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Bacterial Proteases as Targets to Control Bacterial Growth

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New Weapons to Control Bacterial Growth

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Abstract

Proteases (PRs) catalyze the cleavage of peptide bonds by hydrolysis in proteins and peptides playing crucial functions in organisms all over the phylogenetic tree. These enzymes are present in all types of bacteria and are involved in critical processes such as acquisition of nutrients for growth and proliferation, facilitation of dissemination, colonization and evasion of host immune defenses or tissue damage during infection. Bacterial pathogens use their PRs to acquire or activate the function of host PRs to help them in their growth or progression of disease. Research into bacterial PRs and their substrates will allow the development of novel PRs inhibiting compounds that could potentially be used to limit host virulence or to block cell growth. The emergence resistances to traditional antibiotics have created clinical difficulties for nosocomial treatment on a global scale. Thus the pharmacological development of new PRs inhibitors that target essential proteins in the bacterial pathogen is of great interest, and it is the focus of this review.

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References

  • Addinall SG, Holland B (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318:219–236

    Article  CAS  PubMed  Google Scholar 

  • Antonelli AC, Zhang Y, Golub LM, Johnson F, Simon SR (2014) Inhibition of anthrax lethal factor by curcumin and chemically modified curcumin derivatives. J Enzyme Inhib Med Chem 29:663–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baba A, Kadowaki T, Asao T, Yamamoto K (2002) Roles for Arg and Lys-gingipains in the disruption of cytokine responses and loss of viability of human endothelial cells by Porphyromonas gingivalis infection. Biol Chem 383:1223–1230

    Article  CAS  PubMed  Google Scholar 

  • Bannwarth L, Goldberg AB, Chen C, Turk BE (2012) Identification of exosite–targeting inhibitors of anthrax lethal factor by high-throughput screening. Chem Biol 19:875–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker S, Frankel MB, Schneewind O, Missiakas D (2014) Release of protein A from the cell wall of Staphylococcus aureus. Proc Natl Acad Sci USA 111:1574–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bond C (2015) Antibiotic resistance: turning back the tide. Int J Pharm Pract 23:307–308

    Article  PubMed  Google Scholar 

  • Bourhis LL, Werts C (2007) Role of nods in bacterial infection. Microbes Infect 9:629–636

    Article  PubMed  CAS  Google Scholar 

  • Boyle-Vavra S, Yin S, Challapalli M, Daum RS (2003) Transcriptional induction of the penicillin–binding protein 2 gene in Staphylococcus aureus by cell wall-active antibiotics oxacillin and vancomycin. Antimicrob Agents Chemother 47:1028–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brakhage AA, Al-Abdallah Q, Tüncher A, Spröte P (2005) Evolution of beta–lactam biosynthesis genes and recruitment of trans-acting factors. Phytochemistry 66:1200–1210

    Google Scholar 

  • Brotzu G (1948) Ricerche su di un nuovo antibiotico, Lavoratorio dell ́Istituto di Igiene di Cagliari 1–11

    Google Scholar 

  • Camelo-Castillo A, Benítez-Páez A, Belda-Ferre P, Cabrera-Rubio R, Mira A (2014) Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 64:60–65

    Article  CAS  PubMed  Google Scholar 

  • Carlisle MD, Srikantha RN, Brogden KA (2009) Degradation of human alpha- and beta-defensins by culture supernatants of Porphyromonas gingivalis strain 381. J Innate Immun 1:118–122

    Article  CAS  PubMed  Google Scholar 

  • Cathcart GR, Quinn D, Greer B, Harriott P, Lynas JF, Gilmore BF, Walker B (2011) Novel inhibitors of the Pseudomonas aeruginosa virulence factor LasB: a potential therapeutic approach for the attenuation of virulence mechanisms in pseudomonal infection. Antimicrob Agents Chemother 55:2670–2678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan LC, Basuino L, Diep B, Hamilton S, Chatterjee SS, Chambers HF (2015) Ceftobiprole– and ceftaroline–resistant methicillin–resistant Staphylococcus aureus. Antimicrob Agents Chemother 59:2960–2963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Chin W, Dong H, Xu L, Zhong G, Huang Y, Li L, Xu K, Wu M, Hedrick JL, Yang YY, Fan W (2015) Biodegradable Antimicrobial polycarbonates with in vivo efficacy against multidrug-resistant MRSA systemic infection. Adv Healthc Mater 4:2128–2136

