Regulation of bacterial protease activity

• Autorzy: Wladyka B , Pustelny K.
• Języki publikacji: EN

Abstrakty

EN

Proteases, also referred to as peptidases, are the enzymes that catalyse the hydrolysis of peptide bonds in polipeptides. A variety of biological functions and processes depend on their activity. Regardless of the organism’s complexity, peptidases are essential at every stage of life of every individual cell, since all protein molecules produced must be proteolytically processed and eventually recycled. Protease inhibitors play a crucial role in the required strict and multilevel control of the activity of proteases involved in processes conditioning both the physiological and pathophysiological functioning of an organism, as well as in host-pathogen interactions. This review describes the regulation of activity of bacterial proteases produced by dangerous human pathogens, focusing on the Staphylococcus genus.

Słowa kluczowe

EN

protease; protease activity; protease inhibition; enzyme; biological function; protein molecule; host-pathogen interaction; human pathogen; Staphylococcus

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2008
• Tom: 13
• Numer: 2
• Opis fizyczny: p.212-229,fig.,ref.

Twórcy

autor

Wladyka B

• Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland

autor

Pustelny K.

Bibliografia

• 1. Potempa, J. and Pike, R.N. Bacterial peptidases. In: Concepts in Bacterial Virulence (Russell, W., Herwald, H. Eds.) Contrib Microbiol. Basel, Karger, 12 (2005) 132-180.
• 2. Yamaguchi, T., Hayashi, T., Takami, H., Nakasone, K., Ohnishi, M., Nakayama, K., Yamada, S., Komatsuzawa, H. and Sugai, M. Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol. Microbiol. 38 (2000) 694-705.
• 3. Yamaguchi, T., Hayashi, T., Takami, H., Ohnishi, M., Murata, T., Nakayama, K., Asakawa, K., Ohara, M., Komatsuzawa, H. and Sugai, M. Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyltransferase, EDIN-C. Infect. Immun. 69 (2001) 7760-7771.
• 4. Rice, K., Peralta, R., Bast, D., De Azavedo, J. and McGavin, M.J. Description of staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease. Infect. Immun. 69 (2001) 159-169.
• 5. Massimi, I., Park, E., Rice, K., Muller-Esterl, W., Sauder, D. and McGavin, M.J. Identification of a novel maturation mechanism and restricted substrate specificity for the SspB cysteine protease of Staphylococcus aureus. J. Biol. Chem. 277 (2002) 41770-41777.
• 6. Rzychon, M., Sabat, A., Kosowska, K., Potempa, J. and Dubin, A. Staphostatins: an expanding new group of proteinase inhibitors with a unique specificity for the regulation of staphopains, Staphylococcus spp. cysteine proteinases. Mol. Microbiol. 49 (2003) 1051-1066.
• 7. Dubin, G., Krajewski, M., Popowicz, G., Stec-Niemczyk, J., Bochtler, M., Potempa, J., Dubin, A. and Holak, T.A. A novel class of cysteine protease inhibitors: solution structure of staphostatin A from Staphylococcus aureus. Biochemistry 42 (2003) 13449-13456.
• 8. Shaw, L., Golonka, E., Potempa, J. and Foster, S.J. The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology 150 (2004) 217-228.
• 9. Takeuchi, S., Kinoshita, T., Kaidoh, T. and Hashizume, N. Purification and characterization of protease produced by Staphylococcus aureus isolated from a diseased chcken. Vet. Microbiol. 67 (1999) 195-202.
