2y3u Citations

Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis.

Nat Struct Mol Biol 18 1109-14 (2011)
Related entries: 2y50, 2y6i, 2y72

Cited: 57 times
EuropePMC logo PMID: 21947205

Abstract

Collagen constitutes one-third of body protein in humans, reflecting its extensive role in health and disease. Of similar importance, therefore, are the idiosyncratic proteases that have evolved for collagen remodeling. The most efficient collagenases are those that enable clostridial bacteria to colonize their host tissues; but despite intense study, the structural and mechanistic basis of these enzymes has remained elusive. Here we present the crystal structure of collagenase G from Clostridium histolyticum at 2.55-Å resolution. By combining the structural data with enzymatic and mutagenesis studies, we derive a conformational two-state model of bacterial collagenolysis, in which recognition and unraveling of collagen microfibrils into triple helices, as well as unwinding of the triple helices, are driven by collagenase opening and closing.

Articles - 2y3u mentioned but not cited (7)

  1. Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Eckhard U, Schönauer E, Nüss D, Brandstetter H. Nat. Struct. Mol. Biol. 18 1109-1114 (2011)
  2. Proteomic protease specificity profiling of clostridial collagenases reveals their intrinsic nature as dedicated degraders of collagen. Eckhard U, Huesgen PF, Brandstetter H, Overall CM. J Proteomics 100 102-114 (2014)
  3. Structural basis for activity regulation and substrate preference of clostridial collagenases G, H, and T. Eckhard U, Schönauer E, Brandstetter H. J. Biol. Chem. 288 20184-20194 (2013)
  4. Solution structure of clostridial collagenase H and its calcium-dependent global conformation change. Ohbayashi N, Matsumoto T, Shima H, Goto M, Watanabe K, Yamano A, Katoh Y, Igarashi K, Yamagata Y, Murayama K. Biophys. J. 104 1538-1545 (2013)
  5. Candidates for Repurposing as Anti-Virulence Agents Based on the Structural Profile Analysis of Microbial Collagenase Inhibitors. Nitulescu G, Nitulescu GM, Zanfirescu A, Mihai DP, Gradinaru D. Pharmaceutics 14 62 (2021)
  6. Discovery of a proteolytic flagellin family in diverse bacterial phyla that assembles enzymatically active flagella. Eckhard U, Bandukwala H, Mansfield MJ, Marino G, Cheng J, Wallace I, Holyoak T, Charles TC, Austin J, Overall CM, Doxey AC. Nat Commun 8 521 (2017)
  7. Cloning, Purification and Characterization of the Collagenase ColA Expressed by Bacillus cereus ATCC 14579. Abfalter CM, Schönauer E, Ponnuraj K, Huemer M, Gadermaier G, Regl C, Briza P, Ferreira F, Huber CG, Brandstetter H, Posselt G, Wessler S. PLoS ONE 11 e0162433 (2016)


Reviews citing this publication (6)

  1. Interstitial collagen catabolism. Fields GB. J. Biol. Chem. 288 8785-8793 (2013)
  2. Architecture and function of metallopeptidase catalytic domains. Cerdà-Costa N, Gomis-Rüth FX. Protein Sci. 23 123-144 (2014)
  3. Bacterial collagenases - A review. Duarte AS, Correia A, Esteves AC. Crit. Rev. Microbiol. 42 106-126 (2016)
  4. Diversity, Structures, and Collagen-Degrading Mechanisms of Bacterial Collagenolytic Proteases. Zhang YZ, Ran LY, Li CY, Chen XL. Appl. Environ. Microbiol. 81 6098-6107 (2015)
  5. Tension in fibrils suppresses their enzymatic degradation - A molecular mechanism for 'use it or lose it'. Saini K, Cho S, Dooling LJ, Discher DE. Matrix Biol 85-86 34-46 (2020)
  6. An Introduction to Bacterial Biofilms and Their Proteases, and Their Roles in Host Infection and Immune Evasion. Ramírez-Larrota JS, Eckhard U. Biomolecules 12 306 (2022)