    Article  CAS  Google Scholar 

  • Cloud-Hansen KA, Hackett KT, Garcia DL, Dillard JP (2008) Neisseria gonorrhoeae uses two lytic transglycosylases to produce cytotoxic peptidoglycan monomers. J Bacteriol 190:5989–5994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clutterbuck PW, Lovell R, Raistrick H (1932) Studies in the biochemistry of the microorganisms. XXVI. The formation from glucose by members of the Penicillium chrysogenum species of a pigment, an alkali soluble protein and penicillin. The antibacterial substance of Fleming. Biochem J 26:1907–1918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coulthurst SJ, Barnard AML, Salmond GPC (2005) Regulation and biosyn–thesis of carbapenem antibiotics in bacteria. Nat Rev Microbiol 3:295–306

    Article  CAS  PubMed  Google Scholar 

  • Cowell BA, Twining SS, Hobden JA, Kwong MS, Fleiszig SM (2003) Mutation of lasA and lasB reduces Pseudomonas aeruginosa invasion of epithelial cells. Microbiology 149:2291–2299

    Article  CAS  PubMed  Google Scholar 

  • Dell’Aica I, Donà M, Tonello F, Piris A, Mock M, Montecucco C, Garbisa S (2004) Potent inhibitors of anthrax lethal factor from green tea. EMBO Rep 5:418–422

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Denome SA, Elf PK, Henderson TA, Nelson DE, Young KD (1999) Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J Bacteriol 181:3981–3993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Drag M, Salvesen GS (2010) Emerging principles in protease-based drug discovery. Nat Rev Drug Discov 9:690–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott SD (1945) A proteolytic enzyme produced by group A streptococci with special reference to its effect on the type–specific M antigen. J Exp Med 81:573–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson BI, Smith H, Yasothan U, Kirkpatrick P (2008) Dabigatran etexilate. Nat Rev Drug Discov 7:557–558

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Aguado M, Teijeira F, Martín JF, Ullán RV (2013) A vacuolar membrane protein affects drastically the biosynthesis of the ACV tripeptide and the beta–lactam pathway of Penicillium chrysogenum. Appl Microbiol Biotechnol 97:795–808

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Aguado M, Martín JF, Rodríguez-Castro R, García-Estrada C, Albillos SM, Teijeira F, Ullán RV (2014) New insights into the isopenicillin N transport in Penicillium chrysogenum. Metab Eng 22:89–103

    Article  PubMed  CAS  Google Scholar 

  • Fersht A (1985) Enzyme structure and mechanism, 2nd edn. W. H. Freeman and Company, New York

    Google Scholar 

  • Fitzpatrick RE, Wijeyewickrema LC, Pike RN (2009) The gingipains: scissors and glue of the periodontal pathogen, Porphyromonas gingivalis. Future Microbiol 4:471–487

    Article  CAS  PubMed  Google Scholar 

  • Fleming A (1929) On the antibacterial action of cultures of a penicillium with special reference to their use in the isolation of B. influenza. Br J Exp Pathol 10:226–236

    CAS  PubMed Central  Google Scholar 

  • Forino M, Johnson S, Wong TY, Rozanov DV, Savinov AY, Li W, Fattorusso R, Becattini B, Orry AJ, Jung D, Abagyan RA, Smith JW, Alibek K, Liddington RC, Strongin AY, Pellecchia M (2005) Efficient synthetic inhibitors of anthrax lethal factor. Proc Natl Acad Sci USA 102:9499–9504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournier B, Philpott DJ (2005) Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev 18:521–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frankel MB, Schneewind O (2012) Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J Biol Chem 287:10460–10471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frère JM, Page MG (2014) Penicillin–binding proteins: evergreen drug targets. Curr Opin Pharmacol 18:112–119

    Article  PubMed  CAS  Google Scholar 

  • Frick IM, Björck L, Herwald H (2007) The dual role of the contact system in bacterial infectious disease. Thromb Haemost 98:497–502

    CAS  PubMed  Google Scholar 

  • Fuda C, Suvorov M, Vakulen SB, Mobashery S (2004) The basis for resistance to beta-lactam antibiotics by penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus. J Biol Chem 279:40802–40806

    Google Scholar 

  • Fuda CC, Fisher JF, Mobashery S (2005) Beta-Lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome. Cell Mol Life Sci 62:2617–2633

