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Inhibition and Activity Regulation of Bacterial Collagenases

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Zinc Enzyme Inhibitors

Part of the book series: Topics in Medicinal Chemistry ((TMC,volume 22))

Abstract

The imminent antimicrobial resistance dilemma requests for drug discovery initiatives outside the box of classical antibiotics strategies, including the identification of anti-virulence targets. Given their critical roles in diverse infectious diseases, bacterial collagenases constitute one such class of anti-virulence targets. Here we review the essential catalytic elements of bacterial collagenases, including the zinc-coordinating residues, as well as their typical domain organization with relevance to collagenolysis. We further present the structural basis for the substrate specificities, both towards linear and triple-helical peptides. These enzymatic properties shape the structural framework for the discovery and development of competitive, active site-directed inhibitors. While currently available compounds bind the catalytic zinc, alternative interaction possibilities at the active site promise an improved specificity towards other metalloproteases. We finally outline inhibition opportunities that result from exploiting collagenase exosites.

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References

  1. Directorate-General Health and Food Safety EC (2015) AMR: A major European and Global challenge. Factsheet 2. http://ec.europa.eu/dgs/health_food-safety/docs/amr_factsheet_en.pdf. Accessed 10 Dec 2015

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

    Book  Google Scholar 

  3. Cross AS (2008) What is a virulence factor? Crit Care 12:196

    Article  Google Scholar 

  4. Travis J, Potempa J, Maeda H (1995) Are bacterial proteinases pathogenic factors? Trends Microbiol 3:405–407

    Article  CAS  Google Scholar 

  5. Miyoshi S-I, Shinoda S (1997) Bacterial metalloprotease as the toxic factor in infection. J Toxicol Toxin Rev 16:177–194

    Article  CAS  Google Scholar 

  6. Lebrun I, Marques-Porto R, Pereira AS, Pereira A, Perpetuo EA (2009) Bacterial toxins: an overview on bacterial proteases and their action as virulence factors. Mini Rev Med Chem 9:820–828

    Article  CAS  Google Scholar 

  7. Finlay BB, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61:136–169

    CAS  Google Scholar 

  8. Duerden BI (1994) Virulence factors in anaerobes. Clin Infect Dis 18(Suppl 4):S253–S259

    Article  Google Scholar 

  9. Burgeson RE, Nimni ME (1992) Collagen types. Molecular structure and tissue distribution. Clin Orthop Relat Res 282:250–272

    Google Scholar 

  10. Brozek J, Grande F, Anderson JT, Keys A (1963) Densitrometric analysis of body composition: revision of some quantitative assumptions. Ann N Y Acad Sci 110:113–140

    Article  CAS  Google Scholar 

  11. Ramshaw JA, Shah NK, Brodsky B (1998) Gly-X-Y tripeptide frequencies in collagen: a context for host-guest triple-helical peptides. J Struct Biol 122:86–91

    Article  CAS  Google Scholar 

  12. Bruckner P, Prockop DJ (1981) Proteolytic enzymes as probes for the triple-helical conformation of procollagen. Anal Biochem 110:360–368

    Article  CAS  Google Scholar 

  13. Bächinger HP, Bruckner P, Timpl R, Prockop DJ, Engel J (1980) Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Role of disulfide bridges and peptide bond isomerization. Eur J Biochem 106:619–632

    Article  Google Scholar 

  14. Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69:562–573

    Article  CAS  Google Scholar 

  15. Fields GB (2013) Interstitial collagen catabolism. J Biol Chem 288:8785–8793

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  17. 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  Google Scholar 

  18. Gadasi H, Kessler E (1983) Correlation of virulence and collagenolytic activity in Entamoeba histolytica. Infect Immun 39:528–531

    CAS  Google Scholar 

  19. Muñoz M, Rojkind M, Calderon J, Tanimoto M, Arias-Negrete S, Martinze-Palomo A (1984) Entamoeba histolytica: collagenolytic activity and virulence 1. J Protozool 31:468–470

    Article  Google Scholar 

  20. Magos M, La Torre MD, Muñoz M (1991) Collagenase activity in clinical isolates of Entamoeba histolytica maintained in xenic cultures. Arch Med Res 23:115–118

    Google Scholar 

  21. Hatheway CL (1990) Toxigenic clostridia. Clin Microbiol Rev 3:66–98

    Article  CAS  Google Scholar 

  22. Bruggemann H, Baumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, Herzberg C, Martinez-Arias R, Merkl R, Henne A, Gottschalk G (2003) The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc Natl Acad Sci U S A 100:1316–1321

    Article  CAS  Google Scholar 

  23. Smith-Slatas CL, Bourque M, Salazar JC (2006) Clostridium septicum infections in children: a case report and review of the literature. Pediatrics 117:e796–e805

    Article  Google Scholar 

  24. Hsu HY, Lee SF, Hartstein ME, Harocopos GJ (2008) Clostridium perfringens keratitis leading to blinding panophthalmitis. Cornea 27:1200–1203

