Role of the HtrA protein family in the stress response

Heat Shock Proteins: New Research

Volumn , Issue , 2008, Pages 417-458

  Zurawa Janicka, Dorota ^a   Skorko Glonek, Joanna ^a   Lipinska, Barbara ^a  

^a UNIVERSITY OF GDA SK   (Poland)

Author keywords

[No Author keywords available]

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EID: 84895414270     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (160)

1. Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S. R., Shinozaki, K. & Clarke, A. K. (2001). Chloroplast and Mitochondrial Proteases in Arabidopsis. Proposed nomenclature. Plant Physiol, 125, 1912-1918.
2. Ahn, S. J., Lemos, J. A. & Burne, R. A. (2005). Role of HtrA in growth and competence of Streptococcus mutans UA159. J Bacteriol, 187, 3028-3038.
3. Akhurst, R. J. & Derynck, R. (2001). TGF-ß signaling in cancer: a double-edged sword. Trends Cell Biol, 11, S44-S51.
4. Akiyama, Y., Kanehara, K. & Ito, K. (2004). RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. EMBO J, 23, 4434-4442.
5. Anandatheerthavarada, H. K., Biswas, G., Robin, M. A. & Avadhani, N. G. (2003). Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J Cell Biol, 161, 41-54.
6. Baldi, A., De Luca, A., Morini, M., Battista, T., Felsani, A., Baldi, F., Catricala, C., Amantea, A., Noonan, D. M., Albini, A., Natali, P. G., Lombardi, D. & Paggi, M. G. (2002). The HtrA1 serine protease is down-regulated during human melanoma progression and repress growth of metastatic melanoma cells. Oncogene, 21, 6684-6688.
7. Baneyx, F. & Georgiou, G. (1991). Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecularweight substates in vivo. J Bacteriol, 173, 2696-2703.
8. Barrett, A. J., Rawlings, N. D. & Woessner, J. F. (2004). Serine and Threonine Peptidases. In: Handbook of Proteolytic Enzymes., t II. Elsevier Academic Press, pp. 1417-1784.
9. Bass, S., Gu, Q. & Christen, A. (1996). Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and truncated R1pA. J Bacteriol, 178, 1154-1161.
10. Betton, J.-M., Sassoon, N., Hofnung, M. & Laurent, M. (1998). Degradation versus aggregation of misfolded maltose-binding protein in the periplasm of Escherichia coli. J Biol Chem, 273, 8897-8902.
11. Biswas, S. & Biswas, I. (2005). Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. Infect Immun, 73, 6923-6934.
12. Blair, P. J., Jiang, J., Schoeler, G. B., Moron, C., Anaya, E., Cespedes, M., Cruz, C., Felices, V., Guevara, C., Mendoza, L., Villaseca, P., Sumner, J. W., Richards, A. L. & Olson, J. G. (2004). Characterization of Spotted Fever Group Rickettsiae in Flea and Tick Specimens from Northern Peru. J Clin Microbiol, 42, 4961-4967.
13. Blink, E., Maianski, N. A., Alnemri, E. S., Zevros, A. S., Roos, D. & Kuijpers, T. W. (2004). Intramitochondrial serine protease activity of Omi/HtrA2 is required for caspaseindependent cell death of human neutrophils. Cell Death Differ, 11, 937-939.
14. Boer, P., Wagenaar, J. A., Achterberg, R. P., Putten, J. P., Schouls, L. M. & Duim, B. (2002). Generation of Campylobacter jejuni genetic diversity in vivo. Mol Microbiol, 44, 351-359.
15. Boucher, J. C., Martinez-Salazar, J., Schurr, M. J., Mudd, M. H., Yu, H. & Deretic, V. (1996). Two distinct loci affecting conversion to mucoidy in pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J Bacteriol, 178, 511-523.
16. Bringer, M.-A., Barnich, N., Glasser, A.L., Bardot, O. & Darfeuille-Michaud, A. (2005). HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun, 73, 712-721.
17. Brondsted, L., Andersen, M. T., Parker, M., Jorgensen, K. & Ingmer, H. (2005). The HtrA protease of Campylobacter jejuni is required for heat and oxygene tolerance and for optimal interaction with human epithelial cells. Appl Environ Microbiol, 71, 3205-3212.
18. Brustovetsky, N., Brustovetsky, T., Purl, K. J., Capano, M., Crompton, M. & Dubinsky J. M. (2003). Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J Neurosci, 23, 4858-4867.
19. Buelow, D. R. & Raivio, T. L. (2005). Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J Bacteriol, 187, 6622-6630.
20. CastilloKeller, M. & Misra, R. (2003). Protease-Deficient DegP Suppress Lethal Effect of a Mutant OmpC Protein by Its Capture. J Bacteriol, 185, 148-154.
21. Cezairliyan, B. O. & Sauer, R. T. (2007). Inhibition of regulated proteolysis by RseB. Proc Natl Acad Sci USA, 104, 3771-3776.
22. Chien, J., Staub, J., Hu, S-I., Erickson-Johnson, M. R., Couch, F. J., Smith, D. I., Crowl, R. M., Kaufmann, H. & Shridhar, V. (2004). A candidate tumor suppressor HtrA1 is downregulated in ovarian cancer. Oncogene, 23, 1636-1644.
