Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C

Kalinska M, Kantyka T, Greenbaum DC, Larsen KS, Wladyka B, Jabaiah A, Bogyo M, Daugherty PS, Wysocka M, Jaros M, Lesner A, et al. (2012)
Biochimie 94(2): 318-327.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
DOI
Autor*in
Kalinska, Magdalena; Kantyka, Tomasz; Greenbaum, Doron C.; Larsen, Katrine S.; Wladyka, Benedykt; Jabaiah, Abeer; Bogyo, Matthew; Daugherty, Patrick S.; Wysocka, Magdalena; Jaros, Marcelina; Lesner, Adam; Rolka, Krzysztof
Alle
Einrichtung
Fakultät für Chemie
Centrum für Biotechnologie > Arbeitsgruppe N. Schaschke
Abstract / Bemerkung
Human strains of Staphylococcus aureus secrete two papain-like proteases, staphopain A and B. Avian strains produce another homologous enzyme, staphopain C. Animal studies suggest that staphopains B and C contribute to bacterial virulence, in contrast to staphopain A. which seems to have a virulence unrelated function. Here we present a detailed study of substrate preferences of all three proteases. The specificity of staphopain A, B and C substrate-binding subsites was mapped using different synthetic substrate libraries, inhibitor libraries and a protein substrate combinatorial library. The analysis demonstrated that the most efficiently hydrolyzed sites, using Schechter and Berger nomenclature, comprise a P2-Gly down arrow Ala(Ser) sequence motif, where P2 distinguishes the specificity of staphopain A (Leu) from that of both staphopains B and C (Phe/Tyr). However, we show that at the same time the overall specificity of staphopains is relaxed, insofar as multiple substrates that diverge from the sequences described above are also efficiently hydrolyzed. (C) 2011 Elsevier Masson SAS. All rights reserved.
Stichworte
Substrates library; Staphylococcal virulence; Protease; Staphopain; Substrate specificity
Erscheinungsjahr
2012
Zeitschriftentitel
Biochimie
Band
94
Ausgabe
2
Seite(n)
318-327
ISSN
0300-9084
Page URI
https://pub.uni-bielefeld.de/record/2489346

Zitieren

Kalinska M, Kantyka T, Greenbaum DC, et al. Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C. Biochimie. 2012;94(2):318-327.
Kalinska, M., Kantyka, T., Greenbaum, D. C., Larsen, K. S., Wladyka, B., Jabaiah, A., Bogyo, M., et al. (2012). Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C. Biochimie, 94(2), 318-327. doi:10.1016/j.biochi.2011.07.020
Kalinska, Magdalena, Kantyka, Tomasz, Greenbaum, Doron C., Larsen, Katrine S., Wladyka, Benedykt, Jabaiah, Abeer, Bogyo, Matthew, et al. 2012. “Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C”. Biochimie 94 (2): 318-327.
Kalinska, M., Kantyka, T., Greenbaum, D. C., Larsen, K. S., Wladyka, B., Jabaiah, A., Bogyo, M., Daugherty, P. S., Wysocka, M., Jaros, M., et al. (2012). Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C. Biochimie 94, 318-327.
Kalinska, M., et al., 2012. Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C. Biochimie, 94(2), p 318-327.
M. Kalinska, et al., “Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C”, Biochimie, vol. 94, 2012, pp. 318-327.
Kalinska, M., Kantyka, T., Greenbaum, D.C., Larsen, K.S., Wladyka, B., Jabaiah, A., Bogyo, M., Daugherty, P.S., Wysocka, M., Jaros, M., Lesner, A., Rolka, K., Schaschke, N., Stennicke, H., Dubin, A., Potempa, J., Dubin, G.: Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C. Biochimie. 94, 318-327 (2012).
Kalinska, Magdalena, Kantyka, Tomasz, Greenbaum, Doron C., Larsen, Katrine S., Wladyka, Benedykt, Jabaiah, Abeer, Bogyo, Matthew, Daugherty, Patrick S., Wysocka, Magdalena, Jaros, Marcelina, Lesner, Adam, Rolka, Krzysztof, Schaschke, Norbert, Stennicke, Henning, Dubin, Adam, Potempa, Jan, and Dubin, Grzegorz. “Substrate specificity of Staphylococcus aureus cysteine proteases - Staphopains A, B and C”. Biochimie 94.2 (2012): 318-327.