• 10. Takeuchi, S., Matsunaga, K., Inubushi, S., Higuchi, H., Imaizumi, K. and Kaidoh, T. Structural gene and strain specificity of a novel cysteine protease produced by Staphylococcus aureus isolated from a diseased chicken. Vet. Microbiol. 89 (2002) 201-210.
• 11. Dubin, G., Wladyka, B., Stec-Niemczyk, J., Chmiel, D., Zdzalik, M., Dubin, A. and Potempa, J. The staphostatin family of cysteine protease inhibitors in Staphylococcus genus as an example of parallel evolution of protease and inhibitor specificity. Biol. Chem. 388 (2007) 227-235.
• 12. Dubin, G., Stec-Niemczyk, J., Dylag, T., Silbering, J., Dubin, A. and Potempa, J. Characterisation of a highly specific, endogenous inhibitor of cysteine protease from Staphylococcus epidermidis, a new member of the staphostatin family. Biol. Chem. 385 (2004) 543-546.
• 13. Potempa, J., Golonka, E., Filipek, R. and Shaw, L.N. Fighting an enemy within: cytoplasmic inhibitors of bacterial cysteine proteases. Mol. Microbiol. 57 (2005) 605-610.
• 14. Reed, S.B., Wesson, C.A., Liou, L.E., Trumble, W.R., Schlievert, P.M., Bohach, G.A. and Bayles, K.W. Molecular characterization of a novel Staphylococcus aureus serine protease operon. Infect. Immun. 69 (2001) 1521-1527.
• 15. Duong, F., Lazdunski, A., Cami, B. and Murgier, M. Sequence of a cluster of genes controlling synthesis and secretion of alkaline proteinase in Pseudomonas aeruginosa: relationships to other secretory pathways. Gene 121 (1992) 47-54.
• 16. Kagawa, T.F., O’Toole, P.W. and Cooney, J.C. SpeB-Spi: a novel proteaseinhibitor pair from Streptococcus pyogenes. Mol. Microbiol. 57 (2005) 650- 666.
• 17. Rzychon, M., Filipek, R., Sabat, A., Kosowska, K., Potempa, J., Dubin, A. and Bochtler, M. Staphostatins resemble lipocalins, not cystatins in fold. Protein Sci. 12 (2003) 2252-2256.
• 18. Recsei, P., Kreiswirth, B., O’Reilly, M., Schlievert, P., Gruss, A. and Novick, R.P. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol. Gen. Genet. 202 (1986) 58-61.
• 19. Bayer, M.G., Heinrichs, J.H. and Cheung, A.L. The molecular architecture of the sar locus in Staphylococcus aureus. J. Bacteriol. 178 (1996) 4563- 4570.
• 20. Novick, R.P., Projan, S.J., Kornblum, J., Ross, H.F., Ji, G., Kreiswirth, B.,Vandenesch, F. and Moghazeh, S. The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol. Gen. Genet. 248 (1995) 446-458.
• 21. Ji, G., Beavis, R.C. and Novick, R.P. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl. Acad. Sci. USA 92 (1995) 12055-12059.
• 22. Gambello, M.J., Kaye, S. and Iglewski, B.H. LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect. Immun. 61 (1993) 1180- 1184.
• 23. Passador, L., Cook, J.M., Gambello, M.J., Rust, L. and Iglewski, B.H. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260 (1993) 1127-1130.
• 24. Heinrichs, J.H., Bayer, M.G. and Cheung, A.L. Characterization of the sar locus and its interactions with agr in Staphylococcus aureus. J. Bacteriol. 178 (1996) 418-423.
• 25. Cheung, A.L., Bayer, M.G. and Heinrichs, J.H. sar genetic determinants necessary for transcription of RNAII and RNAIII in the agr locus of Staphylococcus aureus. J. Bacteriol. 179 (1997) 3963-3971.
• 26. Chien, Y., Manna, A.C., Projan, S.J. and Cheung, A.L. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J. Biol. Chem. 274 (1999) 37169-37176.
• 27. Chan, P.F. and Foster, S.J. Role of SarA in virulence determinant production and environmental signal transduction in Staphylococcus aureus. J. Bacteriol. 180 (1998) 6232-6241.
