broome-Smith,, U. Schwarz, and, B. G. Spratt. 1982. Spherical E. coli due to elevated levels of D-alanine carboxypeptidase. Nature 297: 702704.
82. Maskos, K., 2004. Pitrilysins/inverzincins. In A. Messerschmidt,, M. Cygler, and, W. Bode (ed.) Handbook of Metalloproteins, vol. 3. John Wiley & Sons, Ltd., Chichester, England.
83. Matsuhashi, M.,, I. N. Maruyama,, Y. Takagaki,, S. Tamaki,, Y. Nishimura, and, Y. Hirota. 1978. Isolation of a mutant of Escherichia coli lacking penicillin-sensitive D-alanine carboxypeptidase IA. Proc. Natl. Acad. Sci. USA 75: 26312635.
84. Matsuhashi, M.,, Y. Takagaki,, I. N. Maruyama,, S. Tamaki,, Y. Nishimura,, H. Suzuki,, U. Ogino, and, Y. Hirota. 1977. Mutants of Escherichia coli lacking in highly penicillin-sensitive D-alanine car-boxypeptidase activity. Proc. Natl. Acad. Sci. USA 74: 29762979.
85. Matsuhashi, M.,, S. Tamaki,, S. J. Curtis, and, J. L. Strominger. 1979. Mutational evidence for identity of penicillin-binding protein 5 in Escherichia coli with the major D-alanine carboxypeptidase IA activity. J. Bacteriol. 137: 644647.
86. Matthews, B. W., 1988. Structural basis of the action of thermolysin and related proteases. Acc. Chem. Res. 21: 333340.
87. McGrath, M. E.,, T. Erpel,, C. Bystroff, and, R. J. Fletterick. 1994. Macromolecular chelation as an improved mechanism of protease inhibition: structure of the ecotin-trypsin complex. EMBO J. 13: 15021507.
88. McGrath, M. E.,, S. A. Gillmor, and, R. J. Fletter-ick. 1995. Ecotin: lessons on survival in a protease-filled world. Protein Sci. 4: 141148.
89. Meberg, B. M.,, A. L. Paulson,, R. Priyadarshini, and, K. D. Young. 2004. Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in de-termining uniform morphology of Escherichia coli. J. Bacteriol. 186: 83268336.
90. Nagasawa, H.,, Y. Sakagami,, A. Suzuki,, H. Suzuki,, H. Hara, and, Y. Hirota. 1989. Determination of the cleavage site involved in C-termi-nal processing of penicillin-binding protein 3 of Es-cherichia coli. J. Bacteriol. 171: 58905893.
91. Nakata, A.,, H. Shinagawa, and, J. Kawamata. 1979. Inhibition of alkaline phosphatase isozyme conversion by protease inhibitors in Escherichia coli K-12. FEBS Lett. 105: 147150.
92. Nakatogawa, H., and, K. Ito. 2001. Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol. Cell 7: 185192.
93. Nelson, D. E., and, K. D. Young. 2000. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182 :17141721.
94. Odintsov, S. G.,, I. Sabala,, M. Marcyjaniak, and, M. Bochtler. 2004. Latent LytM at 1.3A resolution. J. Mol. Biol. 335: 775785.
95. Palomeque-Messia, P.,, S. Englebert,, M. Leyh-Bouille,, M. Nguyen-Disteche,, C. Duez,, S. Houba,, O. Dideberg,, J. Van Beeumen, and, J. M. Ghuysen. 1991. Amino acid sequence of the penicillin-binding protein/DD-peptidase of Strep-tomyces K15. Predicted secondary structures of the low Mr penicillin-binding proteins of class A. Biochem. J. 279: 223230.
96. Park, J. H.,, Y. S. Lee,, C. H. Chung, and, A. L. Goldberg. 1988. Purification and characterization of protease Re, a cytoplasmic endoprotease in Escherichia coli.J. Bacteriol. 170: 921926.
97. Park, P. W., and, R. P. Mecham. 2004. Lysostaphin, p. 10041005. In A. J. Barrett.,, N. D. Rawlings., and, J. F. Woessner (ed.)., Handbook of Proteolytic Enzymes. Elsevier, London, United Kingdom.
98. Perlman, R. K.,, B. D. Gehm,, W. L. Kuo, and, M. R. Rosner. 1993. Functional analysis of conserved residues in the active site of insulin-degrading en-zyme. J. Biol. Chem. 268: 2153821544.
99. Perlman, R. K., and, M. R. Rosner. 1994. Identification of zinc ligands of the insulin-degrading enzyme. J. Biol. Chem. 269: 3314033145.