    Article  Google Scholar 

  25. Badenoch PR, Aggarwal RK, Coster DJ (1995) Clostridium perfringens keratitis after penetrating keratoplasty. Aust N Z J Ophthalmol 23:245–246

    Article  CAS  Google Scholar 

  26. McAllister CM, Zillmer D, Cobelli NJ (1989) Clostridium perfringens and Staphylococcus epidermidis polymicrobial septic arthritis. A case report. Clin Orthop Relat Res 241:245–247

    Google Scholar 

  27. Harrington DJ (1996) Bacterial collagenases and collagen-degrading enzymes and their potential role in human disease. Infect Immun 64:1885–1891

    CAS  Google Scholar 

  28. Li J, Adams V, Bannam TL, Miyamoto K, Garcia JP, Uzal FA, Rood JI, McClane BA (2013) Toxin plasmids of Clostridium perfringens. Microbiol Mol Biol Rev 77:208–233

    Article  CAS  Google Scholar 

  29. Zanella Terrier MC, Simonet ML, Bichard P, Frossard JL (2014) Recurrent Clostridium difficile infections: the importance of the intestinal microbiota. World J Gastroenterol 20:7416–7423

    Article  Google Scholar 

  30. Seddon SV, Hemingway I, Borriello SP (1990) Hydrolytic enzyme production by Clostridium difficile and its relationship to toxin production and virulence in the hamster model. J Med Microbiol 31:169–174

    Article  CAS  Google Scholar 

  31. Poilane I, Karjalainen T, Barc MC, Bourlioux P, Collignon A (1998) Protease activity of Clostridium difficile strains. Can J Microbiol 44:157–161

    Article  CAS  Google Scholar 

  32. Aldape MJ, Bryant AE, Stevens DL (2006) Clostridium sordellii infection: epidemiology, clinical findings, and current perspectives on diagnosis and treatment. Clin Infect Dis 43:1436–1446

    Article  CAS  Google Scholar 

  33. MacLennan J, Mandl I, Howes E (1953) Bacterial digestion of collagen. J Clin Invest 32:1317–1322

    Article  CAS  Google Scholar 

  34. Spencer RC (2003) Bacillus anthracis. J Clin Pathol 56:182–187

    Article  CAS  Google Scholar 

  35. Evans DG, Wardlaw AC (1953) Gelatinase and collagenase production by certain species of Bacillus. J Gen Microbiol 8:481–487

    Article  CAS  Google Scholar 

  36. Bottone EJ (2010) Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23:382–398

    Article  Google Scholar 

  37. Makinen KK, Makinen PL (1987) Purification and properties of an extracellular collagenolytic protease produced by the human oral bacterium Bacillus cereus (strain Soc 67). J Biol Chem 262:12488–12495

    CAS  Google Scholar 

  38. Liu L, Ma M, Yu X, Wang W (2010) Screening of collagenase-producing strain and purification of Bacillus cereus collagenase. Chin J Biotechnol 26:194–200

    Article  CAS  Google Scholar 

  39. Guinebretière M-H, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser M-L, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus Group occasionally associated with food poisoning. Int J Syst Evol Microbiol 63:31–40

    Article  Google Scholar 

  40. Evangelista KV, Coburn J (2010) Leptospira as an emerging pathogen: a review of its biology, pathogenesis and host immune responses. Future Microbiol 5:1413–1425

    Article  Google Scholar 

  41. Ahmed N, Devi SM, Valverde M, de los A, Vijayachari P, Machang’u RS, Ellis WA, Hartskeerl RA (2006) Multilocus sequence typing method for identification and genotypic classification of pathogenic Leptospira species. Ann Clin Microbiol Antimicrob 5:28

    Google Scholar 

  42. Kassegne K, Hu W, Ojcius DM, Sun D, Ge Y, Zhao J, Yang XF, Li L, Yan J (2014) Identification of collagenase as a critical virulence factor for invasiveness and transmission of pathogenic Leptospira species. J Infect Dis 209:1105–1115

    Article  CAS  Google Scholar 

  43. van de Sande WWJ (2013) Global burden of human mycetoma: a systematic review and meta-analysis. PLoS Negl Trop Dis 7, e2550

    Article  Google Scholar 

  44. Venkatswami S, Sankarasubramanian A, Subramanyam S (2012) The madura foot: looking deep. Int J Low Extrem Wounds 11:31–42

    Article  Google Scholar 

  45. Rippon JW, Peck GL (1967) Experimental infection with Streptomyces madurae as a function of collagenase. J Invest Dermatol 49:371–378

    Article  CAS  Google Scholar 

  46. Tantillo GM, Fontanarosa M, Di Pinto A, Musti M (2004) Updated perspectives on emerging vibrios associated with human infections. Lett Appl Microbiol 39:117–126

    Article  CAS  Google Scholar 

  47. Miyoshi S (2013) Extracellular proteolytic enzymes produced by human pathogenic vibrio species. Front Microbiol 4:339

