The HtrA family of serine proteases

Molecular Microbiology

Volumn 26, Issue 2, 1997, Pages 209-221

  Pallen, Mark J ^a   Wren, Brendan W ^a  

^a ST BARTHOLOMEW S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE; SERINE PROTEINASE; SIGMA FACTOR; VACCINE;

BACTERIUM; BRUCELLA; ESCHERICHIA COLI; EUKARYOTE; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SALMONELLA; SIGNAL TRANSDUCTION; YERSINIA;

BACTERIA (MICROORGANISMS); BRUCELLA; ESCHERICHIA COLI; EUKARYOTA; SALMONELLA; YERSINIA;

EID: 0030812638     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.5601928.x     Document Type: Review

References (72)

1. Baird, L., and Georgopoulos, C. (1990) Identification, cloning, and characterization of the Escherichia coli sohA gene, a suppressor of the htrA (degP) null phenotype. J Bacteriol 172: 1587-1594.
2. Baird, L., Lipinska, B., Raina, S., and Georgopoulos, C. (1991) Identification of the Escherichia coli sohB gene, a multicopy suppressor of the htrA (degP) null phenotype. J Bacteriol 173: 5763-5770.
3. Barbieri, J.T., Pizza, M., Cortina, G., and Rappuoli, R. (1990) Biochemical and biological activities of recombinant S1 subunit of pertussis toxin. Infect Immun 58: 999-1003.
4. Bass, S., Gu, Q., and Christen, A. (1996) Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated R1pA. J Bacteriol 178: 1154-1161.
5. Baumler, A.J., Kusters, J.G., Stojiljkovic, I., and Heffron, F. (1994) Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 62: 1623-1630.
6. Cavard, D. (1995) Role of DegP protease on levels of various forms of colicin A lysis protein. FEMS Microbiol Lett 125: 173-178.
7. Cavard, D., Lazdunski, C., and Howard, S.P. (1989) The acylated precursor form of the colicin A lysis protein is a natural substrate of the DegP protease. J Bacteriol 171: 6316-6322.
8. Chabalgoity, J.A., Khan, C.M., Nash, A.A., and Hormaeche, C.E. (1996) A Salmonella typhimurium htrA live vaccine expressing multiple copies of a peptide comprising amino acids 8-23 of Herpes simplex virus glycoprotein D as a genetic fusion to tetanus toxin fragment C protects mice from Herpes simplex virus infection. Mol Microbiol 19: 791-801.
9. Chatfield, S.N., Strahan, K., Pickard, D., Charles, I.G., Hormaeche, C.E., and Dougan, G. (1992) Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microb Pathogen 12: 145-151.
10. Clayton, C.L., Kleanthous, H., Morgan, D.D., Puckey, L., and Tabaqchali, S. (1993) Rapid fingerprinting of Helicobacter pylori by polymerase chain reaction and restriction fragment length polymorphism analysis. J Clin Microbiol 31: 1420-1425.
11. Cosma, C.L., Danese, P.N., Carlson, J.H., Silhavy, T.J., and Snyder, W.B. (1995) Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol Microbiol 18: 491-505.
12. Da Costa, M., Guillou, J.P., Garin-Bastuji, B., Thiebaud, M., and Dubray, G. (1996) Specificity of six gene sequences for the detection of the genus Brucella by DNA amplification. J Appl Bacteriol 81: 267-275.
13. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J., and Silhavy, T.J. (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387-398.
14. Elzer, P.H., Phillips, R.W., Kovach, M.E., Peterson, K.M., and Roop, R.M.n. (1994) Characterization and genetic complementation of a Brucella abortus high-temperature-requirement A (htrA) deletion mutant. Infect Immun 62: 4135-4139.
15. Elzer, P.H., Hagius, S.D., Robertson, G.T., Phillips, R.W., Walker, J.V., Fatemi, M.B., Enright, F.M., and Roop, R.M.n. (1996a) Behaviour of a high-temperature-requirement A (HtrA) deletion mutant of Brucella abortus in goats. Res Vet Sci 60: 48-50.