4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Prevalence of Antibiotic and Heavy Metal Resistance Determinants and Virulence-Related Genetic Elements in Plasmids of Staphylococcus aureus.
Bukowski M, Piwowarczyk R, Madry A, Zagorski-Przybylo R, Hydzik M, Wladyka B., Front Microbiol 10(), 2019
PMID: 31068910
Isolation, biochemical characterization, and cloning of a bacteriocin from the poultry-associated Staphylococcus aureus strain CH-91.
Wladyka B, Wielebska K, Wloka M, Bochenska O, Dubin G, Dubin A, Mak P., Appl Microbiol Biotechnol 97(16), 2013
PMID: 23196985
Biochemical and structural characterization of SplD protease from Staphylococcus aureus.
Zdzalik M, Kalinska M, Wysocka M, Stec-Niemczyk J, Cichon P, Stach N, Gruba N, Stennicke HR, Jabaiah A, Markiewicz M, Kedracka-Krok S, Wladyka B, Daugherty PS, Lesner A, Rolka K, Dubin A, Potempa J, Dubin G., PLoS One 8(10), 2013
PMID: 24130791
Staphylococcus aureus Staphopain A inhibits CXCR2-dependent neutrophil activation and chemotaxis.
Laarman AJ, Mijnheer G, Mootz JM, van Rooijen WJ, Ruyken M, Malone CL, Heezius EC, Ward R, Milligan G, van Strijp JA, de Haas CJ, Horswill AR, van Kessel KP, Rooijakkers SH., EMBO J 31(17), 2012
PMID: 22850671

44 References

Daten bereitgestellt von Europe PubMed Central.