    Article  Google Scholar 

  48. West PA (1989) The human pathogenic vibrios–a public health update with environmental perspectives. Epidemiol Infect 103:1–34

    Article  CAS  Google Scholar 

  49. Broberg CA, Calder TJ, Orth K (2011) Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect 13:992–1001

    Article  CAS  Google Scholar 

  50. Park BR, Zielke RA, Wierzbicki IH, Mitchell KC, Withey JH, Sikora AE (2015) A metalloprotease secreted by the type II secretion system links Vibrio cholerae with collagen. J Bacteriol 197:1051–1064

    Article  CAS  Google Scholar 

  51. Jones MK, Oliver JD (2009) Vibrio vulnificus: disease and pathogenesis. Infect Immun 77:1723–1733

    Article  CAS  Google Scholar 

  52. Kang S-I, Jang Y-B, Choi Y-J, Kong J-Y (2005) Purification and properties of a collagenolytic protease produced by marine bacterium Vibrio vulnificus CYK279H. Biotechnol Bioprocess Eng 10:593–598

    Article  CAS  Google Scholar 

  53. The UniProt Consortium (2014) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212

    Article  Google Scholar 

  54. Brüggemann H, Brzuszkiewicz E, Chapeton-Montes D, Plourde L, Speck D, Popoff MR (2015) Genomics of Clostridium tetani. Res Microbiol 166:326–331

    Article  CAS  Google Scholar 

  55. Popoff MR, Bouvet P (2009) Clostridial toxins. Future Microbiol 4:1021–1064

    Article  CAS  Google Scholar 

  56. Smith LD (1979) Virulence factors of Clostridium perfringens. Rev Infect Dis 1:254–262

    Article  CAS  Google Scholar 

  57. Peterkofsky B (1982) Bacterial collagenase. Methods Enzymol 82:453–471

    Article  CAS  Google Scholar 

  58. Gupta A, Khanna S (2014) Community-acquired Clostridium difficile infection: an increasing public health threat. Infect Drug Resist 7:63–72

    Google Scholar 

  59. Borriello SP, Ketley JM, Mitchell TJ, Barclay FE, Welch AR, Price AB, Stephen J (1987) Clostridium difficile--a spectrum of virulence and analysis of putative virulence determinants in the hamster model of antibiotic-associated colitis. J Med Microbiol 24:53–64

    Article  CAS  Google Scholar 

  60. Gui L, Subramony C, Fratkin J, Hughson MD (2002) Fatal enteritis necroticans (pigbel) in a diabetic adult. Mod Pathol 15:66–70

    Article  Google Scholar 

  61. Olkowski AA, Wojnarowicz C, Chirino-Trejo M, Drew MD (2006) Responses of broiler chickens orally challenged with Clostridium perfringens isolated from field cases of necrotic enteritis. Res Vet Sci 81:99–108

    Article  CAS  Google Scholar 

  62. Olkowski AA, Wojnarowicz C, Chirino-Trejo M, Laarveld B, Sawicki G (2008) Sub-clinical necrotic enteritis in broiler chickens: novel etiological consideration based on ultra-structural and molecular changes in the intestinal tissue. Res Vet Sci 85:543–553

    Article  CAS  Google Scholar 

  63. Pithadia AB, Jain S (2011) Treatment of inflammatory bowel disease (IBD). Pharmacol Rep 63:629–642

    Article  CAS  Google Scholar 

  64. Sohrabpour AA, Malekzadeh R, Keshavarzian A (2010) Current therapeutic approaches in inflammatory bowel disease. Curr Pharm Des 16:3668–3683

    Article  CAS  Google Scholar 

  65. Carroll IM, Maharshak N (2013) Enteric bacterial proteases in inflammatory bowel disease-pathophysiology and clinical implications. World J Gastroenterol 19:7531–7543

    Article  CAS  Google Scholar 

  66. Pruteanu M, Hyland NP, Clarke DJ, Kiely B, Shanahan F (2011) Degradation of the extracellular matrix components by bacterial-derived metalloproteases: implications for inflammatory bowel diseases. Inflamm Bowel Dis 17:1189–1200

    Article  Google Scholar 

  67. Hart G, Strauss M (1990) Gas gangrene – clostridial myonecrosis: a review. J Hyperb Med J Hyperba 5:125–144

    Google Scholar 

  68. Stevens DL (2000) The pathogenesis of clostridial myonecrosis. Int J Med Microbiol 290:497–502

    Article  CAS  Google Scholar 

  69. Legat FJ, Griesbacher T, Lembeck F (1994) Mediation by bradykinin of rat paw oedema induced by collagenase from Clostridium histolyticum. Br J Pharmacol 112:453–460

    Article  CAS  Google Scholar 

  70. Vargaftig BB, Lefort J, Giroux EL (1976) Haemorrhagic and inflammatory properties of collagenase from C. histolyticum. Agents Actions 6:627–635