• 28. McNamara, P.J., Milligan-Monroe, K.C., Khalili, S. and Proctor, R.A. Identification, cloning, and initial characterization of rot, a locus encoding a regulator of virulence factor expression in Staphylococcus aureus. J. Bacteriol. 182 (2000) 3197-3203.
• 29. Saïd-Salim, B., Dunman, P.M., McAleese, F.M., Macapagal, D., Murphy, E., McNamara, P.J., Arvidson, S., Foster, T.J., Projan, S.J. and Kreiswirth, B.N. Global regulation of Staphylococcus aureus genes by Rot. J. Bacteriol. 185 (2003) 610-619.
• 30. Horsburgh, M., Aish, J., White, I., Shaw, L., Lithgow, J. and Foster, S. SigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184 (2002) 5457-5467.
• 31. Shaw, L.N., Golonka, E., Szmyd, G., Foster, S.J., Travis, J. and Potempa, J. Cytoplasmic control of premature activation of a secreted protease zymogen: deletion of staphostatin B (SspC) in Staphylococcus aureus 8325-4 yields a profound pleiotropic phenotype. J. Bacteriol. 187 (2005) 1751-1762.
• 32. Lowther, W.T. and Matthews, B.W. Structure and function of the methionine aminopeptidases. Biochim. Biophys. Acta 1477 (2000) 157-167.
• 33. Tuteja, R. Type I signal peptidase: an overview. Arch. Biochem. Biophys. 441 (2005) 107-111.
• 34. Neurath, H. The versatility of proteolytic enzymes. J. Cell Biochem. 32 (1986) 35-49.
• 35. Vasantha, N., Thompson, L.D., Rhodes, C., Banner, C., Nagle, J. and Filpula, D. Genes for alkaline protease and neutral protease from Bacillus amyloliquefaciens contain a large open reading frame between the regions coding for signal sequence and mature protein. J. Bacteriol. 159 (1984) 811-819.
• 36. Zhu, X., Ohta, Y., Jordan, F. and Inouye, M. Pro-sequence of subtilisin can guide the refolding of denatured subtilisin in an intermolecular process. Nature 339 (1989) 483-484.
• 37. Sabat, A., Kosowska, K., Poulsen, K., Kasprowicz, A., Sekowska, A., van der Burg, B., Travis, J. and Potempa, J. Two allelic forms of the aureolysin gene (aur) within Staphylococcus aureus. Infect. Immun. 68 (2000) 973-976.
• 38. Miyoshi, S. and Shinoda, S. Microbal metalloproteases and pathogenesis. Microbes Infect. 2 (2000) 91-98.
• 39. Carmona, C. and Gray, G.L. Nucleotide sequence of the serine protease gene of Staphylococcus aureus, strain V8. Nucleic Acids Res. 15 (1987) 6757.
• 40. Yoshikawa, K., Tsuzuki, H., Fujiwara, T., Nakamura, E., Iwamoto, H., Matsumoto, K., Shin, M., Yoshida, N. and Teraoka, H. Purification, characterization and gene cloning of a novel glutamic acid-specific endopeptidase from Staphylococcus aureus ATCC 12600. Biochim. Biophys. Acta 1121 (1992) 221-228.
• 41. Beaudet, R., Saheb, S.A. and Drapeau, G.R. Structural heterogenicity of the protease isolated from several strains of Staphylococcus aureus. J. Biol. Chem. 249 (1974) 6468-6471.
• 42. Drapeau, G.R. Role of a metalloprotease in activation of the precursor of staphylococcal protease. J. Bacteriol. 136 (1978) 607-613.
• 43. Lindsay, J. and Foster, S. Interactive regulatory pathways control virulence determinant production and stability in response to the environment in Staphylococcus aureus. Mol. Gen. Genet. 262 (1999) 323-331.
• 44. Filipek, R., Szczepanowski, R., Sabat, A., Potempa, J. and Bochtler, M. Prostaphopain B structure: a comparison of proregion-mediated and staphostatin-mediated protease inhibition. Biochemistry 43 (2004) 14306- 14315.