    Google Scholar 

  • Gi M, Jeong J, Lee K, Lee KM, Toyofuku M, Yong DE, Yoon SS, Choi JY (2014) A drug-repositioning screening identifies pentetic acid as a potential therapeutic agent for suppressing the elastase-mediated virulence of Pseudomonas aeruginosa. Antimicrob Agents Chemother 58:7205–7214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gohlke H, Klebe G (2002) Approaches to the description and prediction of the binding affinity of small-molecule ligands to macromolecular receptors. Angew Chem Int Ed 41:2645–2676

    Article  Google Scholar 

  • Guilhelmelli F, Vilela N, Albuquerque P, Derengowski Lda S, Silva-Pereira I, Kyaw CM (2013) Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Front Microbiol 4:353

    PubMed  PubMed Central  Google Scholar 

  • Guo Y, Nguyen K-A, Potempa J (2010) Dichotomy of gingipains action as virulence factors: from cleaning substrates with the precision of a surgeon’s knife to a meat chopper–like brutal degradation of proteins. Periodontol 2000 54:15–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamilton-Miller JMT (2000) Sir Edward Abraham’s contribution to the development of the cephalosporins: a reassessment. Int J Antimicrob Agents 15:179–184

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto M, Ooiwa S, Sekiguchi J (2012) Synthetic lethality of the lytE cwlO genotype in Bacillus subtilis is caused by lack of D, L-endopeptidase activity at the lateral cell wall. J Bacteriol 194:796–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henzler-Wildman KA, Martinez GV, Brown MF, Ramamoorthy A (2004) Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43:8459–8469

    Article  CAS  PubMed  Google Scholar 

  • Hoge R, Pelzer A, Rosenau F, Wilhelm S (2010) Weapons of a pathogen: proteases and their role in virulence of Pseudomonas aeruginosa. In: Mendez–Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology, vol 2, pp 383–395. Microbiology book series, Formatex Research Center

    Google Scholar 

  • Humann J, Lenz LL (2009) Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J Innate Immun 1:88–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imamura T, Potempa J, Tanase S, Travis J (1997) Activation of blood coagulation factor X by arginine–specific cysteine proteinases (gingipain–Rs) from Porphyromonas gingivalis. J Biol Chem 272:16062–16067

    Article  CAS  PubMed  Google Scholar 

  • Imamura T, Tanase S, Hamamoto T, Potempa J, Travis J (2001) Activation of blood coagulation factor IX by gingipains R, arginine–specific cysteine proteinases from Porphyromonas gingivalis. Biochem J 353:325–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imamura T, Tanase S, Szmyd G, Kozik A, Travis J, Potempa J (2005) Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus. J Exp Med 201:1669–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin–resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen WT, Beitsma MM, Koeman CJ, van Wamel WJ, Verhoef J, Fluit AC (2006) Novel mobile variants of staphylococcal cassette chromosome mec in Staphylococcus aureus. Antimicrob Agents Chemother 50:2072–2208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenssen H, Hamill P, Hancock RE (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19:491–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansson BP, Shannon O, Björck L (2008) Ides: a bacterial proteolytic enzyme with therapeutic potential. PLoS ONE 3:e1692

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jovetic S, Zhu Y, Marcone GL, Marinelli F, Tramper J (2010) β–Lactam and glycopeptide antibiotics: first and last line of defense? Trends Biotechnol 28:596–604

    Article  CAS  PubMed  Google Scholar 

  • Kantyka T, Potempa J (2011) Human SCCA serpins inhibit staphylococcal cysteine proteases by forming classic “serpin–like” covalent complexes. Methods Enzymol 499:331–345

    Article  CAS  PubMed  Google Scholar 

  • Kantyka T, Plaza K, Koziel J, Florczyk D, Stennicke HR, Thogersen IB, Enghild JJ, Silverman GA, Pak SC, Potempa J (2011) Inhibition of Staphylococcus aureus cysteine proteases by human serpin potentially limits staphylococcal virulence. Biol Chem 392:483–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapur V, Topouzis S, Majesky MW, Li LL, Hamrick MR, Hamill RJ, Patti JM, Musser JM (1993) A conserved streptococcus-pyogenes extracellular cysteine protease cleaves human fibronectin and degrades vitronectin. Microb Pathog 15:327–346