16. Elzer, P.H., Phillips, R.W., Robertson, G.T., and Roop, R.M.n. (1996b) The HtrA stress response protease contributes to resistance of Brucella abortus to killing by murine phagocytes. Infect Immun 64: 4838-4841.
17. Everest, P., Frankel, G., Li, J., Lund, P., Chatfield, S., and Dougan, G. (1995) Expression of LacZ from the htrA, nirB and groE promoters in a Salmonella vaccine strain: influence of growth in mammalian cells. FEMS Microbiol Lett 126: 97-101.
18. Fanning, A.S., and Anderson, J.M. (1996) Protein-protein interactions: PDZ domain networks. Curr Biol 6: 1385-1388.
19. Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30: 465-506.
20. Jackson, S.H., Gallin, J.I., Holland, S.M. (1995) The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med 182: 751-758.
21. Johnson, K., Charles, I., Dougan, G., Pickard, D., O'Gaora, P., Costa, G., Ali, T., Miller, I., and Hormaeche, C. (1991) The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol 5: 401-407.
22. Keiler, K.C., and Sauer, R.T. (1996) Sequence determinants of C-terminal substrate recognition by the Tsp protease. J Biol Chem 271: 2589-93.
23. Keiler, K.C., Silber, K.R., Downard, K.M., Papayannopoulos, I.A., Biemann, K., and Sauer, R.T. (1995) C-terminal specific protein degradation: activity and substrate specificity of the Tsp protease. Protein Sci 4: 1507-15.
24. Keiler, K.C., Waller, P.R., and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990-3.
25. Kolmar, H., Waller, P.R., and Sauer, R.T. (1996) The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for Cleavage sites and substrate conformation. J Bacteriol 178: 5925-5929.
26. Laskowska, E., Kuczynska-Wisnik, D., Skorko-Glonek, J., and Taylor, A. (1996) Degradation by proteases Lon, Clp and HtrA, of Escherichia coli proteins aggregated in vivo by heat shock; HtrA protease action in vivo and in vitro. Mol Microbiol 22: 555-571.
27. Levine, M.M., Galen, J., Barry, E., Noriega, F., Chatfield, S., Sztein, M., Dougan, G., and Tacket, C. (1996) Attenuated Salmonella as live oral vaccines against typhoid fever and as live vectors. J Biotechnol 44: 193-196.
28. Li, S.R., Dorrell, N., Everest, P.H., Dougan, G., and Wren, B.W. (1996) Construction and characterization of a Yersinia enterocolitica O: 8 high-temperature requirement (htrA) isogenic mutant. Infect Immun 64: 2088-2094.
29. Lipinska, B., Sharma, S., and Georgopoulos, C. (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: 10053-10067.
30. Lipinska, B., Fayet, O., Baird, L., and Georgopoulos, C. (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: 1574-1584.
31. Lipinska, B., Zylicz, M., and Georgopoulos, C. (1990) The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase. J Bacteriol 172: 1791-1797.
32. Meerman, H.J., and Georgiou, G. (1994) Construction and characterization of a set of E. coli strains deficient in all known loci affecting the proteolytic stability of secreted recombinant proteins. Biotechnology 12: 1107-1110.
33. Misra, R., Peterson, A., Ferenci, T., and Silhavy, T.J. (1991) A genetic approach for analyzing the pathway of LamB assembly into the outer membrane of Escherichia coli. J Biol Chem 266: 13592-13597.
34. Missiakas, D., and Raina, S. (1997a) Protein misfolding in the cell envelope of Escherichia coli: new signaling pathways. Trends Biochem Sci 22: 59-63.
35. Missiakas, D., and Raina, S. (1997b) Signal transduction pathways in response to protein misfolding in the extra-cytoplasmic compartments of E. coli: role of two new phosphoprotein phosphatases PrpA and PrpB. EMBO J 16: 1670-1685.
36. Missiakas, D., and Raina, S. (1997c) Protein folding in the bacterial periplasm. J Bacteriol 179: 2465-2471.