    Article  CAS  Google Scholar 

  71. Scallan J, Huxley VH, Korthuis RJ (2010) Capillary fluid exchange: regulation, functions, and pathology. Morgan & Claypool Life Sciences, San Rafael, pp 47–53

    Google Scholar 

  72. Awad MM, Ellemor DM, Bryant AE, Matsushita O, Boyd RL, Stevens DL, Emmins JJ, Rood JI (2000) Construction and virulence testing of a collagenase mutant of Clostridium perfringens. Microb Pathog 28:107–117

    Article  CAS  Google Scholar 

  73. Jung CM, Matsushita O, Katayama S, Minami J, Sakurai J, Okabe A (1999) Identification of metal ligands in the Clostridium histolyticum ColH collagenase. J Bacteriol 181:2816–2822

    CAS  Google Scholar 

  74. Eckhard U, Schönauer E, Nüss D, Brandstetter H (2011) Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Nat Struct Mol Biol 18:1109–1114

    Article  CAS  Google Scholar 

  75. Eckhard U, Schönauer E, Brandstetter H (2013) Structural basis for activity regulation and substrate preference of clostridial collagenases g, h, and T. J Biol Chem 288:20184–20194

    Article  CAS  Google Scholar 

  76. Duarte AS, Correia A, Esteves AC (2016) Bacterial collagenases – a review. Crit Rev Microbiol 42:106–126

    Google Scholar 

  77. Lopez-Pelegrin M, Cerda-Costa N, Martinez-Jimenez F, Cintas-Pedrola A, Canals A, Peinado JR, Marti-Renom MA, Lopez-Otin C, Arolas JL, Gomis-Rüth FX (2013) A novel family of soluble minimal scaffolds provides structural insight into the catalytic domains of integral membrane metallopeptidases. J Biol Chem 288:21279–21294

    Article  CAS  Google Scholar 

  78. Matthews BW (1988) Structural basis of the action of thermolysin and related zinc peptidases. Acc Chem Res 21:333–340

    Article  CAS  Google Scholar 

  79. Kato T, Takahashi N, Kuramitsu HK (1992) Sequence analysis and characterization of the Porphyromonas gingivalis prtC gene, which expresses a novel collagenase activity. J Bacteriol 174:3889–3895

    CAS  Google Scholar 

  80. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H, Holden MTG, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38:779–786

    Article  CAS  Google Scholar 

  81. Lee JH, Kim GT, Lee JY, Jun HK, Yu JH, Kong IS (1998) Isolation and sequence analysis of metalloprotease gene from Vibrio mimicus. Biochim Biophys Acta 1384:1–6

    Article  CAS  Google Scholar 

  82. Yu MS, Lee CY (1999) Expression and characterization of the prtV gene encoding a collagenase from Vibrio parahaemolyticus in Escherichia coli. Microbiology 145(Pt 1):143–150

    Google Scholar 

  83. Keil B (1992) Vibrio alginolyticus (“Achromobacter”) collagenase: biosynthesis, function and application. Matrix Suppl 1:127–133

    CAS  Google Scholar 

  84. Teramura N, Tanaka K, Iijima K, Hayashida O, Suzuki K, Hattori S, Irie S (2011) Cloning of a novel collagenase gene from the gram-negative bacterium Grimontia (Vibrio) hollisae 1706B and its efficient expression in Brevibacillus choshinensis. J Bacteriol 193:3049–3056

    Article  CAS  Google Scholar 

  85. Lee J-H, Ahn S-H, Lee E-M, Kim Y-O, Lee S-J, Kong I-S (2003) Characterization of the enzyme activity of an extracellular metalloprotease (VMC) from Vibrio mimicus and its C-terminal deletions. FEMS Microbiol Lett 223:293–300

    Article  CAS  Google Scholar 

  86. Endo A, Murakawa S, Shimizu H, Shiraishi Y (1987) Purification and properties of collagenase from a Streptomyces species. J Biochem 102:163–170

    CAS  Google Scholar 

  87. Bond MD, Van Wart HE (1984) Characterization of the individual collagenases from Clostridium histolyticum. Biochemistry 23:3085–3091

    Article  CAS  Google Scholar 

  88. Matsushita O, Jung CM, Katayama S, Minami J, Takahashi Y, Okabe A (1999) Gene duplication and multiplicity of collagenases in Clostridium histolyticum. J Bacteriol 181:923–933

    CAS  Google Scholar 

  89. Lee JH, Ahn SH, Lee EM, Jeong SH, Kim YO, Lee SJ, Kong IS (2005) The FAXWXXT motif in the carboxyl terminus of Vibrio mimicus metalloprotease is involved in binding to collagen. FEBS Lett 579:2507–2513

    Article  CAS  Google Scholar 

  90. Matsushita O, Koide T, Kobayashi R, Nagata K, Okabe A (2001) Substrate recognition by the collagen-binding domain of Clostridium histolyticum class I collagenase. J Biol Chem 276:8761–8770