    Article  CAS  PubMed  Google Scholar 

  • Katayama Y, Ito T, Hiramatsu K (2000) A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley WL, Jousselin A, Barras C, Lelong E, Renzoni A (2015) Missense mutations in PBP2A Affecting ceftaroline susceptibility detected in epidemic hospital–acquired methicillin-resistant Staphylococcus aureus clonotypes ST228 and ST247 in Western Switzerland archived since 1998. Antimicrob Agents Chemother 59:1922–1930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler E, Safrin M, AbramsWR Rosenbloom J, Ohman DE (1997) Inhibitors and specificity of Pseudomonas aeruginosa LasA. J Biol Chem 272:9884–9889

    Article  CAS  PubMed  Google Scholar 

  • Kindrachuk J, Nijnik A, Hancock REW (2010) Host defense peptides: bridging antimicrobial and immunomodulatory activities. In: Mander L, Lui H-W (eds) Comprehensive natural products II chemistry and biology. Elsevier, Oxford, pp 175–216

    Google Scholar 

  • Kirk O, Borchert TV, Fuglsang CC (2002) Industrial enzyme applications. Curr Opin Biotechnol 13:345–351

    Article  CAS  PubMed  Google Scholar 

  • Komori Y, Nonogaki T, Nikai T (2001) Hemorrhagic activity and muscle damaging effect of Pseudomonas aeruginosa metalloproteinase (elastase). Toxicon 39:1327–1332

    Article  CAS  PubMed  Google Scholar 

  • Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Cordani JJ, Connerton IF, Cummings NJ, Daniel RA, Denziot F, Devine KM, Düsterhöft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Hènaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee SM, Levine A, Liu H, Masuda S, Mauël C, Médigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O’Reilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, Parro V, Pohl TM, Portelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin BS, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Togoni A, Tosato V, Uchiyama S, Vandebol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa HF, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–256

    Article  CAS  PubMed  Google Scholar 

  • Lantz MS (1997) Are bacterial proteases important virulence factors? J Periodontal Res 32:126–132

    Article  CAS  PubMed  Google Scholar 

  • Leidal KG, Munson KL, Johnson MC, Denning GM (2003) Metalloproteases from Pseudomonas aeruginosa degrade human RANTES, MCP–1, and ENA–78. J Interferon Cytokine Res 23:307–318

    Article  CAS  PubMed  Google Scholar 

  • Li F, Chvyrkova I, Terzyan S, Wakeham N, Turner R, Ghosh AK, Zhang XC, Tang J (2012) Inhibition of anthrax lethal factor: lability of hydroxamate as a chelating group. Appl Microbiol Biotechnol 94:1041–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liras P (1999) Biosynthesis and molecular genetics of cephamycins. Antonie Van Leeuwenhoek 75:109–124

    Article  CAS  PubMed  Google Scholar 

  • Livermore DM (2006) Can beta-lactams be re–engineered to beat MRSA? Clin Microbiol Infect 12(Suppl 2):11–16

    Article  CAS  PubMed  Google Scholar 

  • Maeda H (1996) Role of microbial proteases in pathogenesis. Microbiol Immunol 40:685–699

    Article  CAS  PubMed  Google Scholar 

  • Margolin W (2009) Sculpting the bacterial cell. Curr Biol 19:R812–R822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massimi I, Park E, Rice K, Muller-Esterl W, Sauder D, McGavin MJ (2002) Identification of a novel maturation mechanism and restricted substrate specificity for the SspB cysteine protease of Staphylococcus aureus. J Biol Chem 277:41770–41777

    Google Scholar 

  • Matheson NR, Potempa J, Travis J (2006) Interaction of a novel form of Pseudomonas aeruginosa alkaline protease (aeruginolysin) with interleukin-6 and interleukin-8. Biol Chem 387:911–915

    Article  CAS  PubMed  Google Scholar 

  • Mikolajczyk-Pawlinska J, Travis J, Potempa J (1998) Modulation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: implications for pathogenicity of periodontal disease. FEBS Lett 440:282–286

    Article  CAS  PubMed  Google Scholar 

  • Miyoshi SI, Shinoda S (1997) Bacterial metalloproteases as the toxic factor in infection. J Toxicol Toxin Rev 16:177–194

    Article  CAS  Google Scholar 

  • Moayeri M, Crown D, Jiao GS, Kim S, Johnson A, Leysath C, Leppla SH (2013) Small–molecule inhibitors of lethal factor protease activity protect against anthrax infection. Antimicrob Agents Chemother 57:4139–4145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morihara K (1964) Production of elastase and proteinase by Pseudomonas aeruginosa. J Bacteriol 88:745–757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nandakumar KS, Johansson BP, Björck L, Holmdahl R (2007) Blocking of experimental arthritis by cleavage of igg antibodies in vivo. Arthritis Rheum 56:3253–3260