37. Moran, N.A. (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93: 2873-2878.
38. Phillips, R.W., Elzer, P.H., and Roop, II, R.M. (1995) A Brucella melitensis high temperature requirement A (htrA) deletion mutant demonstrates a stress response defective phenotype in vitro and transient attenuation in the BALB/c mouse model. Microb Pathogen 19: 227-284.
39. Pollock, J.D., Williams, D.A., Gifford, M.A., Li, L.L., Du, X., Fisherman, J., Orkin, S.H., Doerschuk, C.M., Dinauer, M.C. (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nature Genet 9: 202-209.
40. Ponting, C.P. (1997) Evidence for PDZ domains in bacteria, yeast, and plants. Protein Sci 6: 464-468.
41. Reed, K.E., and Cronan, Jr, J.E. (1991) Escherichia coli exports previously folded and biotinylated protein domains. J Biol Chem 266: 11425-11428.
42. Robertson, G.T., Elzer, P.H., and Roop, R.M.n. (1996) In vitro and in vivo phenotypes resulting from deletion of the high temperature requirement A (htrA) gene from the bovine vaccine strain Brucella abortus S19. Vet Microbiol 49: 197-207.
43. Roop, R.M.n., Fletcher, T.W., Sriranganathan, N.M., Boyle, S.M., and Schurig, G.G. (1994) Identification of an immunoreactive Brucella abortus HtrA stress response protein homolog. Infect Immun 62: 1000-1007.
44. Schurr, M.J., Yu, H., Boucher, J.C., Hibler, N.S., and Deretic, V. (1995) Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor AlgU (sigma E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J Bacteriol 177: 5670-5679.
45. Schurr, M.J., Yu, H., Martinez-Salazar, J.M., Boucher, J.C., and Deretic, V. (1996) Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol 178: 4997-5004.
46. Seol, J.H., Woo, S.K., Jung, E.M., Yoo, S.J., Lee, C.S., Kim, K.J., Tanaka, K., Ichihara, A., Ha, D.B., and Chung, C.H. (1991) Protease Do is essential for survival of Escherichia coli at high temperatures: its identity with the htrA gene product. Biochem Biophys Res Commun 176: 730-736.
47. Silber, K.R., and Sauer, R.T. (1994) Deletion of the prc (tsp) gene provides evidence for additional tail-specific proteolytic activity in Escherichia coli K-12. Mol Gen Genet 242: 237-40.
48. Sinha, K., Mastroeni, P., Harrison, J., de Hormaeche, R.D., and Hormaeche, C.E. (1997) Salmonella typhimurium aroA, htrA, and aroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infect Immun 65: 1566-1569.
49. Skorko-Glonek, J., Wawrzynow, A., Krzewski, K., Kurpierz, K., and Lipinska, B. (1995a) Site-directed mutagenesis of the HtrA (DegP) serine protease, whose proteolytic activity is indispensable for Escherichia coli survival at elevated temperatures. Gene 163: 47-52.
50. Skorko-Glonek, J., Krzewski, K., Lipinska, B., Bertoli, E., and Tanfani, F. (1995b) Comparison of the structure of wildtype HtrA heat shock protease and mutant HtrA proteins. A Fourier transform infrared spectroscopic study. J Biol Chem 270: 11140-11146.
51. Skorko-Glonek, J., Lipinska, B., Krzewski, K., Zolese, G., Bertoli, E., and Tanfani, F. (1997) HtrA heat shock protease interacts with phospholipid membranes and undergoes conformational changes. J Biol Chem 272: 8974-8982.
52. Sone, M., Kishigami, S., Yoshihisa, T., and Ito, K. (1997) Roles of disulfide bonds in bacterial alkaline phosphatase. J Biol Chem 272: 6174-6178.
53. Songyang, Z., Fanning, A.S., Fu, C., Xu, J., Marfatia, S.M., Chishti, A.H., Crompton, A., Chan, A.C., Anderson, J.M., and Cantley, L.C. (1997) Recognition of unique carboxylterminal motifs by distinct PDZ domains. Science 275: 73-77.