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  1. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Manka SW, Carafoli F, Visse R, Bihan D, Raynal N, Farndale RW, Murphy G, Enghild JJ, Hohenester E, Nagase H. Proc. Natl. Acad. Sci. U.S.A. 109 12461-12466 (2012)
  2. Structural basis for matrix metalloproteinase 1-catalyzed collagenolysis. Bertini I, Fragai M, Luchinat C, Melikian M, Toccafondi M, Lauer JL, Fields GB. J. Am. Chem. Soc. 134 2100-2110 (2012)
  3. Metalloproteases meprin α and meprin β are C- and N-procollagen proteinases important for collagen assembly and tensile strength. Broder C, Arnold P, Vadon-Le Goff S, Konerding MA, Bahr K, Müller S, Overall CM, Bond JS, Koudelka T, Tholey A, Hulmes DJ, Moali C, Becker-Pauly C. Proc. Natl. Acad. Sci. U.S.A. 110 14219-14224 (2013)
  4. Structural basis of collagen fiber degradation by cathepsin K. Aguda AH, Panwar P, Du X, Nguyen NT, Brayer GD, Brömme D. Proc. Natl. Acad. Sci. U.S.A. 111 17474-17479 (2014)
  5. Conformational dynamics accompanying the proteolytic degradation of trimeric collagen I by collagenases. Adhikari AS, Glassey E, Dunn AR. J. Am. Chem. Soc. 134 13259-13265 (2012)
  6. Inhibition of Collagenase by Mycosporine-like Amino Acids from Marine Sources. Hartmann A, Gostner J, Fuchs JE, Chaita E, Aligiannis N, Skaltsounis L, Ganzera M. Planta Med. 81 813-820 (2015)
  7. Structural comparison of ColH and ColG collagen-binding domains from Clostridium histolyticum. Bauer R, Wilson JJ, Philominathan ST, Davis D, Matsushita O, Sakon J. J. Bacteriol. 195 318-327 (2013)
  8. Characterization of a novel subtilisin-like protease myroicolsin from deep sea bacterium Myroides profundi D25 and molecular insight into its collagenolytic mechanism. Ran LY, Su HN, Zhou MY, Wang L, Chen XL, Xie BB, Song XY, Shi M, Qin QL, Pang X, Zhou BC, Zhang YZ, Zhang XY. J. Biol. Chem. 289 6041-6053 (2014)
  9. Clostridium sordellii genome analysis reveals plasmid localized toxin genes encoded within pathogenicity loci. Couchman EC, Browne HP, Dunn M, Lawley TD, Songer JG, Hall V, Petrovska L, Vidor C, Awad M, Lyras D, Fairweather NF. BMC Genomics 16 392 (2015)
  10. Structural and mechanistic insights into collagen degradation by a bacterial collagenolytic serine protease in the subtilisin family. Ran LY, Su HN, Zhao GY, Gao X, Zhou MY, Wang P, Zhao HL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhang YZ. Mol. Microbiol. 90 997-1010 (2013)
  11. Enhancement of the structural stability of full-length clostridial collagenase by calcium ions. Ohbayashi N, Yamagata N, Goto M, Watanabe K, Yamagata Y, Murayama K. Appl. Environ. Microbiol. 78 5839-5844 (2012)
  12. Collagen V Is a Potential Substrate for Clostridial Collagenase G in Pancreatic Islet Isolation. Shima H, Inagaki A, Imura T, Yamagata Y, Watanabe K, Igarashi K, Goto M, Murayama K. J Diabetes Res 2016 4396756 (2016)
  13. Calcium binding by the PKD1 domain regulates interdomain flexibility in Vibrio cholerae metalloprotease PrtV. Edwin A, Rompikuntal P, Björn E, Stier G, Wai SN, Sauer-Eriksson AE. FEBS Open Bio 3 263-270 (2013)
  14. Identification and Characterization of Novel Matrix-Derived Bioactive Peptides: A Role for Collagenase from Santyl® Ointment in Post-Debridement Wound Healing? Sheets AR, Demidova-Rice TN, Shi L, Ronfard V, Grover KV, Herman IM. PLoS ONE 11 e0159598 (2016)