    Article  CAS  PubMed  Google Scholar 

  • Newman ZL, Sirianni N, Mawhinney C, Lee MS, Leppla SH, Moayeri M, Johansen LM (2011) Auranofin protects against anthrax lethal toxin–induced activation of the Nlrp1b inflammasome. Antimicrob Agents Chemother 55:1028–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ngai PHK, Ng TB (2004) A napin-like polypeptide from dwarf Chinese white cabbage seeds with translation-inhibitory, trypsininhibitory, and antibacterial activities. Peptides 25:171–176

    Article  CAS  PubMed  Google Scholar 

  • Oda Kohei (2012) New families of carboxyl peptidases: serine-carboxyl peptidases and glutamic peptidases. J Biochem 151:13–25

    Article  CAS  PubMed  Google Scholar 

  • Olsen I, Potempa J (2014) Strategies for the inhibition of gingipains for the potential treatment of periodontitis and associated systemic diseases. J Oral Microbiol 18:6

    Google Scholar 

  • Otto HH, Schirmeister T (1997) Cysteine proteases and their inhibitors. Chem Rev 97:133–171

    Article  CAS  PubMed  Google Scholar 

  • Pascual A, Tan JP, Yuen A, Chan JM, Coady DJ, Mecerreyes D, Hedrick JL, Yang YY, Sardon H (2015) Broad-spectrum antimicrobial polycarbonate hydrogels with fast degradability. Biomacromolecules 16:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Plaut AG (1983) The IgA1 proteases of pathogenic bacteria. Annu Rev Microbiol 37:603–622

    Article  CAS  PubMed  Google Scholar 

  • Pohlmann J, Vasilevich NI, Glushkov AI, Kellenberger L, Shapiro S, Caspers P, Page MG, Danel F (2010) Propenylamide and propenylsulfonamide cephalosporins as a novel class of anti–MRSA beta–lactams. Bioorg Med Chem Lett 20:4635–4638

    Article  CAS  PubMed  Google Scholar 

  • Poole K (2004) Resistance to beta-lactam antibiotics. Cell Mol Life Sci 61:2200–2223

    Article  CAS  PubMed  Google Scholar 

  • Popadiak K, Potempa J, Riesbeck K, Blom AM (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 178:7242–7250

    Article  CAS  PubMed  Google Scholar 

  • Potempa J, Pike RN (2009) Corruption of innate immunity by bacterial proteases. J Innate Immun 1:70–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potempa J, Banbula A, Travis J (2000) Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontology 24:153–192

    Article  CAS  Google Scholar 

  • Poulsen K, Reinholdt J, Jespersgaard C, Boye K, Brown TA, Hauhe MA (1998) comprehensive genetic study of streptococcal immunoglobulin A1 proteases: evidence for recombination within and between species. Infect Immun 66:181–190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rachel KV, Vimala Y, Apta Chaitanya D (2013) A trypsin inhibitor–SNTI with antidandruff activity from Sapindus trifoliatus. Indian J Appl Res 3:3–5

    Article  Google Scholar 

  • Rakashanda S, Ishaq M, Masood A, Amin S (2012) Antibacterial activity of a Trypsin–chymotrypsin–elastase inhibitor isolated from Lavatera cashmeriana camb. seeds. J Anim Plant Sci 22:983–986

    Google Scholar 

  • Rani K, Rana R, Datt S (2012) Review on latest overview of proteases. Int J Curr Life Sci 2:12–18

    Google Scholar 

  • Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597–635

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9:117–128

    Article  CAS  PubMed  Google Scholar 

  • Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Res 38 (Database issue):D227–33

    Google Scholar 

  • Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40:D343–D350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray A (2012) Protease enzyme-potential industrial scope. Int J Technol 2:1–4

    Google Scholar 

  • Rice SA, Givskov M, Steinberg P, Kjelleberg S (1999) Bacterial signals and antagonists: the interaction between bacteria and higher organisms. J Mol Microbiol Biotechnol 1:23–31

    CAS  PubMed  Google Scholar 

  • Rogers HJ, Taylor C, Rayter S, Ward JB (1984) Purification and properties of an autolytic endo-β-N-glucosaminidase and the N–acetylmuramyl-L-alanine amidase from Bacillus subtilis strain 168. J Gen Microbiol 130:2395–2402