54. Strauch, K.L., and Beckwith, J. (1988) An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc Natl Acad Sci USA 85: 1576-1580.
55. Strauch, K.L., Johnson, K., and Beckwith, J. (1989) Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J Bacteriol 171: 2689-2696.
56. Stricker, N.L., Christopherson, K.S., Yi, B.A., Schatz, P.J., Raab, R.W., Dawes, G., Bassett, Jr, D.E., Bredt, D.S., and Li, M. (1997) PDZ domain of neuronal nitric oxide synthase recognizes novel C-terminal peptide sequences. Nature Biotechnol 15: 336-342.
57. Suzuki, C.K., Rep, M., van Dijn, J.M., Suda, K., Grivell, L.A., and Schatz, G. (1997) ATP-dependent proteases that also chaperone protein biosynthesis. Trends Biochem Sci 22: 118-123.
58. Swamy, K.H., and Goldberg, A.L. (1982) Subcellular distribution of various proteases in Escherichia coli. J Bacteriol 149: 1027-1033.
59. Tacket, C.O., Sztein, M.B., Losonsky, G.A., Wasserman, S.S., Nataro, J.P., Edelman, R., Pickard, D., Dougan, G., Chaffield, S.N., and Levine, M.M. (1997) Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect Immun 65: 452-456.
60. Tatum, F.M., Cheville, N.F., and Morfitt, D. (1994) Cloning, characterization and construction of htrA and htrA-like mutants of Brucella abortus and their survival in BALB/c mice. Microb Pathogen 17: 23-36.
61. Toth, T.E., Cobb, J.A., Boyle, S.M., Roop, R.M., and Schurig, G.G. (1995) Selective humoral immune response of Balb/ C mice to Brucella abortus proteins expressed by vaccinia virus recombinants. Vet Microbiol 45: 171-183.
62. Tu, G.F., Reid, G.E., Zhang, J.G., Moritz, R.L., and Simpson, R.J. (1995) C-terminal extension of truncated recombinant proteins in Escherichia coli with a 10Sa RNA decapeptide. J Biol Chem 270: 9322-9326.
63. Waller, P.R., and Sauer, R.T. (1996) Characterization of degQ and degS, Escherichia coli genes encoding homologs of the DegP protease. J Bacteriol 178: 1146-1153.
64. Wootton, J.C., and Drummond, M.H. (1989) The Q-linker: a class of interdomain sequences found in bacterial multidomain regulatory proteins. Protein Eng 2: 535-543.
65. Wren, B.W., Olsen, A.L., Stabler, R., and Li, S.R. (1995) A PCR-based strategy for the construction of a defined Yersinia enterocolitica O: 8 htrA mutant. Contrib Microbiol Immunol 13: 290-293.
66. Wülfing, C., and Rappuoli, R. (1997) Efficient production of heat-labile enterotoxin mutant proteins by overexpression of dsbA in a degrP-deficient Escherichia coli strain. Arch Microbiol 167: 280-283.
67. Xie, Z.D., Hershberger, C.D., Shankar, S., Ye, R.W., and Chakrabarty, A.M. (1996) Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J Bacteriol 178: 4990-4996.
68. Yamamoto, T., Hanawa, T., Ogata, S., and Kamiya, S. (1996) Identification and characterization of the Yersinia enterocolitica gsrA gene, which protectively responds to intracellular stress induced by macrophage phagocytosis and to extra-cellular environmental stress. Infect Immun 64: 2980-2987.
69. Yoo, S.J., Seol, J.H., Woo, S.K., Suh, S.W., Hwang, D.S., Ha, D.B., and Chung, C.H. (1993) Hydrolysis of the IciA protein, an inhibitor of DNA replication initiation, by protease Do in Escherichia coli. FEBS Lett 327: 17-20.
70. Yu, H., Schurr, M.J., and Deretic, V. (1995) Functional equivalence of Escherichia coli sigma E and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa. J Bacteriol 177: 3259-3268.
71. Zdanovsky, A.G., Kulaeva, O.I., and Yankovsky, N.K. (1992) Construction and expression of diphtheria toxin-encoding gene derivatives in Escherichia coli. Gene 116: 81-86.
72. Zumbrunn, J., and Trueb, B. (1996) Primary structure of a putative serine protease specific for IGF-binding proteins. FEBS Lett 398: 187-192.