• 45. Popowicz, G.M., Dubin, G., Stec-Niemczyk, J., Czarny, A., Dubin, A., Potempa, J. and Holak, T.A. Functional and structural characterization of Spl proteases from Staphylococcus aureus. J. Mol. Biol. 358 (2006) 270-279.
• 46. Rasmussen, M. and Björck, L. Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol. Microbiol. 43 (2002) 537-544.
• 47. Kagawa, T.F., Cooney, J.C., Baker, H.M., McSweeney, S., Liu, M., Gubba, S., Musser, J.M. and Baker, E.N. Crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease. Proc. Natl. Acad. Sci. USA 97 (2000) 2235-2240.
• 48. Doran, J.D., Nomizu, M., Takebe, S., Ménard, R., Griffith, D. and Ziomek, E. Autocatalytic processing of the streptococcal cysteine protease zymogen: processing mechanism and characterization of the autoproteolytic cleavage sites. Eur. J. Biochem. 263 (1999) 145-151.
• 49. Braun, P., de Groot, A., Bitter W. and Tommassen, J. Secretion of elastolytic enzymes and their propeptides by Pseudomonas aeruginosa. J. Bacteriol. 173 (1998) 3467-3469.
• 50. Miyoshi, S., Wakae, H., Tomochika, K. and Shinoda, S. Functional domains of a zinc metalloprotease from Vibrio vulnificus. Infect. Immun. 179 (1997) 7606-7609.
• 51. Prokesová, L., Porwit-Bobr, Z., Baran, K., Potempa, J., Pospisil, M. and John, C. Effect of metalloproteinase from Staphylococcus aureus on in vitro stimulation of human lymphocytes. Immun. Lett. 27 (1991) 225-230.
• 52. Potempa, J., Watorek, W. and Travis, J. The inactivation of human plasma α1-proteinase inhibitor by proteinases form Staphylococcus aureus. J. Biol. Chem. 261 (1986) 14330-14334.
• 53. Potempa, J., Fedak, D., Dubin, A., Mast, A. and Travis, J. Proteolytic inactivation of α-1-antichymotrypsin. Sites of cleavage and generation of chemotactic activity. J. Biol. Chem. 266 (1991) 21482-21487.
• 54. Amagai, M., Matsuyoshi, N., Wang, Z.H., Andl, C. and Stanley, J.R. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nature Med. 6 (2000) 1275-1277.
• 55. Arvidson, S. Extracellular enzymes. In: Gram-Positive Pathogens (Fischetti, V.A., Novick, R.P., Ferretti, J.J., Portnoy, D.A. and Rood, J.I. Eds.) Washington, D.C., USA, American Society for Microbiology, pp. 379- 385.
• 56. Potempa, J., Dubin, A., Korzus, G. and Travis, J. Degradation of elastin by a cysteine proteinase from Staphylococcus aureus. J. Biol. Chem. 263 (1988) 2664-2667.
• 57. Imamura, T., Tanase, S., Szmyd, G., Kozik, A., Travis, J. and Potempa, J. Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus. J. Exp. Med. 201 (2005) 1669-1676.
• 58. Rieneck, K., Rennenberg, J., Diamant, M., Gutschik, E. and Bendtzen, K. Molecular cloning and expression of novel Staphylococcus aureus antigen. Biochim. Biophys. Acta 44 (1997) 128-132.
• 59. Matsumoto, K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol. Chem. 385 (2004) 1007-1016.
• 60. Dubin, G., Popowicz, G., Krajewski, M., Potempa, J., Dubin, A. and Holak, T.A. 1H, 15N and 13C NMR resonance assignments of staphostatin A, a specific Staphylococcus aureus cysteine proteinase inhibitor. J. Biomol. NMR 28 (2004) 295-296.
• 61. Filipek, R., Rzychon, M., Oleksy, A., Gruca, M., Dubin, A., Potempa, J. and Bochtler, M. The staphostatin-staphopain complex: a forward binding inhibitor in complex with its target cysteine protease. J. Biol. Chem. 278 (2003) 40959-40966.
• 62. Dubin, G. Defense against own arms: staphylococcal cysteine proteases and their inhibitors. Acta Biochim. Polon. 50 (2003) 715-724.