23. Chien, J., Aletti, G., Baldi, A., Catalano, V., Muretto, P., Keeney, G. L., Kalli, K. C., Staub, J., Ehrmann, E., Cliby, W. A. & Shridhar, V. (2006). Serine protease HtrA1 modulates chemotherapy-induced cytotoxicity. J Clin Invest, 116, 1994-2004.
24. Chinchila, M., Paseti, M. F., Medina-Moreno, S., Wang, J. Y., Gomez-Duarte, O., Stout, R., Levine, M. M. & Galen, J. E. (2007). Enhanced Immunity to Plasmodium Falciparum Circumsprozoite Protein (PfCSP) by Using Salmonella enterica Serovar Typhi Expressing PfCSP and a PfCSP-Encoding DNA Vaccine in Heterologous Prijme-Boost Strategy. Infect Immun, 75, 3769-3779.
25. Choudhury, D. A., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J. S., Hultgren, S. J. & Knight, S. D. (1999). X-ray structure of the FimC-FimH chaperone adhesion complex from uropathogenic Escherichia coli. Science, 285, 1061-1066.
26. Cilenti, L., Soundarapandrian, M. M., Kyriasis, G. A., Stratico, V., Singh, S., Gupta, S., Bonventre, J. V., Alnemri, E. S. & Zervos, A. S. (2004). Regulation of HAX-1 Antiapoptotic Protein by Omi/HtrA2 Protease during Cell Death. J Biol Chem, 279, 50295-50301.
27. Clausen, T., Southan, C. & Ehrmann, M. (2002). The HtrA Family of Proteases: Implications for Protein Composition and Cell Fate. Mol Cell, 10, 443-455.
28. Cole, J. N., Aquilina, J. A., Hains, P. G., Henningham, A., Sriprakash, K. S., Caparon, M. G., Nizet, V., Kotb, M., Cordwell, S. J., Djordjevic, S. P. & Walker, M. K. (2007). Role of group A Streptococcus HtrA in the maturation of SpeB protease. Proteomics 7, 4488-4498.
29. Collery, R. & Devine, K. M. (2001). YkdA and YvtA, HtrA-like serine proteases in Bacillus subtilis, engage in negative autoregulation and reciprocal cross-regulation of ykdA and yvtA gene expression. J Bacteriol, 183, 654-663.
30. Cortes, G., de Astorza, B., Benedi, V. J. & Alberti, S. (2002). Role of the htrA gene in Klebsiella pneumoniae virulence. Infect Immun, 70, 4772-4776.
31. Dartigalongue, C., Missiakas, D. & Raina, S. (2001). Characterization of the Escherichia coli σE regulon. J Biol Chem, 276, 20866-20875.
32. De Luca, A., Falco, M., Luca, L., Penta, R., Shridhar, V., Baldi, F., Campioni, M., Paggi, M. G. & Baldi, A. (2004). Pattern of Expression of HtrA1 During Mouse Development. J Histochem Cytochem, 52, 1609-1617.
33. Demoor-Fossard, M., Redini, F., Boittin, M. & Pujol, J. P. (1998). Expression of decorin and biglycan by rabbit articular chondrocytes. Effects of cytokines and phenotypic modulation. Biochem Biophys Acta, 1389, 179-191.
34. Derynck, R., Akhurst, R. J. & Balmain, A. (2001). TGF-beta signaling in tumor suppression and cancer progression. Nat Genet, 29, 117-129.
35. Dorel, C., Lejeune, P. & Rodrigue, A. (2006). The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res Microbiol, 157, 306-314.
36. Duguay, A. & Silhavy, T. J. (2004). Quality control in the bacterial periplasm. Biochim Biophys Acta, 1694, 121-134.
37. Everest, P., Frankel, G., Li, J., Lund, P., Chatfield, S., 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.
38. Faccio, L., Fusco, C., Chen, A., Martinotti, S., Bonventres, J. V. & Zervos, A. S. (2000a). Characterization of Novel Human Serine Protease That Has Extensive Homology to Bacterial Heat Shock Endoprotease HtrA and Is Regulated by Kidney Ischemia. J Biol Chem, 275, 2581-2588.
39. Faccio, L., Fusco, C., Viel, A. & Zevros A. S. (2000b). Tissue-specific splicing of Omi stress-regulated endoprotease leads to inactive protease with a modified PDZ domain. Genomics, 68, 343-347.
40. Fahrenkrog, B., Sauder, U. & Aebi, U. (2004). The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J Cell Sci, 117, 115-126.
41. Flannagan, R. S., Aubert, D., Kooi, C., Sokol, P. A. & Valvano, M. A. (2007). Burkholderia cenocepacia requires a periplasmic HtrA protease for growth under thermal and osmotic stress and for survival in vivo. Infect Immun, 75, 1679-1689.
42. Foucaud-Scheunemann C. & Poquet, I. (2003). HtrA is a key factor in the response to specific stress conditions in Lactococcus lactis. FEMS Microbiol Lett, 224, 53-59.