100. Perona, J. J., and, C. S. Craik. 1995. Structural basis of substrate specificity in the serine proteases. Pro-tein Sci. 4: 337360.
101. Phillips, M. A.,, L. Hedstrom, and, W. J. Rutter. 1992. Guanidine derivatives restore activity to car-boxypeptidase lacking arginine-127. Protein Sci. 1: 517521.
102. Polgar, L., 2004. Catalytic mechanism of serine and threonine peptidases, p. 14401448. In A. J. Barrett,, N. D. Rawlings, and, J. F.W oessner (ed.), Handbook of Proteolytic Enzymes, 2nd ed., vol. 2. Elsevier, London, United Kingdom.
103. Ponting, C. P., 1997. Evidence for PDZ domains in bacteria, yeast, and plants. Protein Sci. 6: 464468.
104. Pratt, J. M.,, I. B. Holland, and, B. G. Spratt. 1981. Precursor forms of penicillin-binding proteins 5 and 6 of E. coli cytoplasmic membrane. Nature 293: 307309.
105. Pratt, J. M.,, M. E. Jackson, and, I. B. Holland. 1986. The C terminus of penicillin-binding protein 5 is essential for localisation to the E. coli inner membrane. EMBO J. 5: 23992405.
106. Rawlings, N., and, A. Barrett. 1994. Families of ser-ine peptidases. Methods Enzymol. 244: 1961.
107. Rawlings, N. D., and, A. J. Barrett. 1995. Evolutionary families of metallopeptidases. Methods En-zymol. 248: 183228.
108. Rawlings, N. D., and, A. J. Barrett. 2004a. Catalytic mechanisms for metalloproteases, p. 283284. In A. J. Barrett.,, N. D. Rawlings., and, J. F. Woessner (ed.), Handbook of Proteolytic Enzymes, vol 1. Elsevier, London, United Kingdom.
109. Rawlings, N. D., and, A. J. Barrett. 2004b. Introduction: serine peptidases and their clans, p. 14171439. In A. J. Barrett.,, N. D. Rawlings, and, J. F. Woessner (ed.) Handbook of Proteolytic Enzymes, 2nd ed., vol. 2. Elsevier, London, United Kingdom.
110. Rawlings, N. D.,, D. P. Tolle, and, A. J. Barrett. 2004. Evolutionary families of peptidase inhibitors. Biochem. J. 378: 705716.
111. Roberts, M. G.,, D. A. Phoenix, and, A. R. Pewsey. 1997. An algorithm for the detection of surface-active alpha helices with the potential to anchor proteins at the membrane interface. Comput. Appl. Biosci. 13: 99106.
112. Romeis, T., and, J. V. Holtje. 1994. Penicillin-binding protein 7/8 of Escherichia coli is a DD-endopep-tidase. Eur. J. Biochem. 224: 597604.
113. Schiffer, G., and, J. V. Holtje. 1999. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274: 3203132039.
114. Seoane, A.,, A. Sabbaj,, L. M. McMurry, and, S. B. Levy. 1992. Multiple antibiotic susceptibility associated with inactivation of the prc gene. J. Bacteriol. 174: 78447847.
115. Silber, K. R.,, K. C. Keiler, and, R. T. Sauer. 1992. Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini. Proc. Natl. Acad. Sci. USA 89: 295299.
116. Snyder, W., and, T. Silhavy. 1995. Beta-galactosidase is inactivated by intermolecular disulfide bonds and is toxic when secreted to the periplasm of Es-cherichia coli. J. Bacteriol. 177: 953963.
117. Songyang, Z.,, A. S. Fanning,, C. Fu,, J. Xu,, S. M. Marfatia,, A. H. Chishti,, A. Crompton,, A. C. Chan,, J. M. Anderson, and, L. C. Cantley. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275: 7377.
118. Spiess, C.,, A. Beil, and, M. Ehrmann. 1999. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97: 339347.
119. Spratt, B. G., 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 72: 29993003.
120. Spratt, B. G., 1977. Properties of the penicillin-binding proteins of Escherichia coli K12. Eur. J. Biochem. 72: 341352.
121. Spratt, B. G., 1980. Deletion of the penicillin-binding protein 5 gene of Escherichia coli. J. Bacteriol. 144: 11901192.
122. Spratt, B. G., and, J. L. Strominger. 1976. Identification of the major penicillin-binding proteins of Escherichia coli as D-alanine carboxypeptidase IA. J. Bacteriol. 127: 660663.
123. Steitz, T. A., and, R. G. Shulman. 1982. Crystallo-graphic and NMR studies of the serine proteases. Annu. Rev. Biophys. Bioeng. 11: 419444.