    Article  CAS  Google Scholar 

  91. Matsushita O, Jung CM, Minami J, Katayama S, Nishi N, Okabe A (1998) A study of the collagen-binding domain of a 116-kDa Clostridium histolyticum collagenase. J Biol Chem 273:3643–3648

    Article  CAS  Google Scholar 

  92. Wang Y-K, Zhao G-Y, Li Y, Chen X-L, Xie B-B, Su H-N, Lv Y-H, He H-L, Liu H, Hu J, Zhou B-C, Zhang Y-Z (2010) Mechanistic insight into the function of the C-terminal PKD domain of the collagenolytic serine protease deseasin MCP-01 from deep sea Pseudoalteromonas sp. SM9913: binding of the PKD domain to collagen results in collagen swelling but does not unwind the. J Biol Chem 285:14285–14291

    Article  CAS  Google Scholar 

  93. Bond M, Van Wart H (1984) Purification and separation of individual collagenases of Clostridium histolyticum using red dye ligand chromatography. Biochemistry 23:3077–3085

    Article  CAS  Google Scholar 

  94. Bond MD, Van Wart HE (1984) Relationship between the individual collagenases of Clostridium histolyticum: evidence for evolution by gene duplication. Biochemistry 23:3092–3099

    Article  CAS  Google Scholar 

  95. Mitchell A, Chang H-Y, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong S-Y, Bateman A, Punta M, Attwood TK, Sigrist CJA, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD (2014) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213–D221

    Article  Google Scholar 

  96. Wilson JJ, Matsushita O, Okabe A, Sakon J (2003) A bacterial collagen-binding domain with novel calcium-binding motif controls domain orientation. EMBO J 22:1743–1752

    Article  CAS  Google Scholar 

  97. Toyoshima T, Matsushita O, Minami J, Nishi N, Okabe A, Itano T (2001) Collagen-binding domain of a Clostridium histolyticum collagenase exhibits a broad substrate spectrum both in vitro and in vivo. Connect Tissue Res 42:281–290

    Article  CAS  Google Scholar 

  98. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millán JL, Gamble V, Harris PC (1995) The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151–160

    Article  CAS  Google Scholar 

  99. Bycroft M, Bateman A, Clarke J, Hamill SJ, Sandford R, Thomas RL, Chothia C (1999) The structure of a PKD domain from polycystin-1: implications for polycystic kidney disease. EMBO J 18:297–305

    Article  CAS  Google Scholar 

  100. Eckhard U, Brandstetter H (2011) Polycystic kidney disease-like domains of clostridial collagenases and their role in collagen recruitment. Biol Chem 392:1039–1045

    Article  CAS  Google Scholar 

  101. Ohbayashi N, Yamagata N, Goto M, Watanabe K, Yamagata Y, Murayama K (2012) Enhancement of the structural stability of full-length clostridial collagenase by calcium ions. Appl Environ Microbiol 78:5839–5844

    Article  CAS  Google Scholar 

  102. Zhao G-Y, Chen X-L, Zhao H-L, Xie B-B, Zhou B-C, Zhang Y-Z (2008) Hydrolysis of insoluble collagen by deseasin MCP-01 from deep-sea Pseudoalteromonas sp. SM9913: collagenolytic characters, collagen-binding ability of C-terminal polycystic kidney disease domain, and implication for its novel role in deep-sea sedimentary. J Biol Chem 283:36100–36107

    Article  CAS  Google Scholar 

  103. Gross J, Nagai Y (1965) Specific degradation of the collagen molecule by tadpole collagenolytic enzyme. Proc Natl Acad Sci U S A 54:1197–1204

    Article  CAS  Google Scholar 

  104. Welgus HG, Jeffrey JJ, Eisen AZ (1981) Human skin fibroblast collagenase. Assessment of activation energy and deuterium isotope effect with collagenous substrates. J Biol Chem 256:9516–9521

    CAS  Google Scholar 

  105. Hasty KA, Jeffrey JJ, Hibbs MS, Welgus HG (1987) The collagen substrate specificity of human neutrophil collagenase. J Biol Chem 262:10048–10052

    CAS  Google Scholar 

  106. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G (1996) Biochemical characterization of human collagenase-3. J Biol Chem 271:1544–1550

    Article  CAS  Google Scholar 

  107. Seifter S, Harper E (1971) The enzymes. Academic, New York, pp 649–697

    Google Scholar 

  108. Mookhtiar KA, Van Wart HE (1992) Clostridium histolyticum collagenases: a new look at some old enzymes. Matrix Suppl 1:116–126

    CAS  Google Scholar 

  109. Mallya SK, Mookhtiar KA, Van Wart HE (1992) Kinetics of hydrolysis of type I, II, and III collagens by the class I and II Clostridium histolyticum collagenases. J Protein Chem 11:99–107

    Article  CAS  Google Scholar 

  110. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K (2009) Improved visualization of protein consensus sequences by iceLogo. Nat Methods 6:786–787