    CAS  PubMed  Google Scholar 

  • Rolain JM, Canton R, Cornaglia G (2012) Emergence of antibiotic resistance: need for a new paradigm. Clin Microbiol Infect 18:615–616

    Article  CAS  PubMed  Google Scholar 

  • Rzychon M, Sabat A, Kosowska K, Potempa J, Dubin A (2003) Staphostatins: an expanding new group of proteinase inhibitors with a unique specificity for the regulation of staphopains, Staphylococcus spp. cysteine proteinases. Mol Microbiol 49:1051–1066

    Article  CAS  PubMed  Google Scholar 

  • Sakata Y, Akaike T, Suga M, Ijiri S, Ando M, Maeda H (1996) Bradykinin generation triggered by Pseudomonas proteases facilitates invasion of the systemic circulation by Pseudomonas aeruginosa. Microbiol Immunol 40:415–423

    Article  CAS  PubMed  Google Scholar 

  • Santos-Beneit F, Martín JF, Barreiro C (2014) Glycopeptides and Bacterial Cell Walls. In: Villa TG, Veiga-Crespo P (eds) Antimicrobial compounds. Springer, Berlin, pp 285–311

    Chapter  Google Scholar 

  • Satheesh LP, Murugan K (2011) Antimicrobial activity of protease inhibitors from leaves of Coccinia grandis (L.) Voigt. Indian J Exp Biol 49:366–374

    CAS  PubMed  Google Scholar 

  • Schaumburg F, Peters G, Alabi A, Becker K, Idelevich EA (2015) Missense mutations of PBP2a are associated with reduced susceptibility to ceftaroline and ceftobiprole in African MRSA. J Antimicrob Chemother. doi:10.1093/jac/dkv325 (first published online October 5)

  • Scheurwater EM, Pfeffer JM, Clarke AJ (2007) Production and purification of the bacterial autolysin N-acetylmuramoyl-L-alanine amidase B from Pseudomonas aeruginosa. Protein Expr Purif 56:128–137

    Article  CAS  PubMed  Google Scholar 

  • Scheurwater E, Reid CW, Clarke AJ (2008) Lytic transglycosylases: bacterial space–making autolysins. Int J Biochem Cell Biol 40:586–591

    Article  CAS  PubMed  Google Scholar 

  • Schmidtchen A, Frick IM, Andersson E, Tapper H, Björck L (2002) Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL–37. Mol Microbiol 46:157–168

    Article  CAS  PubMed  Google Scholar 

  • Sheets SM, Robles-Price AG, McKenzie RM, Casiano CA, Fletcher HM (2008) Gingipain–dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci 13:3215–3238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shilabin AG, Dzhekieva L, Misra P, Jayaram B, Pratt RF (2012) 4–quinolones as noncovalent inhibitors of high molecular mass penicillin-binding proteins. ACS Med Chem Lett 3:592–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoop WL, Xiong Y, Wiltsie J, Woods A, Guo J, Pivnichny JV, Felcetto T, Michael BF, Bansal A, Cummings RT, Cunningham BR, Friedlander AM, Douglas CM, Patel SB, Wisniewski D, Scapin G, Salowe SP, Zaller DM, Chapman KT, Scolnick EM, Schmatz DM, Bartizal K, MacCoss M, Hermes JD (2005) Anthrax lethal factor inhibition. Proc Natl Acad Sci USA 102:7958–7963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sieprawska-Lupa M, Mydel P, Krawczyk K, Wójcik K, Puklo M, Lupa B, Suder P, Silberring J, Reed M, Pohl J, Shafer W, McAleese F, Foster T, Travis J, Potempa J (2004) Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48:4673–4679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith A (2007) Bacterial resistance to antibiotics. In: Denyer SP, Hodges NA, Gorman SP (eds) Hugo and Russell’s pharmaceutical microbiology. Blackwell Science Ltd., Oxford

    Google Scholar 

  • Smith TJ, Blackman SA, Foster SJ (1996) Peptidoglycan hydrolases of Bacillus subtilis 168. Microb Drug Resist 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Smith TJ, Blackman SA, Foster SJ (2000) Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249–262

    Article  CAS  PubMed  Google Scholar 

  • Song MD, Wachi M, Doi M, Ishino F, Matsuhashi M (1987) Evolution of an inducible penicillin–target protein in methicillin-resistant Staphylococcus aureus by gene fusion. FEBS Lett 221:167–171