  15. Aeromonas piscicola AH-3 expresses an extracellular collagenase with cytotoxic properties. Duarte AS, Cavaleiro E, Pereira C, Merino S, Esteves AC, Duarte EP, Tomás JM, Correia AC. Lett. Appl. Microbiol. 60 288-297 (2015)
  16. Extracellular matrix alterations in low-grade lung adenocarcinoma compared with normal lung tissue by imaging mass spectrometry. Angel PM, Bruner E, Bethard J, Clift CL, Ball L, Drake RR, Feghali-Bostwick C. J Mass Spectrom 55 e4450 (2020)
  17. Phosphonate as a Stable Zinc-Binding Group for "Pathoblocker" Inhibitors of Clostridial Collagenase H (ColH). Voos K, Schönauer E, Alhayek A, Haupenthal J, Andreas A, Müller R, Hartmann RW, Brandstetter H, Hirsch AKH, Ducho C. ChemMedChem 16 1257-1267 (2021)
  18. Probing the kinetics of quantum dot-based proteolytic sensors. Díaz SA, Malonoski AP, Susumu K, Hofele RV, Oh E, Medintz IL. Anal Bioanal Chem 407 7307-7318 (2015)
  19. Human cathepsin L, a papain-like collagenase without proline specificity. Korenč M, Lenarčič B, Novinec M. FEBS J. 282 4328-4340 (2015)
  20. Identification and characterization of the proteolytic flagellin from the common freshwater bacterium Hylemonella gracilis. Eckhard U, Blöchl C, Jenkins BGL, Mansfield MJ, Huber CG, Doxey AC, Brandstetter H. Sci Rep 10 19052 (2020)
  21. Protein Truncating Variants of colA in Clostridium perfringens Type G Strains. Van Damme L, Cox N, Callens C, Dargatz M, Flügel M, Hark S, Thiemann F, Pelzer S, Haesebrouck F, Ducatelle R, Van Immerseel F, Goossens E. Front Cell Infect Microbiol 11 645248 (2021)
  22. Secretion of collagenases by Saccharomyces cerevisiae for collagen degradation. Xiao H, Liu X, Feng Y, Zheng L, Zhao M, Huang M. Biotechnol Biofuels Bioprod 15 89 (2022)
  23. Single-Molecule Assay for Proteolytic Susceptibility: Force-Induced Collagen Destabilization. Kirkness MWH, Forde NR. Biophys. J. 114 570-576 (2018)
  24. Discovery of a Potent Inhibitor Class with High Selectivity toward Clostridial Collagenases. Schönauer E, Kany AM, Haupenthal J, Hüsecken K, Hoppe IJ, Voos K, Yahiaoui S, Elsässer B, Ducho C, Brandstetter H, Hartmann RW. J. Am. Chem. Soc. 139 12696-12703 (2017)
  25. High-speed atomic force microscopy reveals strongly polarized movement of clostridial collagenase along collagen fibrils. Watanabe-Nakayama T, Itami M, Kodera N, Ando T, Konno H. Sci Rep 6 28975 (2016)
  26. Neural Crest-Derived Chondrocytes Isolation for Tissue Engineering in Regenerative Medicine. Salamone M, Rigogliuso S, Nicosia A, Tagliavia M, Campora S, Cinà P, Bruno C, Ghersi G. Cells 9 (2020)
  27. Structure-Functional Characteristics of the Svx Protein-The Virulence Factor of the Phytopathogenic Bacterium Pectobacterium atrosepticum. Tendiuk N, Konnova T, Petrova O, Osipova E, Mukhametzyanov T, Makshakova O, Gorshkov V. Int J Mol Sci 23 6914 (2022)
  28. A novel computationally engineered collagenase reduces the force required for tooth extraction in an ex-situ porcine jaw model. Ansbacher T, Tohar R, Cohen A, Cohen O, Levartovsky S, Arieli A, Matalon S, Bar DZ, Gal M, Weinberg E. J Biol Eng 17 47 (2023)
  29. Biochemical characterisation of a collagenase from Bacillus cereus strain Q1. Hoppe IJ, Brandstetter H, Schönauer E. Sci Rep 11 4187 (2021)
  30. Ca2+ -induced orientation of tandem collagen binding domains from clostridial collagenase ColG permits two opposing functions of collagen fibril formation and retardation. Caviness P, Bauer R, Tanaka K, Janowska K, Roeser JR, Harter D, Sanders J, Ruth C, Matsushita O, Sakon J. FEBS J. 285 3254-3269 (2018)