    Article  CAS  Google Scholar 

  111. Eckhard U, Huesgen PF, Brandstetter H, Overall CM (2014) Proteomic protease specificity profiling of clostridial collagenases reveals their intrinsic nature as dedicated degraders of collagen. J Proteomics 100:102–114

    Article  CAS  Google Scholar 

  112. Allen Foegeding E, Larick DK (1986) Tenderization of beef with bacterial collagenase. Meat Sci 18:201–214

    Article  CAS  Google Scholar 

  113. Kanth SV, Venba R, Madhan B, Chandrababu NK, Sadulla S (2008) Studies on the influence of bacterial collagenase in leather dyeing. Dye Pigment 76:338–347

    Article  CAS  Google Scholar 

  114. Wendt MD, Rockway TW, Geyer A, McClellan W, Weitzberg M, Zhao X, Mantei R, Nienaber VL, Stewart K, Klinghofer V, Giranda VL (2004) Identification of novel binding interactions in the development of potent, selective 2-naphthamidine inhibitors of urokinase. Synthesis, structural analysis, and SAR of N-phenyl amide 6-substitution. J Med Chem 47:303–324

    Article  CAS  Google Scholar 

  115. Zhao G-Y, Zhou M-Y, Zhao H-L, Chen X-L, Xie B-B, Zhang X-Y, He H-L, Zhou B-C, Zhang Y-Z (2012) Tenderization effect of cold-adapted collagenolytic protease MCP-01 on beef meat at low temperature and its mechanism. Food Chem 134:1738–1744

    Article  CAS  Google Scholar 

  116. Raven RB, Kushner H, Nguyen D, Naam N, Curtin C (2013) Analysis of efficacy and safety of treatment with collagenase Clostridium histolyticum among subgroups of patients with dupuytren contracture. Ann Plast Surg 73:286–290

    Article  CAS  Google Scholar 

  117. Zhou C, Hovius SER, Slijper HP, Feitz R, Van Nieuwenhoven CA, Pieters AJ, Selles RW (2015) Collagenase Clostridium histolyticum versus limited fasciectomy for dupuytren’s contracture. Plast Reconstr Surg 136:87–97

    Article  CAS  Google Scholar 

  118. Fischer S, Hirsch T, Diehm Y, Kiefer J, Bueno EM, Kueckelhaus M, Kremer T, Hirche C, Kneser U, Pomahac B (2015) The collagenase of the bacterium Clostridium histolyticum for the treatment of capsular fibrosis after silicon implants. Plast Reconstr Surg 136:981–989

    Article  CAS  Google Scholar 

  119. Dhillon S (2015) Collagenase Clostridium histolyticum: a review in Peyronie’s disease. Drugs 75:1405–1412

    Article  CAS  Google Scholar 

  120. Ramundo J, Gray M (2009) Collagenase for enzymatic debridement: a systematic review. J Wound Ostomy Continence Nurs 36:S4–S11

    Article  Google Scholar 

  121. Brunengraber LN, Jayes FL, Leppert PC (2014) Injectable Clostridium histolyticum collagenase as a potential treatment for uterine fibroids. Reprod Sci 21:1452–1459

    Article  CAS  Google Scholar 

  122. Oshima N, Narukawa Y, Takeda T, Kiuchi F (2013) Collagenase inhibitors from Viola yedoensis. J Nat Med 67:240–245

    Article  CAS  Google Scholar 

  123. Tanaka T, Metori K, Mineo S, Hirotani M, Furuya T, Matsumoto H, Satoh T, Kobayashi S (1991) Studies on collagenase inhibitors. IV. Inhibitors of bacterial collagenase in Coptidis rhizoma. Yakugaku Zasshi 111:538–541

    CAS  Google Scholar 

  124. Thring TSA, Hili P, Naughton DP (2009) Anti-collagenase, anti-elastase and anti-oxidant activities of extracts from 21 plants. BMC Complement Altern Med 9:27

    Article  CAS  Google Scholar 

  125. Grobelny D, Galardy RE (1985) Aldehyde and ketone substrate analogues inhibit the collagenase of Clostridium histolyticum. Biochemistry 24:6145–6152

    Article  CAS  Google Scholar 

  126. Vencill CF, Rasnick D, Crumley KV, Nishino N, Powers JC (1985) Clostridium histolyticum collagenase: development of new thio ester, fluorogenic, and depsipeptide substrates and new inhibitors. Biochemistry 24:3149–3157

    Article  CAS  Google Scholar 

  127. Dive V, Yiotakis A, Nicolaou A, Toma F (1990) Inhibition of Clostridium histolyticum collagenases by phosphonamide peptide inhibitors. Eur J Biochem 191:685–693

    Article  CAS  Google Scholar 

  128. Supuran CT, Scozzafava A (2000) Protease inhibitors. Part 7. Inhibition of Clostridium histolyticum collagenase with sulfonylated derivatives of L-valine hydroxamate. Eur J Pharm Sci 10:67–76