43. Foynes, S., Holley, J. L., Garmory, H. S., Titball, R. W., Fairweather, N. F. (2002). Vaccination against type F botulinum toxin using attenuated Salmonella enterica var Thypimurium strains expressing the BoNT/F HC fragment. Vaccine, 21, 1052-1059.
44. Glazebrook, J., Ichige, A., Walker, G. C. (1996) Genetic analysis of Rhizobium meliloti bacA-phoA fusion results in identification of degP: two loci required for symbiosis are closely linked to degP. J Bacteriol 178, 745-752.
45. Grau, S., Baldi, A., Bussani, R., Tian, X., Stefanescu, R., Przybylski, M., Richards, P., Jones, S. A., Shridhar, V., Clausen, T. & Ehrmann M. (2005). Implications of the serine protease HtrA1 in amyloid precursor protein processing. Proc Natl Acad Sci, 102, 6021-6026.
46. Grau, S., Richards, P. J., Keer, B., Hughes, C., Caterson, B., Williams, A. S., Junker, U., Jones, S. A., Clausen, T. & Ehrmann, M. (2006). The Role of Human HtrA1 in Arthritic Disease. J Biol Chem, 281, 6124-6129.
47. Gray, C. W., Ward, R. V., Karran, E., Turconi, S., Rowles, A., Viglienghi, D., Southan, C., Barton, A., Fantom, K. G., West, A., Savopoulos, J., Hassan, N. J., Clinkenbeard, H., Hanning, C., Amegadzie, B., Davis, J. B., Dingwall, C., Livi, G. P. & Creasy, C. L. (2000). Characterization of Human HtrA2, novel serine protease involved in the mammalian cellular stress response. Eur J Biochem, 267, 5699-5710.
48. Guo, Q., Fu, W. M., Sopher, B. L., Miller, M. W., Ware, C. B. Martin, G. M. & Mattson, M. P. (1999). Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice. Nat Med, 5, 101-106.
49. Guo, Q., Sopher, B. L., Furukawa, K., Pham, D. G., Robinson, N., Martin, G. M. & Mattson, M. P. (1997). Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide-involvement of calcium and oxyradicals. J Neurosci, 17, 4212-4222.
50. Gupta, S., Singh, R., Datta, P., Zhang, Z. J., Orr, C., Lu, Z., Dubois, G., Zevros, A. S., Meisler, H. M., Srinivasula, S. M., Fernandes-Alnemri, T. & Alnemri, E. S. (2004). The C-terminal Taill of Presenilin Regulates Omi/HtrA2 Protease Activity. J Biol Chem, 279, 45844-45854.
51. Hansmann, Y., DeMartino, S., Piemont, Y., Meyer, N., Mariet, P., Heller, R., Christmann, D. & Jaulhac, B. (2005). Diagnosis of Cat Scratch Disease of Bartonella henselae by PCR: a Study of Patients with Lymph Node Enlargement. J Clin Microbiol, 43, 3800-3806.
52. Hansson, C. A., Frykman, S., Farmery, M. R., Tjernberg, L. O., Nilsberth, C., Pursglove, S. E., Ito, A., Winblad, B., Cowburn, R. F., Thyberg, J. & Ankarcrona, M. (2004). Nicastrin, presenilin, APH-1, and PEN-2 form active gamma-secretase complexes in mitochondria. J Biol Chem, 279, 51654-51660.
53. Hasselblatt, H., Kurzbauer, R., Wilken, C., Krojer, T., Sawa, J., Kurt, J., Kirk, R., Hasenbein, S., Ehrmann, M., Clausen, T. (2007). Regulation of the σE stress response by DegS: hoe the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes & Dev, 21, 2659-2670.
54. Haussuhl, K., Andersson, B. & Adamska, I. (2001). A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J, 20, 713-722.
55. Hedge, R., Srinivasula, S. M., Zhang, Z. J., Wassell, R., Mukattash, R., Cilenti, L., DoBois, G., Lazebnik, Y., Zevros, A. S., Fernandes-Alnemri, T. & Alnemri, E. S. (2002). Identification of Omi/HtrA2 as Mitochondrial Apoptotic Serine Protease That Disrupts Inhibitors of Apoptosis Protein-Caspase Interaction. J Biol Chem, 277, 432-438.
56. Hu, S.-I., Carozza, M., Klein, M., Nantermet, P., Luk, D. & Crowl, R. M. (1998). Human HtrA, evolutionary conserved serine protease identified as differentially expressed gene product on osteoarthritis cartilage. J Biol Chem, 273, 34406-34412.
57. Hung, A. Y. & Sheng, M. (2002). PDZ domains: structural modules for protein complex assembly. J Biol Chem, 277, 5699-5702.
58. Ibrahim, Y. M., Kerr, A. R., McCluskey, J. & Mitchell, T. J. (2004). Role of HtrA in in the virulence and competence of Streptococcus pneumoniae. Infect Immun, 72, 3584-3591.
59. Isaac, D. D., Pinkner, J. S., Hultgren, S. J. & Silhavy, T. J. (2005). The extracytoplsmic adaptor protein CpxP is degraded by DegP. Proc Natl Acad Sci USA, 102, 17775-17779.
60. Iwanczyk, J., Damjanovic, D., Kooistra, J., Leong, V., Jomaa, A., Ghirlando, R. & Ortega, J. (2007). The role of the PDZ domains in Escherichia coli DegP protein. J Bacteriol, 189, 3176-3186.