    Article  CAS  PubMed  Google Scholar 

  • Sugai M, Fujiwara T, Komatsuzawa H, Suginaka H (1998) Identification and molecular characterization of a gene homologous to epr (endopeptidase resistance gene) in Staphylococcus aureus. Gene 224:67–75

    Article  CAS  PubMed  Google Scholar 

  • Tan CM, Therien AG, Lu J, Lee SH, Caron A, Gill CJ, Lebeau-Jacob C, Benton-Perdomo L, Monteiro JM, Pereira PM, Elsen NL, Wu J, Deschamps K, Petcu M, Wong S, Daigneault E, Kramer S, Liang L, Maxwell E, Claveau D, Vaillancourt J, Skorey K, Tam J, Wang H, Meredith TC, Sillaots S, Wang-Jarantow L, Ramtohul Y, Langlois E, Landry F, Reid JC, Parthasarathy G, Sharma S, Baryshnikova A, Lumb KJ, Pinho MG, Soisson SM, Roemer T (2012) Restoring methicillin-resistant Staphylococcus aureus susceptibility to β-lactam antibiotics. Sci Transl Med 4:126ra35

    Google Scholar 

  • Tenorio EL, Klein BA, Cheung WS, Hu LT (2011) Identification of interspecies interactions affecting Porphyromonas gingivalis virulence phenotypes. J Oral Microbiol 3:8396

    Article  Google Scholar 

  • Thomas M, Castignetti D (2009) Examination of anthrax lethal factor inhibition by siderophores, small hydroxamates and protamine. J Microbiol Immunol Infect 42:284–289

    CAS  PubMed  Google Scholar 

  • Tomasz A (1979) The mechanism of the irreversible antimicrobial effects of penicillins: how the beta-lactam antibiotics kill and lyse bacteria. Annu Rev Microbiol 33:113–137

    Article  CAS  PubMed  Google Scholar 

  • Toney JH, Hammond GG, Leiting B, Pryor KD, Wu JK, Cuca GC, Pompliano DL (1998) Soluble penicillin–binding protein 2a: beta-lactam binding and inhibition by non-betalactams using a 96-well format. Anal Biochem 255:113–119

    Article  CAS  PubMed  Google Scholar 

  • Travis J, Potempa J (2000) Bacterial proteinases as targets for the development of second generation antibiotics. Biochim Biophys Acta 1477:35–50

    Article  CAS  PubMed  Google Scholar 

  • Turk S, Verlaine O, Gerards T, Zivec M, Humljan J, Sosič I, Amoroso A, Zervosen A, Luxen A, Joris B, Gobec S (2011) New noncovalent inhibitors of penicillin–binding proteins from penicillin-resistant bacteria. PLoS ONE 6(5):e19418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullan RV, Casqueiro J, Banuelos O, Fernandez FJ, Gutierrez S, Martin JF (2002) A novel epimerization system in fungal secondary metabolism involved in the conversion of isopenicillin N into penicillin N in Acremonium chrysogenum. J Biol Chem 277:46216–46225

    Article  CAS  PubMed  Google Scholar 

  • Ullán RV, Campoy S, Casqueiro J, Fernández FJ, Martín JF (2007) Deacetylcephalosporin C production in Penicillium chrysogenum by expression of the isopenicillin N epimerization, ring expansion, and acetylation genes. Chem Biol 14:329–339

    Article  PubMed  CAS  Google Scholar 

  • Ullán RV, Teijeira F, Guerra SM, Vaca I, Martín JF (2010) Characterization of a novel peroxisome membrane protein essential for conversion of isopenicillin N into cephalosporin C. Biochem J 432:227–236

    Article  PubMed  CAS  Google Scholar 

  • van Berkel SS, Nettleship JE, Leung IK, Brem J, Choi H, Stuart DI, Claridge TD, McDonough MA, Owens RJ, Ren J, Schofield CJ (2013) Binding of (5S)-penicilloic acid to penicillin binding protein 3. ACS Chem Biol 8:2112–2116

    Article  PubMed  CAS  Google Scholar 

  • Velayati AA, Masjedi MR, Farnia P, Tabarsi P, Ghanavi J, Ziazarifi AH, Hoffner SE (2009) Emergence of new forms of totally drug-resistant tuberculosis bacilli: super extensively drug–resistant tuberculosis or totally drug-resistant strains in iran. Chest 136:420–435

    Article  PubMed  Google Scholar 

  • Vermehren J, Sarrazin C (2011) New HCV therapies on the horizon. Clin Microbiol Infect 17:122–134