Staphylococcus aureus infections
Lowy, N. Engl. J. Med. 339(), 1998
Pathogenesis of methicillin-resistant Staphylococcus aureus infection.
Gordon RJ, Lowy FD., Clin. Infect. Dis. 46 Suppl 5(), 2008
PMID: 18462090
Laboratory-based surveillance of current antimicrobial resistance patterns and trends among Staphylococcus aureus: 2005 status in the United States.
Styers D, Sheehan DJ, Hogan P, Sahm DF., Ann. Clin. Microbiol. Antimicrob. 5(), 2006
PMID: 16469106
Diminished virulence of a sar-/agr- mutant of Staphylococcus aureus in the rabbit model of endocarditis
Cheung, J. Clin. Invest. 94(), 1994
Variation in extracellular protease production among clinical isolates of Staphylococcus aureus due to different levels of expression of the protease repressor sarA.
Karlsson A, Arvidson S., Infect. Immun. 70(8), 2002
PMID: 12117932
Staphylococcus aureus-derived staphopain B, a potent cysteine protease activator of plasma chemerin
Kulig, J. Immunol. 178(), 2007
Staphylococcal cysteine protease staphopain B (SspB) induces rapid engulfment of human neutrophils and monocytes by macrophages.
Smagur J, Guzik K, Bzowska M, Kuzak M, Zarebski M, Kantyka T, Walski M, Gajkowska B, Potempa J., Biol. Chem. 390(4), 2009
PMID: 19284294
The role and regulation of the extracellular proteases of Staphylococcus aureus.
Shaw L, Golonka E, Potempa J, Foster SJ., Microbiology (Reading, Engl.) 150(Pt 1), 2004
PMID: 14702415
Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments.
Coulter SN, Schwan WR, Ng EY, Langhorne MH, Ritchie HD, Westbrock-Wadman S, Hufnagle WO, Folger KR, Bayer AS, Stover CK., Mol. Microbiol. 30(2), 1998
PMID: 9791183
Description of staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease.
Rice K, Peralta R, Bast D, de Azavedo J, McGavin MJ., Infect. Immun. 69(1), 2001
PMID: 11119502
Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection.
Burlak C, Hammer CH, Robinson MA, Whitney AR, McGavin MJ, Kreiswirth BN, Deleo FR., Cell. Microbiol. 9(5), 2007
PMID: 17217429
Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.
Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, Simpson AJ, Rambaut A, Nubel U, Fitzgerald JR., Proc. Natl. Acad. Sci. U.S.A. 106(46), 2009
PMID: 19884497
Structural gene and strain specificity of a novel cysteine protease produced by Staphylococcus aureus isolated from a diseased chicken.
Takeuchi S, Matsunaga K, Inubushi S, Higuchi H, Imaizumi K, Kaidoh T., Vet. Microbiol. 89(2-3), 2002
PMID: 12243897
The staphostatin family of cysteine protease inhibitors in the genus Staphylococcus as an example of parallel evolution of protease and inhibitor specificity.
Dubin G, Wladyka B, Stec-Niemczyk J, Chmiel D, Zdzalik M, Dubin A, Potempa J., Biol. Chem. 388(2), 2007
PMID: 17261086
Genetic characterization of staphopain genes in Staphylococcus aureus.
Golonka E, Filipek R, Sabat A, Sinczak A, Potempa J., Biol. Chem. 385(11), 2004
PMID: 15576326
Purification and characterization of protease produced by Staphylococcus aureus isolated from a diseased chicken.
Takeuchi S, Kinoshita T, Kaidoh T, Hashizume N., Vet. Microbiol. 67(3), 1999
PMID: 10418873
Staphostatins: an expanding new group of proteinase inhibitors with a unique specificity for the regulation of staphopains, Staphylococcus spp. cysteine proteinases.
Rzychon M, Sabat A, Kosowska K, Potempa J, Dubin A., Mol. Microbiol. 49(4), 2003
PMID: 12890028
Simplified screening for the detection of soluble fusion constructs expressed in E. coli using a modular set of vectors.
Dummler A, Lawrence AM, de Marco A., Microb. Cell Fact. 4(), 2005
PMID: 16351710
A role for the protease falcipain 1 in host cell invasion by the human malaria parasite.
Greenbaum DC, Baruch A, Grainger M, Bozdech Z, Medzihradszky KF, Engel J, DeRisi J, Holder AA, Bogyo M., Science 298(5600), 2002
PMID: 12471262
Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools.
Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M., Chem. Biol. 7(8), 2000
PMID: 11048948
Cluster analysis and display of genome-wide expression patterns.
Eisen MB, Spellman PT, Brown PO, Botstein D., Proc. Natl. Acad. Sci. U.S.A. 95(25), 1998
PMID: 9843981
Chemical approaches for functionally probing the proteome.