61. Jin, S., Kalkum, M., Overholtzer, M., Stoffel, A., Chait, B. T. & Levine, A. J. (2003). CIAP1 and the serine protease HtrA2 are involved in a novel p53-dependent apoptosis pathway in mammals. Genes Dev, 17, 359-367.
62. Jomaa, A., Damianovic, D., Leong, V., Ghirlando, R., Iwanczyk, J. & Ortega, J. (2007). The inner cavity of Escherichia coli DegP protein is not essential for molecular chaperone and proteolytic activity. J Bacteriol, 189, 706-716.
63. Jones, C. H., Bolken, T. C., Jones, K. F., Zeller, G. O. & Hruby, D. E. (2001). Conserved DegP protease in gram-positive bacteria is essential for thermal and oxidative toleranceand full virulence of Streptococcus pyogenes. Infect Immun, 69, 5538-5545.
64. Jones, C. H., Dexter, P., Evans, A. K., Liu, C., Hultgren, S. J. & Hruby, D. E. (2002). Escherichia coli DegP protease cleaves between paired hydrophobic residues in a natural substrate: the PapA pilin. J Bacteriol, 184, 5762-5771.
65. Jones, J. M., Datta, P., Srinivasula, S. M., Ji, W., Gupta, S., Zhang, Z. J., Davies, E., Hajnoczky, G., Saunders, T. L., Van Keuren, M. L., Fermandes-Alnemri, T., Meisler, M. H. & Alnemri, E. S. (2003). Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature, 425, 721-727.
66. Kaminska, B., Wesolowska, A. & Danilkiewicz, M. (2005). TGF beta signaling and its role in tumour pathogenesis. Acta Biochim Polon, 52, 329-337.
67. Kim, K. I., Park, S., Kang, S. H., Cheong, G. & Chung C. H. (1999). Selective degradation of unfolded proteins by the self-compartmentalizing HtrA protease, a periplasmic heat shock protein in Escherichia coli. J Mol Biol, 294, 1363-1374.
68. Kirkitadze, M. D. & Kowalska, A. (2005). Molecular mechanisms initiating amyloid β-fibril formation in Alzheimer's disease. Acta Biochim Polon, 52, 417-423.
69. Kolmar, H., Waller, P. R. H. & Sauer, R. T. (1996). The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrates conformation. J Bacteriol, 178, 5925-5929.
70. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M. & Clausen, T. (2002). Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature, 416, 455-459.
71. Kuninaka, S., Nomura, M., Hirota, T., Iida, S.-I., Hara, T., Honda, S., Kunitoku, N., Sasayama, T., Arima, Y., Marumoto, T., Koja, K., Yonehara, S. & Saya, H. (2005). The tumor suppressor WARTS activates the Omi/HtrA2-dependent pathway of cell death. Oncogene, 24, 5287-5298.
72. Laskowska, E., Kuczynska-Wisnik, D., Skorko-Glonek, J. & 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.
73. Li, S.-R., Dorrell, N., Everest, P. H., Dougan, G. & Wren, B. W. (1996). Construction and characterization of a Yersinia enterocolica O:8 high temperature requirement (htrA) isogenic mutant. Infect Immun, 64, 2088-2094.
74. Li, W., Srinivasula, S. M., Chai, J., Li, P., Wu, J-W., Zhang, Z., Alnemri, E. S. & Shi, Y. (2002). Structural insights into the pro-apoptotic function of mitochondrial serine protease HtrA2/Omi. Nat Struct Biol, 9, 436-441.
75. Lipinska, B., Fayet, O., Baird, L. & 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.
76. Lipinska, B., Zylicz, M. & Georgopoulos C. (1990). The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase. J Bacteriol, 172, 1791-1797.
77. Liu, M. L., Liu, M. J., Kim, M. J., Kim, H. J. & Hong, S. T. (2005). HtrA2 Interacts with Aβ Peptide but Does Not Directly Alter Its Production and Degradation. Mol Cells, 20, 83-89.
78. Liu, M.-J., Liu, M.-L., Shen, Y.-F., Kim, J.-M., Lee, B.-H., Lee, Y.S. & Hong, S.-T. (2007). Transgenic mice with neuron-specific overexpression of HtrA2/Omi suggestr a neuroprotective role for HtrA2/Omi. Biochem Biophys Res Commun, 362, 295-300.
79. Londorno-Arcila, P., Freeman, D., Kleanthous, H., O'Dowd, A. M., Lewis, S., Turner, A. K., Rees, E. L., Tibbits, T. J., Greenwood, J., Monath, T. P. & Darsley, M. J. (2002). Attenuated Salmonella enterica Serovar Typhi Expressing Urease Effectively Immunizes Mice against Helicobacter pylori Challenge as Part of a Heterologous Mucosal Priming-Parental Boosting Vaccination. Infect Immun, 70, 5096-5106.
80. Lowe, D. C., Savidge, T. C., Pickard, D., Eckmann, L., Kagnoff, M. F. & Dougan, G. (1999). Characterization of candidate oral vaccine strains harboring defined mutations in aroA, aroC, and htrA. Infect Immun, 67, 700-707.