    Article  CAS  Google Scholar 

  129. Scozzafava A, Supuran CT (2000) Protease inhibitors. Part 8: synthesis of potent Clostridium histolyticum collagenase inhibitors incorporating sulfonylated L-alanine hydroxamate moieties. Bioorg Med Chem 8:637–645

    Article  CAS  Google Scholar 

  130. Scozzafava A, Ilies MA, Manole G, Supuran CT (2000) Protease inhibitors. Part 12. Synthesis of potent matrix metalloproteinase and bacterial collagenase inhibitors incorporating sulfonylated N-4-nitrobenzyl-beta-alanine hydroxamate moieties. Eur J Pharm Sci 11:69–79

    Article  CAS  Google Scholar 

  131. Supuran CT, Briganti F, Mincione G, Scozzafava A (2000) Protease inhibitors: synthesis of L-alanine hydroxamate sulfonylated derivatives as inhibitors of clostridium histolyticum collagenase. J Enzyme Inhib 15:111–128

    Article  CAS  Google Scholar 

  132. Ilies MAM, Banciu MD, Scozzafava A, Ilies MAM, Caproiu MT, Supuran CT (2003) Protease inhibitors: synthesis of bacterial collagenase and matrix metalloproteinase inhibitors incorporating arylsulfonylureido and 5-dibenzo-suberenyl/suberyl moieties. Bioorg Med Chem 11:2227–2239

    Article  CAS  Google Scholar 

  133. Galardy RE, Grobelny D (1983) Inhibition of collagenase from Clostridium histolyticum by phosphoric and phosphonic amides. Biochemistry 22:4556–4561

    Article  CAS  Google Scholar 

  134. Van Wart HE, Steinbrink DR (1981) A continuous spectrophotometric assay for Clostridium histolyticum collagenase. Anal Biochem 113:356–365

    Article  Google Scholar 

  135. Wünsch E, Heidrich HH-G (1963) Zur quantitativen Bestimmung der Kollagenase. Hoppe-Seyler‘s Zeitschrift für Physiol. Chemie 333:149–151

    Google Scholar 

  136. Jacobsen FE, Lewis JA, Cohen SM (2007) The design of inhibitors for medicinally relevant metalloproteins. ChemMedChem 2:152–171

    Article  CAS  Google Scholar 

  137. Rouffet M, Cohen SM (2011) Emerging trends in metalloprotein inhibition. Dalt Trans 40:3445–3454

    Article  CAS  Google Scholar 

  138. Castelhano AL, Billedeau R, Dewdney N, Donnelly S, Horne S, Kurz LJ, Liak TJ, Martin R, Uppington R, Krantz A (1995) Novel indolactam-based inhibitors of matrix metalloproteinases. Bioorg Med Chem Lett 5:1415–1420

    Article  CAS  Google Scholar 

  139. Scozzafava A, Supuran CT (2000) Carbonic anhydrase and matrix metalloproteinase inhibitors: sulfonylated amino acid hydroxamates with MMP inhibitory properties act as efficient inhibitors of CA isozymes I, II, and IV, and N-hydroxysulfonamides inhibit both these zinc enzymes. J Med Chem 43:3677–3687

    Article  CAS  Google Scholar 

  140. Clare BW, Scozzafava A, Supuran CT (2001) Protease inhibitors: synthesis of a series of bacterial collagenase inhibitors of the sulfonyl amino acyl hydroxamate type. J Med Chem 44:2253–2258

    Article  CAS  Google Scholar 

  141. Scozzafava A, Supuran CT (2000) Protease inhibitors – part 5. Alkyl/arylsulfonyl- and arylsulfonylureido-/arylureido-glycine hydroxamate inhibitors of Clostridium histolyticum collagenase. Eur J Med Chem 35:299–307

    Article  CAS  Google Scholar 

  142. Santos MA, Marques S, Gil M, Tegoni M, Scozzafava A, Supuran CT (2003) Protease inhibitors: synthesis of bacterial collagenase and matrix metalloproteinase inhibitors incorporating succinyl hydroxamate and iminodiacetic acid hydroxamate moieties. J Enzyme Inhib Med Chem 18:233–242

    Article  CAS  Google Scholar 

  143. Supuran CT (2009) Drug design of zinc-enzyme inhibitors. Wiley, Hoboken, pp 721–729

    Book  Google Scholar 

  144. Scozzafava A, Supuran CT (2002) Protease inhibitors: synthesis of matrix metalloproteinase and bacterial collagenase inhibitors incorporating 5-amino-2-mercapto-1,3,4-thiadiazole zinc binding functions. Bioorg Med Chem Lett 12:2667–2672

    Article  CAS  Google Scholar 

  145. Park HI, Jin Y, Hurst DR, Monroe CA, Lee S, Schwartz MA, Sang Q-XA (2003) The intermediate S1′ pocket of the endometase/matrilysin-2 active site revealed by enzyme inhibition kinetic studies, protein sequence analyses, and homology modeling. J Biol Chem 278:51646–51653