Greenbaum D, Baruch A, Hayrapetian L, Darula Z, Burlingame A, Medzihradszky KF, Bogyo M., Mol. Cell Proteomics 1(1), 2002
PMID: 12096141
Primed-site probing of papain-like cysteine proteases
Pfizer, Int. J. Peptide Res. Therapeut. 13(), 2007
Generation and use of synthetic peptide combinatorial libraries for basic research and drug discovery.
Houghten RA, Pinilla C, Blondelle SE, Appel JR, Dooley CT, Cuervo JH., Nature 354(6348), 1991
PMID: 1719428
Selection of new chromogenic substrates of serine proteinases using combinatorial chemistry methods.
Wysocka M, Kwiatkowska B, Rzadkiewicz M, Lesner A, Rolka K., Comb. Chem. High Throughput Screen. 10(3), 2007
PMID: 17346116
Design, chemical synthesis and kinetic studies of trypsin chromogenic substrates based on the proteinase binding loop of Cucurbita maxima trypsin inhibitor (CMTI-III).
Lesner A, Brzozowski K, Kupryszewski G, Rolka K., Biochem. Biophys. Res. Commun. 269(1), 2000
PMID: 10694481
Chromogenic substrates of bovine beta-trypsin: the influence of an amino acid residue in P1 position on their interaction with the enzyme.
Lesner A, Kupryszewski G, Rolka K., Biochem. Biophys. Res. Commun. 285(5), 2001
PMID: 11478806
Engineering the substrate and inhibitor specificities of human coagulation Factor VIIa.
Larsen KS, Ostergaard H, Bjelke JR, Olsen OH, Rasmussen HB, Christensen L, Kragelund BB, Stennicke HR., Biochem. J. 405(3), 2007
PMID: 17456045
Protease specificity determination by using cellular libraries of peptide substrates (CLiPS).
Boulware KT, Daugherty PS., Proc. Natl. Acad. Sci. U.S.A. 103(20), 2006
PMID: 16672368
Directed evolution of a biterminal bacterial display scaffold enhances the display of diverse peptides.
Rice JJ, Daugherty PS., Protein Eng. Des. Sel. 21(7), 2008
PMID: 18480093
On the size of the active site in proteases. I. Papain.
Schechter I, Berger A., Biochem. Biophys. Res. Commun. 27(2), 1967
PMID: 6035483
MEROPS: the peptidase database.
Rawlings ND, Barrett AJ, Bateman A., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19892822
The lysosomal cysteine proteases.
McGrath ME., Annu Rev Biophys Biomol Struct 28(), 1999
PMID: 10410800
The inactivation of human plasma alpha 1-proteinase inhibitor by proteinases from Staphylococcus aureus
Potempa, J. Biol. Chem. 261(), 1986
Occurrence of an extracellular serineproteinase among Staphylococcus aureus strains.
Bjorklind A, Arvidson S., Acta Pathol Microbiol Scand B 85(4), 1977
PMID: 899795
The staphostatin–staphopain complex: a forward binding inhibitor in complex with its target cysteine protease
Filipek, J. Biol. Chem. 278(), 2003
Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries.
Harris JL, Backes BJ, Leonetti F, Mahrus S, Ellman JA, Craik CS., Proc. Natl. Acad. Sci. U.S.A. 97(14), 2000
PMID: 10869434
Specificity profiling of seven human tissue kallikreins reveals individual subsite preferences
Debela, J. Biol. Chem. 281(), 2006
Design of selective substrates of proteinase 3 using combinatorial chemistry methods.
Wysocka M, Lesner A, Guzow K, Mackiewicz L, Legowska A, Wiczk W, Rolka K., Anal. Biochem. 378(2), 2008
PMID: 18445466
Highly sensitive intramolecularly quenched fluorogenic substrates for renin based on the combination of L-2-amino-3-(7-methoxy-4-coumaryl)propionic acid with 2,4-dinitrophenyl groups at various positions.
Paschalidou K, Neumann U, Gerhartz B, Tzougraki C., Biochem. J. 382(Pt 3), 2004
PMID: 15233625
Crystal structure of a thiol proteinase from Staphylococcus aureus V8 in the E-64 inhibitor complex
Hoffman, Acta Crystallograp. (), 1993
Prostaphopain B structure: a comparison of proregion-mediated and staphostatin-mediated protease inhibition.
Filipek R, Szczepanowski R, Sabat A, Potempa J, Bochtler M., Biochemistry 43(44), 2004
PMID: 15518582
Identification of a novel maturation mechanism and restricted substrate specificity for the SspB cysteine protease of Staphylococcus aureus
Massimi, J. Biol. Chem. 277(), 2002
Activation mechanism of thiol protease precursor from broiler chicken specific Staphylococcus aureus strain CH-91.
Wladyka B, Dubin G, Dubin A., Vet. Microbiol. 147(1-2), 2010
PMID: 20598816
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 21802486
PubMed | Europe PMC

Suchen in

Google Scholar