81. Lyon, W. R. & Caparon, M. G. (2004). Role for the serine protease HtrA (DegP) of Streptococcus pyogenes in the biogenesis of virulence factors SpeB and the hemolysin streptolysin S. Infect Immun, 72, 1618-1625.
82. Martins, L. M., Iaccarino, I., Tenev, T., Gschmeissner, S., Totty, N. F., Lemoines, N. R., Savopoulos, J., Gray, C. W., Creasy, C. L., Dingwall, C. & Downward, J. (2002). The Serine Protease Omi/HtrA2 Regulates Apoptosis by Binding XIAP through a Reaper-like Motif. J Biol Chem, 277, 439-444.
83. Martins, L. M., Morrison, A., Klupsch, K., Fedele, V., Moisoi, N., Teismann, P., Abuin, A., Grau, E., Geppert, M., Livi, G. P., Creasy, C. L., Martin, A., Hargreaves, I., Heales, S. J., Okada, H., Brandner, S., Schulz, J. B., Mak, T. & Downward, J. (2004). Neuroprotective Role of the Reaper-Realated Serine Protease Htra2/Omi Revealed by Targeted Deletion in Mice. Mol Cell Biol, 24, 9848-9862.
84. Misra, R., CastilloKeller, M. & Deng, M. (2000). Overexpression of protease-deficient DegPS210A rescues the lethal phenotype of Escherichia coli OmpF assembly mutants in a degP background. J Bacteriol, 182, 4882-4888.
85. Mo, E., Peters, S. E., Willers, C., Maskell, D. J. & Charles, I. G. (2006). Single, double and triple mutants of Salmonellaenterica serovar Typhimurium degP (htrA), degQ (hhoA) and degS (hhoB) have diverse phenotypes on exposure to elevated temperature and their growth in vivo is attenuated to different extent. Microb Pathog, 41, 174-182.
86. Mogensen, J. E. & Otzen, D. E. (2005). Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol, 57, 326-346.
87. Morton, M., Garmory, H. S., Perkins, S. D., O'Dowd A. M., Griffin, K. F., Turner, A. K., Bennet, A. M. & Titball, R. W. (2004). A Salmonella enterica serover Typhi vaccine expressing Yersinia pestis F1 antigen on its surface provides protection against plague in mice. Vaccine, 22, 2524-2532.
88. Mukhopadhyay, S., Good, D., Miller, R. D., Graham, J. E., Mathews S. A., Timms, P. & Summersgill, J. T. (2006). Identification of Chlamydia pneumoniae proteins in the transition from reticulate to elementary body formation. Mol Cell Proteom, 5, 2311-2318.
89. Nakamoto, H. & Bardwell, J. C. A. (2004). Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim Biophys Acta, 1694, 111-119.
90. Nie, G.-Y., Hampton, A., Li, Y., Findlay, J. K. & Salamonsen, L. A. (2003a). Identification and cloning of two isoforms of human high-temperature requirement factor A3 (HtrA3), characterization of its genomic structure and comparison of its tissue distribution with HtrA1 and HtrA2. Biochem J, 371, 39-48.
91. Nie, G.-Y., Li, Y., Hale, K., Okada, H., Manuelpillai, U., Wallace, E. M. & Salamonsen, L. A. (2006). Serine protease HtrA3 is closely associated with human plancetal development and is elevated in pregnancy serum. Biol Reprod, 74, 366-374.
92. Nie, G.-Y., Li, Y., Minoura, H., Batten, L. & Ooi, G. T. (2003b). A novel serine protease of the mammalian HtrA family is up-regulated in mouse uterus coinciding with plancentation. Mol Hum Reprod, 9, 279-290.
93. Noone, D., Howell, A., Collery, R. & Devine, K. M. (2001). YkdA and YvtA, HtrA-like serine proteases in Bacillus subtilis, engage in negative autoregulation and reciprocal cross-regulation of ykdA and yvtA gene expression. J Bacteriol, 183, 654-663.
94. Noone, D., Howell, A., Rigoulay, C., Entenza, J. M., Halpern, D., Widmer, E., Moreillon, P., Poquet, I. & Gruss, A. (2005). Comparative Analysis of the Roles of HtrA-Like Surface Proteases in Two Virulent Staphylococcus aureus Strains. Infect Immun, 73, 563-572.
95. Oka, C., Tsujimoto, R., Kajikawa, M., Koshiba-Takeuchi, K., Ina, J., Yano, M., Tsuchiya, A., Ueta, Y., Soam, A., Kanda, H., Matsumoto, M. & Kawaichi, M. (2003). HtrA1 serine protease inhibits signaling mediated by Tgfβ family proteins. Development, 131, 1041-1053.
96. Pallen, B. W. & Wren, M. J. (1997). The HtrA family of serine proteases. Mol Microbiol, 26, 209-221.
97. Park, H.-J., Kim, S.-S., Seong, Y.-M., Kim, K.-H., Goo, H. G., Yoon, E. J., Min, D. S., Kang, S. & Rhim, H. (2006). β-Amyloid Precursor Protein Is a Direct Cleavage Target of HtrA2 Serine Protease. Implications for the Physiological Function of HtrA2 in the Mitochondria. J Biol Chem, 281, 34277-34287.