  31. Crystal structure of Grimontia hollisae collagenase provides insights into its novel substrate specificity toward collagen. Ikeuchi T, Yasumoto M, Takita T, Tanaka K, Kusubata M, Hayashida O, Hattori S, Mizutani K, Mikami B, Yasukawa K. J Biol Chem 298 102109 (2022)
  32. Discovery and Characterization of Synthesized and FDA-Approved Inhibitors of Clostridial and Bacillary Collagenases. Alhayek A, Abdelsamie AS, Schönauer E, Camberlein V, Hutterer E, Posselt G, Serwanja J, Blöchl C, Huber CG, Haupenthal J, Brandstetter H, Wessler S, Hirsch AKH. J Med Chem 65 12933-12955 (2022)
  33. Discovery of New Microbial Collagenase Inhibitors. Nitulescu G, Mihai DP, Zanfirescu A, Stan MS, Gradinaru D, Nitulescu GM. Life (Basel) 12 2114 (2022)
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  35. Induction of posterior vitreous detachment (PVD) by non-enzymatic reagents targeting vitreous collagen liquefaction as well as vitreoretinal adhesion. Santra M, Sharma M, Katoch D, Jain S, Saikia UN, Dogra MR, Luthra-Guptasarma M. Sci Rep 10 8250 (2020)
  36. MIL-100(Fe) Sub-Micrometric Capsules as a Dual Drug Delivery System. Abuçafy MP, Frem RCG, Polinario G, Pavan FR, Zhao H, Mielcarek A, Boissiere C, Serre C, Chiavacci LA. Int J Mol Sci 23 7670 (2022)
  37. Mechanistic Insight into the Fragmentation of Type I Collagen Fibers into Peptides and Amino Acids by a Vibrio Collagenase. Wang Y, Su HN, Cao HY, Liu SM, Liu SC, Zhang X, Wang P, Li CY, Zhang YZ, Zhang XY, Chen XL. Appl Environ Microbiol 88 e0167721 (2022)
  38. Phytochemical profile, antioxidant, antiproliferative, and enzyme inhibition-docking analyses of Salvia ekimiana Celep & Doğan. Karatoprak GŞ, Göger F, Çelik İ, Budak Ü, Akkol EK, Aschner M. S Afr J Bot 146 36-47 (2022)
  39. Quantitative cross-linking via engineered cysteines to study inter-domain interactions in bacterial collagenases. Serwanja J, Brandstetter H, Schönauer E. STAR Protoc 4 102519 (2023)
  40. Recombinant collagenase from Grimontia hollisae as a tissue dissociation enzyme for isolating primary cells. Tanaka K, Okitsu T, Teramura N, Iijima K, Hayashida O, Teramae H, Hattori S. Sci Rep 10 3927 (2020)
  41. Screening Collagenase Activity in Bacterial Lysate for Directed Enzyme Applications. Tohar R, Ansbacher T, Sher I, Afriat-Jurnou L, Weinberg E, Gal M. Int J Mol Sci 22 8552 (2021)
  42. Standardized Pomegranate (Pomella®) and Red Maple (Maplifa®) Extracts and Their Phenolics Protect Type I Collagen by the Inhibition of Matrix Metalloproteinases, Collagenase, and Collagen Cross-Linking. Li H, Roy T, Boateng ST, He H, Liu C, Liu W, Li D, Wu P, Seeram NP, Chamcheu JC, Ma H. Molecules 27 7919 (2022)
  43. Structure of Vibrio collagenase VhaC provides insight into the mechanism of bacterial collagenolysis. Wang Y, Wang P, Cao HY, Ding HT, Su HN, Liu SC, Liu G, Zhang X, Li CY, Peng M, Li F, Li S, Chen Y, Chen XL, Zhang YZ. Nat Commun 13 566 (2022)
  44. The bone-degrading enzyme machinery: From multi-component understanding to the treatment of residues from the meat industry. Fernandez-Lopez L, Sanchez-Carrillo S, García-Moyano A, Borchert E, Almendral D, Alonso S, Cea-Rama I, Miguez N, Larsen Ø, Werner J, Makarova KS, Plou FJ, Dahlgren TG, Sanz-Aparicio J, Hentschel U, Bjerga GEK, Ferrer M. Comput Struct Biotechnol J 19 6328-6342 (2021)