    Article  CAS  PubMed  Google Scholar 

  • von Pawel-Rammingen U, Björck L (2003) IdeS and SpeB: immunoglobulin–degrading cysteine proteinases of Streptococcus pyogenes. Curr Opin Microbiol 6:50–55

    Article  CAS  Google Scholar 

  • von Pawel-Rammingen U, Johansson BP, Tapper H, Björck L (2002) IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J 21:1607–1615

    Article  Google Scholar 

  • Walsh C (2003) Antibiotics: actions, origins, resistance. ASM Press, Washington DC

    Google Scholar 

  • Wise EM Jr, Park JT (1965) Penicillin: its basic site of action as an inhibitor of a peptide cross-linking reaction in cell wall mucopeptide synthesis. Proc Natl Acad Sci USA 54:75–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worthington RJ, Melander C (2013) Overcoming resistance to β–lactam antibiotics. J Org Chem 78:4207–4213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SW, de Lencastre H, Tomasz A (2001) Recruitment of the mecA Gene Homologue of Staphylococcus sciuri into a resistance determinant and expression of the resistant phenotype in Staphylococcus aureus. J Bacteriol 183:2417–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto H, Miyake Y, Hisaoka M, Kurosawa S, Sekiguchi J (2008) The major and minor wall teichoic acids prevent the sidewall localization of vegetative DL–endopeptidase LytF in Bacillus subtilis. Mol Microbiol 70:297–310

    Article  CAS  PubMed  Google Scholar 

  • Zahrl D, Wagner M, Bischof K, Bayer M, Zavecz B, Beranek A, Ruckenstuhl C, Zarfel GE, Koraimann G (2005) Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems. Microbiology 151:3455–3467

    Article  CAS  PubMed  Google Scholar 

  • Zervosen A, Lu WP, Chen Z, White RE, Demuth TP Jr, Frère JM (2004) Interactions between penicillin-binding proteins (PBPs) and two novel classes of PBP inhibitors, arylalkylidene rhodanines and arylalkylidene iminothiazolidin-4-ones. Antimicrob Agents Chemother 48:961–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhanel GG, Lam A, Schweizer F, Thomson K, Walkty A, Rubinstein E, Gin AS, Hoban DJ, Noreddin AM, Karlowsky JA (2008) Ceftobiprole: a review of a broad–spectrum and anti-MRSA cephalosporin. Am J Clin Dermatol 9:245–254

    Article  PubMed  Google Scholar 

  • Zhanel GG, Sniezek G, Schweizer F, Zelenitsky S, Lagacé-Wiens PR, Rubinstein E, Gin AS, Hoban DJ, Karlowsky JA (2009) Ceftaroline: a novel broad-spectrum cephalosporin with activity against meticillin-resistant Staphylococcus aureus. Drugs 69:809–831

    Article  CAS  PubMed  Google Scholar 

  • Zindel S, Kaman WE, Fröls S, Pfeifer F, Peters A, Hays JP, Fuchsbauer HL (2013) The papain inhibitor (SPI) of Streptomyces mobaraensis inhibits bacterial cysteine proteases and is an antagonist of bacterial growth. Antimicrob Agents Chemother 57:3388–3391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors want to thank the European Union (FP7-ENVIRONMENT 2012-two-stage (BIOCORIN, project reference: 28288) and the Spanish Ministry of Economy and Competitively (Madrid, Spain) [Subprogramme for Non-Guided Fundamental Research Projects 2012 (FAES, project reference: CTM2012-320269)].

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  1. INBIOTEC (Instituto de Biotecnología de León), Parque Científico de León, Avda, Real 1, 24006, León, Spain

    Ricardo V. Ullán & Carlos Barreiro

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  1. Ricardo V. Ullán
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  2. Carlos Barreiro
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Correspondence to Ricardo V. Ullán .

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  1. Faculty of Pharmacy, University of Santiago de Compostel, Santiago de Compostela, Spain

    Tomas G. Villa

  2. Faculty of Medicine, University of Barcelona, L'Hospitalet de Llobregat, Spain

    Miguel Vinas

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Ullán, R.V., Barreiro, C. (2016). Bacterial Proteases as Targets to Control Bacterial Growth. In: Villa, T., Vinas, M. (eds) New Weapons to Control Bacterial Growth. Springer, Cham. https://doi.org/10.1007/978-3-319-28368-5_7

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