98. Park, H.-J., Song, Y. M., Choi, J. Y., Kang, S. & Rhim, H. (2004). Alzheimer's diseaseassociated amyloid beta interacts with the human serine protease HtrA2/Omi. Neurosci Lett, 357, 63-67.
99. Paseti, M. F., Pickett, T. E., Levine, M. M. & Sztein, M. B. (2000). A comparison of immunogenicity and in vivo distribution of Salmonella enterica serover Typhi and Typhimurium live vector vaccine delivered by mucosal routes in the murine model. Vaccine, 18, 3208-3213.
100. Pedersen, L., L., Radulic, M., Doric, M., Abu Kwaik, J. (2001) HtrA homologue of Legionella pneumophila: an indispensable element for intracellular infection of mammalian but not protozoan cells. Infect Immun, 69, 2569-2579.
101. Phillips, R. W. & Roop II R. M. (2001). Brucella abortus HtrA functions as an authentic stress response protease but is not required for wild-type virulence in BALB/c mice. Infect Immun, 69, 5911-5913.
102. Plun-Favreau, H., Klupsch, K., Moisoi, N., Gandhi, S., Kjaer, S., Frith, D., Harvey, K., Deas, E., Harvey, R. J., McDonald, N., Wood, N. W., Martins, L. M. & Downward J. (2007). The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat Cell Biol, 9, 1243-1252.
103. Poquet, I., Saint, V., Seznec, E., Simoes, N., Bolotin, A. & Gruss, A. (2000). HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol Microbiol, 35, 1042-1051.
104. Raivio, T. L. (2005). Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol, 56, 1119-1128.
105. Redford, P. & Welch, R. A. (2006). Role of sigma E-regulated genes in Escherichia coli uropathogenesis. Infect Immun, 74, 4030-4038.
106. Rigoulay, C., Entenza, J. M., Halpern, D., Widmer, E., Moreillon, P., Poquet, I. & Gruss, A. (2005). Comparative Analysis of the Roles of HtrA-Like Surface Proteases in Two Virulent Staphylococcus aureus Strains. Infect Immun, 73, 563-572.
107. Rizzitello, A. E., Harper, J. R. & Silhavy, T. (2001). Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol, 183, 6794-6800.
108. Roy, F., Vanterpool, E. & Fletcher, H. M. (2006). HtrA in Porphyromonas gingivalis can regulate growth and gingipain activity under stressful experimental conditions. Microbiol, 152, 3391-3398.
109. Rozenkranz, C. D., Chiara, D., Agorio, C., Baz, A., Pasetti, M. F., Schreiber, F., Dematteis, S., Martinez, M., Sztein, M. B. & Chabalgoity, J. A. (2003). Towards New Immunotherapies: Targeting Recombinant Cytokines to the Immune System using Live Attenuated Salmonella. Vaccine, 21, 798-801.
110. Ruiz, N. & Silhavy, T. J. (2005). Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol, 8, 122-126.
111. Salerno-Goncalves, R., Wyant, T. L., Pasetti, M. F., Fernandez-Vina, M., Tacket, C. O., Levine, M. M. & Sztein, M. B. (2003). Concomitant Induction of CD4+ and CD8+ T cell Responses in Volunteers Immunizes with Salmonella enterica Serovar Thypi Strain CVD 908-htrA. J Immunol 170: 2734-2741.
112. Sarvas, M., Harwood, C., R., Bron, S., van Dijl, J., M. (2004) Post-translational folding of secretory proteins in Gram-positive bacteria. Biochim. Biophys. Acta 1694, 311-327.
113. Sauer, F. G., Futterer, K., Pinkner, J. S., Dodson, K. W., Hultgren, S. J. & Waksman, G. (1999). Structural basis of chaperone function and pilus biogenesis. Science, 285, 1058-1061.
114. Schon, E. A. & Manfredi, G. (2003). Neuronal degeneration and mitochondrial dysfunction. J Clin Invest, 111, 303-312.
115. 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. & 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.
116. Seong, Y.-M., Choi, J.-Y., Park, H.-J., Kim, K.-J., Ahn, S.-G., Seong, G.-H., Kim, I.-K., Kang, S. & Rhim, H. (2004). Autocatalytic Processing of HtrA2/Omi Is Essential for Induction of Caspase-dependent Cell Death through Antagonizing XIAP. J Biol Chem, 279, 37588-37596.
117. Serra, R., Johnson, M., Filvaroff, E. H., LaBorde, J., Sheehan, D. M., Derynck, R. & Moses, H. L. (1997). Expression of truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol, 139, 541-552.
118. Shi, Y. & Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 113, 685-700.
119. Shi, Y. (2004). Caspase activation, inhibition and reactivation: A mechanistic view. Prot Sci, 13, 1979-1987.
120. Silvestri, L., Capato, V., Bellacchio, E., Atorino, L., Dallapiccola, B., Valente, E.M. & Casari, G. (2005). Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet, 14, 3477-3492.
121. Skorko-Glonek, J., Wawrzynow, A., Krzewski, K., Kurpierz, K. & Lipińska, B. (1995). Sitedirected mutagenesis of the HtrA (DegP) serine protease, whose proteolytic activity is indispensable for Escherichia coli survival at elevated temperatures. Gene, 163, 47-52.