• 63. Wladyka, B., Puzia, K. and Dubin, A. Efficient co-expression of a recombinant staphopain A and its inhibitor staphostatin A in Escherichia coli. Biochem. J. 385 (2005) 181-187.
• 64. Herwald, H., Collin, M., Muller-Esterl, W. and Björck, L. Streptococcal cysteine proteinase releases kinins: a virulence mechanism. J. Exp. Med. 184 (1996) 665-673.
• 65. Schroeter, J.P., Kolodziej, S.J., Wagenknecht, T., Bretaudiere, J.P., TaponBretaudiere, J., Strickland, D.K. and Stoops, J.K. Three-dimensional structures of the human alpha 2-macroglobulin-methylamine and chymotrypsin complexes. J. Struct. Biol. 109 (1992) 235-247.
• 66. Starkey, P.M. and Barrett, A.J. Inhibition by α-macroglobulin and other serum proteins. Biochem. J. 131 (1973) 823-831.
• 67. Sottrup-Jensen, L., Sand, O., Kristensen, L. and Fey, G.H. The α-macroglobulin bait region. Sequence diversity and localization of cleavage sites for proteinases in five mammalian α-macroglobulins. J. Biol. Chem. 264 (1989) 15781-15789.
• 68. Maeda, S., Molla, T., Oda, A. and Katsuki, T. Internalization of serratia1 protease into cells as an enzyme-inhibitor complex with α2-macroglobulin and regeneration of protease activity and cytotoxicity. J. Biol. Chem. 262 (1987) 10946-10950.
• 69. Nyberg, P., Rasmussen, M. and Björck, L. α2-macroglobulin-proteinase complexes protect Streptococcus pyogenes from killing by the antimicrobal peptide LL-37. J. Biol. Chem. 279 (2004) 52820-52823.
• 70. Giles, N.M., Watts, A.B., Giles, G.I., Fry, F.H., Littlechild, J.A. and Jacob, C. Metal and redox modulation of cysteine protein function. Chem. Biol. 10 (200) 3677-1093.
• 71. Wasylewski, Z., Stryjewski, W., Wasniowska, A., Potempa, J. and Baran, K. Effect of calcium binding on conformational changes of staphylococcal metalloproteinase measured by means of intrinsic protein fluorescence. Biochim. Biophys. Acta 871 (1986) 177-181.
• 72. Potempa, J., Porwit-Bobr, Z. and Travis, J. Stabilization vs. degradation of Staphylococcus aureus metalloproteinase. Biochim. Biophys. Acta 993 (1989) 301-304.
• 73. Gottesman, S. Regulation by proteolysis: developmental switches. Curr. Opin. Microbiol. 2 (1999) 142-147.
• 74. Hoskins, J.R., Singh, A.K., Maurizi, M.R. and Wickner, S. Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl. Acad. Sci. USA 97 (2000) 8892-8897.
• 75. Frees, D., Qazi, S.N., Hill, P.J. and Ingmer, H. Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol. Microbiol. 48 (2003) 1565-1578.
• 76. Frees, D., Sørensen, K. and Ingmer, H. Global virulence regulation in Staphylococcus aureus: pinpointing the roles of ClpP and ClpX in the sar/agr regulatory network. Infect. Immun. 73 (2005) 8100-8108.
• 77. Butler, S.M., Festa, R.A., Pearce, M.J. and Darwin, K.H. Selfcompartmentalized bacterial proteases and pathogenesis. Mol. Microbiol. 60 (2006) 553-562.
• 78. Brötz-Oesterhelt, H., Beyer, D., Kroll, H.P., Endermann, R., Ladel, C., Schroeder, W., Hinzen, B., Raddatz, S., Paulsen, H., Henninger, K., Bandow, J.E., Sahl, H.G. and Labischinski, H. Disregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat. Med. 11 (2005) 1082-1087.
• 79. Spiess, C., Beil, A. and Ehrmann, M. A temperature-dependent switch from chaperon to protease in widely conserved heat shock protein. Cell 97 (1999) 339-347.
• 80. Clausen, T., Southan, C. and Ehrmann, M. The HrtA family of proteases: implications for protein coposition and cell fate. Mol. Cell 10 (2002) 443-455.