    Article  CAS  Google Scholar 

  146. Jacobsen JA, Major Jourden JL, Miller MT, Cohen SM (2010) To bind zinc or not to bind zinc: an examination of innovative approaches to improved metalloproteinase inhibition. Biochim Biophys Acta 1803:72–94

    Article  CAS  Google Scholar 

  147. Jacobsen EJ, Mitchell MA, Hendges SK, Belonga KL, Skaletzky LL, Stelzer LS, Lindberg TJ, Fritzen EL, Schostarez HJ, O’Sullivan TJ, Maggiora LL, Stuchly CW, Laborde AL, Kubicek MF, Poorman RA, Beck JM, Miller HR, Petzold GL, Scott PS, Truesdell SE, Wallace TL, Wilks JW, Fisher C, Goodman LV, Kaytes PS (1999) Synthesis of a series of stromelysin-selective thiadiazole urea matrix metalloproteinase inhibitors. J Med Chem 42:1525–1536

    Article  CAS  Google Scholar 

  148. Stockman BJ, Waldon DJ, Gates JA, Scahill TA, Kloosterman DA, Mizsak SA, Jacobsen EJ, Belonga KL, Mitchell MA, Mao B, Petke JD, Goodman L, Powers EA, Ledbetter SR, Kaytes PS, Vogeli G, Marshall VP, Petzold GL, Poorman RA (1998) Solution structures of stromelysin complexed to thiadiazole inhibitors. Protein Sci 7:2281–2286

    Article  CAS  Google Scholar 

  149. Park S, Kim J-K, Oh CJ, Choi SH, Jeon J-H, Lee I-K (2015) Scoparone interferes with STAT3-induced proliferation of vascular smooth muscle cells. Exp Mol Med 47, e145

    Article  CAS  Google Scholar 

  150. Hornick A, Lieb A, Vo NP, Rollinger JM, Stuppner H, Prast H (2011) The coumarin scopoletin potentiates acetylcholine release from synaptosomes, amplifies hippocampal long-term potentiation and ameliorates anticholinergic- and age-impaired memory. Neuroscience 197:280–292

    Article  CAS  Google Scholar 

  151. Lim NC, Schuster JV, Porto MC, Tanudra MA, Yao L, Freake HC, Brückner C (2005) Coumarin-based chemosensors for zinc(II): toward the determination of the design algorithm for CHEF-type and ratiometric probes. Inorg Chem 44:2018–2030

    Article  CAS  Google Scholar 

  152. Gomis-Rüth FX, Botelho TO, Bode W (2012) A standard orientation for metallopeptidases. Biochim Biophys Acta 1824:157–163

    Article  CAS  Google Scholar 

  153. Cerdà-Costa N, Xavier Gomis-Rüth FX (2014) Architecture and function of metallopeptidase catalytic domains. Protein Sci 23:123–144

    Article  CAS  Google Scholar 

  154. Gomis-Rüth FX (2009) Catalytic domain architecture of metzincin metalloproteases. J Biol Chem 284:15353–15357

    Article  CAS  Google Scholar 

  155. Bode W, Gomis-Rüth FX, Stöcker W, Stöckler W (1993) Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the “metzincins”. FEBS Lett 331:134–140

    Article  CAS  Google Scholar 

  156. Hooper NM (1994) Families of zinc metalloproteases. FEBS Lett 354:1–6

    Article  CAS  Google Scholar 

  157. DeLano WL (2010) The PyMOL molecular graphics system, Version~1.3r1. Schrödinger, LLC, New York

    Google Scholar 

  158. Maskos K, Bode W (2003) Structural basis of matrix metalloproteinases and tissue inhibitors of metalloproteinases. Mol Biotechnol 25:241–266

    Article  CAS  Google Scholar 

  159. Maskos K (2005) Crystal structures of MMPs in complex with physiological and pharmacological inhibitors. Biochimie 87:249–263

    Article  CAS  Google Scholar 

  160. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34:W116–W118

    Article  CAS  Google Scholar 

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  1. Department of Molecular Biology, University of Salzburg, 5020, Salzburg, Austria

    Esther Schönauer & Hans Brandstetter

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  1. Esther Schönauer
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  2. Hans Brandstetter
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  1. Neurofarba Department, University of Florence, Sesto Fiorentino (Firenze), Italy

    Claudiu T. Supuran

  2. Neurofarba Department, University of Florence, Sesto Fiorentino (Firenze), Italy

    Clemente Capasso

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Schönauer, E., Brandstetter, H. (2016). Inhibition and Activity Regulation of Bacterial Collagenases. In: Supuran, C., Capasso, C. (eds) Zinc Enzyme Inhibitors. Topics in Medicinal Chemistry, vol 22. Springer, Cham. https://doi.org/10.1007/7355_2016_9

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