122. Skorko-Glonek, J., Zurawa, D., Kuczwara, E., Wozniak, M., Wypych, Z. & Lipinska, B. (1999). Escherichia coli heat shock HtrA protease participates in the defense against oxidative stress. Mol Gen Genet, 262, 342-350.
123. Skorko-Glonek, J., Zurawa, D., Tanfani, F., Scire, A., Wawrzynow, A., Narkiewicz, J. & Lipinska, B. (2003). The N-terminal region of HtrA heat shock protease from Escherichia coli is essential for stabilization of HtrA primary structure and maintaining of its oligomeric structure. Biochim Biophys Acta, 1649, 171-182.
124. Skorko-Glonek, J., Laskowska, E., Sobiecka-Szkatula, A., Lipinska, B. (2007) Characterization of the chaperone-like activity of HtrA (DegP) protein from Escherichia coli under the conditions of heat shock. Arch. Bioch. Biophys, 464, 80-89.
125. Sohn, J., Grant, R. A., Sauer, R. T. (2007) Allosteric activation of DegS, a stress sensor PDZ protease. Cell 131, 572-583.
126. Sone, M., Kishigami, S., Yoshihisa, T. & Ito, K. (1997). Roles of disulfide bonds in bacterial alkaline phosphatase. J Biol Chem, 272, 6174-6178.
127. Spiess, C., Beil, A. & Ehrmann, M. (1999). A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell, 97, 339-347.
128. Srinivasula, S. M., Gupta, S., Datta, P., Zhang, Z. J., Hedge, R., Cheong, N., Fernandes-Alnemri, T. & Alnemri, E. S. (2003). Inhibitor of Apoptosis Proteins Are Substrates for the Mitochondrial Serine Protease Omi/HtrA2. J Biol Chem, 278, 31469-31472.
129. Stack, H. M., Sleator, R. D., Bowers, M., Hill, C. & Gahan, C. G. M. (2005). Role for HtrA in stress induction and virulence potential in Listeria monocytogenes. Appl Environ Microbiol, 71, 4241-4247.
130. Strauch, K. L. & Beckwith, J. (1988). An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc Natl Acad Sci USA, 85, 1576-1580.
131. Strauch, K. L., Johnson K., 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.
132. Strauss, K. M., Martins, L. M., Plun-Favreau, H., Marx, F. P., Kautzmann, S., Berg, D., Gasser, T., Wszolek, Z., Muller, T., Bornemann, A., Wolburg, H., Downward, J., Riess, O., Schulz, J. B. & Kruger, R. (2005). Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum Mol Genet, 14, 2099-2111.
133. Swamy, K. H. S., Chung, C. H., Goldberg, A. L. (1983). Isolation and characterization of protease Do, a large serine protease containing multiple subunits. Arch Biochem Biol, 224, 543-554.
134. Tacket, C. O., Galen, J., Sztein, M. B., Losonsky, G. A., Wyant, T. L., Nataro, P., Wasserman, S. S., Edelman, R., Chatfield, S. N., Dougan, G., & Levine, M. M. (2000b). Safety and Immune Responses to Attenuated Salmonella enterica Serovar Typhi Oral Vaccines Expressing Tetanus Toxin Fragment C. Clin Immunol, 97, 146-153.
135. Tacket, C. O., Sztein, M. B., Losonsky, G. A., Wassreman, S. S., Nataro, P., Edelman, R., Pickard, D., Dougan, Chatfield, S. N. & Levine, M. M. (1997). Safety of oral Salmonella typhi vaccine strains with deletions in htrA and aroA aroC and immune response in human. Infect Immun, 65, 452-456.
136. Tacket, C. O., Sztein, M. B., Wassreman, S. S., Losonsky, G. A., Kotloff, K. L., Wzant, T. L., Nataro, P., Edelman, R., Perry, J., Bedford, P., Brown, D., Chatfield, S. N., Dougan, G., & Levine, M. M. (2000a). Phase 2 clinical trial of attenuated Salmonella enterica serovar Typhi oral live vaccine CVD 908-htrA in US volunteers. Infect Immun, 68, 1196-1201.
137. Tocharus, J., Tsuchiya, A., Kajikawa, M., Ueta, Y., Oka, C. & Kawaichi, M. (2004). Developmentally regulated expression of Mouse HtrA3 and its role as an inhibitor of TGF-β signaling. Dev Growth Differ, 46, 257-274.
138. Trencia, A., Fiory, F., Maitan, M. A., Vito, P., Barbagallo, A. P. M., Perfetti, A., Miele, C., Ungaro, P., Oriente, F., Cilenti, L., Zervos, A. S., Formisano, P. & Beguinot, F. (2004). Omi/HtrA2 Promotes Cell Death by Binding and Degrading the Anti-apoptotic Protein ped/pea15. J Biol Chem, 279, 46566-46572.
139. Tsuchiya, A., Yano, M., Tocharus, J., Kojami, H., Fukumoto, M., Kawaichi, M. & Oka, C. (2005). Expression of mouse HtrA1 serine protease in normal bone and cartilage and its upregulation in joint cartilage damaged by experimental arthritis. Bone, 37, 323-336.