124. Stoker, N. G.,, J. K. Broome-Smith,, A. Edelman,, and B. G. Spratt. 1983. Organization and sub-cloning of the dacA-rodA-pbpA cluster of cell shape genes in Escherichia coli. J. Bacteriol. 155: 847853.
125. Strauch, K. L., and, J. Beckwith. 1988. An Es-cherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. Natl. Acad. Sci. USA 85: 15761580.
126. Strauch, K. L.,, K. Johnson, and, J. Beckwith. 1989. Characterization of degP, a gene required for prote-olysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171: 26892696.
127. Swamy, K. H.,, C. H. Chung, and, A. L. Goldberg. 1983. Isolation and characterization of protease do from Escherichia coli, a large serine protease containing multiple subunits. Arch. Biochem. Biophys. 224: 543554.
128. Tadokoro, A.,, H. Hayashi,, T. Kishimoto,, Y. Makino,, S. Fujisaki, and, Y. Nishimura. 2004. Interaction of the Escherichia coli lipoprotein NlpI with periplasmic Prc (Tsp) protease. J. Biochem. (Tokyo) 135: 185191.
129. Tatum, F. M.,, N. F. Cheville, and, D. Morfitt. 1994. Cloning, characterization and construction of htrA and htrA-like mutants of Brucella abortus and their survival in BALB/c mice. Microb. Pathog. 17: 2336.
130. Thunnissen, M. M.,, F. Fusetti,, B. de Boer, and, B. W. Dijkstra. 1995. Purification, crystallisation and preliminary X-ray analysis of penicillin binding protein 4 from Escherichia coli, a protein related to class A beta-lactamases. J. Mol. Biol. 247: 149153.
131. Tuomanen, E., and, J. Schwartz. 1987. Penicillin-binding protein 7 and its relationship to lysis of nongrowing Escherichia coli. J. Bacteriol. 169: 49124915.
132. Vacheron, M. J.,, M. Guinand,, A. Francon, and, G. Michel. 1979. [Characterisation of a new en-dopeptidase from sporulating Bacillus sphaericus which is specific for the gamma-D-glutamyl-L-lysine and gamma-D-glutamyl-(L)meso-diamino-pimelate linkages of peptidoglycan substrates (author’s transl)]. Eur.J. Biochem. 100: 189196.
133. Valentin, C.,, M. J. Vacheron,, C. Martinez,, M. Guinand, and, G. Michel. 1983. Action of Bacillus sphaericus endopeptidases on bacterial pepti-doglycans and peptidoglycan fragments. Biochimie 65: 239245.
134. van der Linden, M. P.,, L. de Haan,, M. A. Hoyer, and, W. Keck. 1992. Possible role of Escherichia coli penicillin-binding protein 6 in stabilization of stationary-phase peptidoglycan. J. Bacteriol. 174: 75727578.
135. Vernet, T.,, D. C. Tessier,, J. Chatellier,, C. Plouffe,, T. S. Lee,, D. Y. Thomas,, A. C. Storer, and, R. Menard. 1995. Structural and functional roles of asparagine 175 in the cysteine protease papain. J. Biol. Chem. 270: 1664516652.
136. Vijayaraghavan, J.,, Y. A. Kim,, D. Jackson,, M. Or-lowski, and, L. B. Hersh. 1990. Use of site-directed mutagenesis to identify valine-573 in the S’1 binding site of rat neutral endopeptidase 24.11 (enkephalinase). Biochemistry 29: 80528056.
137. Waller, P., and, R. Sauer. 1996. Characterization of degQ and degS, Escherichia coli genes encoding ho-mologs of the DegP protease. J. Bacteriol. 178: 11461153.
138. Walsh, N. P.,, B. M. Alba,, B. Bose,, C. A. Gross, and, R. T. Sauer. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113: 6171.
139. Waxman, D. J., and, J. L. Strominger. 1983. Penicillin-binding proteins and the mechanism of action of beta-lactam antibiotics. Annu. Rev. Biochem. 52: 825869.
140. Wilken, C.,, K. Kitzing,, R. Kurzbauer,, M. Ehrmann, and, T. Clausen. 2004. Crystal structure of the DegS stress sensor: how a PDZ domain recognizes misfolded protein and activates a protease domain. Cell 117: 483494.


Generic image for table

List of periplasmic proteases and a protease inhibitor

Citation: Nicolette K, Michael M, Michael E. 2007. Periplasmic Proteases and Protease Inhibitors, p 150-170. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch9

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error