140. van der Kraan, P. M., Vitters, E. L. & van den Berg, W. B. (1992). Inhibition of proteoglycan synthesis by transforming growth factor beta in anatomically intact articular cartilage of mature patelle. Ann Rheum Dis, 51, 643-647.
141. Vaux, D. L. & Silke, J. (2003). Mammalian mitochondrial IAP binding proteins. Biochem Biophys Res Commun, 304, 499-504.
142. Verhagen, A. M., Silke, J., Ekert, P. G., Pakush, M., Kaufmann, H., Connolly, L. M., Day, C. L., Tikoo, A., Burke, R., Wrobel, C., Moritz, R. L., Simpson, R. J. & Vaux, D. L. (2002). HtrA2 Promotes Cell Death through Its Serine Protease Activity and Its Ability to Antagonize Inhibitor of Apoptosis Proteins. J Biol Chem, 277, 445-454.
143. Wahid, R., Salerno-Goncalves, R., Tacket, C. O., Levine, M. M. & Sztein, M. B. (2007). Cell-mediated immune response in humans after immunization with one or two doses of oral live attenuated typhoid vaccine CVD 909. Vaccine, 25, 1416-1425.
144. Waller, P. R. & Sauer, R. T. (1996). Characterization of degQ and degS Escherichia coli genes encoding homologs of the DegP protease. J Bacteriol, 178, 1146-1153.
145. Walsh, N. P., Alba, B. M., Bose, B., Gross, C. A. & Sauer, R. T. (2003). OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief on inhibition mediated by its PDZ domain. Cell, 113, 61-71.
146. Walter, D., Wissing, S., Madeo, F. & Fahrenkrog, B. (2006). The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is s substrate for the yeast homologue of Omi/HtrA2. J Cell Sci, 119, 1843-1851.
147. Wang, J.-Y., Noriega, F.R., Galen, J.E., Barry, E. and Levine, M.M. (2000). Constitutive expression of the Vi polysaccharide capsular antigen in attenuated Salmonella enterica serovar Typhi oral vaccine strain CVD 909. Infect. Immun. 68, 4647-4652.
148. Wilken, C., Kitzing, K., Kurzbauer, R. & Ehrmann, M. (2004). Crystal Structure of the DegS Stress Sensor: How PDZ Domain Recognizes Misfolded Protein and Activates a Protease. Cell, 117, 483-494.
149. Williams, K., Oyston, P. C. F., Dorrell, N., Li, S.-R., Titball, R. W. & Wren, B. W. (2000). Investigation into the role of the serine protease HtrA in Yersinia pestis pathogenesis. FEMS Microbiol Lett, 186, 281-286.
150. Wilson, R. L., Brown, L. L., Kirkwood-Watts, D., Warren, T. K., Lund, S. A., King, D. S., Jones, K. F. & Hruby, D. E. (2006). Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence. Infect Immun, 74, 765-768.
151. Wonderling, L. D., Wilkinson, B. J. & Bayles, D. O. (2004). The HtrA (DegP) gene of Listeria monocytogenes 10403S is essential for optimal growth under stress conditions. Appl Environ Microbiol, 70, 1935-1943.
152. Wood, L. F. & Ohman, D. E. (2006). Independent regulation of MucD, an HtrA-like protease in Pseudomonas aeruginosa, and the role of its proteolytic motif in alginate gene regulation. J Bacteriol, 188, 3134-3137.
153. Wootton, J. C. & Drummond, M. H. (1989). The Q-linker-a class of interdomain sequences found in bacterial multidomain regulatory proteins. Proteins Eng, 2, 535-543.
154. Yang, H., Chen, L., Xu, X., Li, C., Huang, C. & Deng, C. X. (2001). TGF-beta/Smad3 signals repress chondrocyte hypertophic differentiation and are required for maintaining articular cartilage. J Cell Biol, 153, 35-46.
155. Yang, L., Sun, M., Sun, X., Cheng, G. Z., Nikosia, S. V. & Cheng, J. Q. (2007). Akt Attenuation of the Serine Protease Activity of HtrA2/Omi through Phosphorylation of Serine 212. J Biol Chem, 282, 10981-10987.
156. Yang, Q. H., Church-Hajduk, R., Ren, J., Newton, N. L., Du, C. (2003). Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAP and facilities caspase activity in apoptosis. Genes Dev, 17, 1487-1496.
157. Yorgey, P., Rahme, L. G., Tan, M. W. & Ausubel, F. M. (2001). The roles of mucD and alginate in the virulence of Pseudomonas aeruginosa in plants, nematodes and mice. Mol Microbiol, 41, 1063-1076.
158. Zeth, K. (2004). Structural analysis of DegS, a stress sensor of the bacterial periplasm. FEBS Lett, 569, 351-358.
159. Zumbrunn, J. & Treub, B. (1996). Primary structure of a putative serine protease specific for IGF-binding proteins. FEBS Letters, 398, 187-192.
160. Zumbrunn, J. & Trueb, B. (1997). Localization of the gene for a serine protease with IGFbinding domain (PRSS11) to human chromosome 10q25.3-q26.2. Genomics, 45, 461-465.