Proteomic protease specificity profiling of clostridial collagenases reveals their intrinsic nature as dedicated degraders of collagen

Journal of Proteomics

Volumn 100, Issue , 2014, Pages 102-114

  Eckhard, Ulrich ^a,b   Huesgen, Pitter F ^a   Brandstetter, Hans ^b   Overall, Christopher M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF SALZBURG   (Austria)

Author keywords

Clostridia; Collagenase; Mass spectrometry; MMPs; PICS

Indexed keywords

COLLAGEN; COLLAGENASE; GLYCINE; MATRIX METALLOPROTEINASE; PROLINE; PROTEINASE; PROTEOME;

AMINO ACID SEQUENCE; ARTICLE; CLOSTRIDIUM; CLOSTRIDIUM HISTOLYTICUM; CLOSTRIDIUM TETANI; COLLAGEN DEGRADATION; CRYSTAL STRUCTURE; ENZYMATIC ASSAY; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SPECIFICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; MASS SPECTROMETRY; NONHUMAN; PEPTIDE LIBRARY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; TANDEM MASS SPECTROMETRY; ENZYMOLOGY; HUMAN; METABOLISM; MOLECULAR CLONING; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

CLOSTRIDIA; CLOSTRIDIUM HISTOLYTICUM; CLOSTRIDIUM TETANI;

CLONING, MOLECULAR; CLOSTRIDIUM; COLLAGEN; COLLAGENASES; HUMANS; HYDROLYSIS; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; SUBSTRATE SPECIFICITY;

EID: 84897038767     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.10.004     Document Type: Article

References (92)

1. Traub W., Yonath A., Segal D.M. On the molecular structure of collagen. Nature 1969, 221:914-917.
2. Hulmes D.J., Miller A. Quasi-hexagonal molecular packing in collagen fibrils. Nature 1979, 282:878-880.
3. Hulmes D.J. The collagen superfamily-diverse structures and assemblies. Essays Biochem 1992, 27:49-67.
4. Perumal S., Antipova O., Orgel J.P.R.O. Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proc Natl Acad Sci U S A 2008, 105:2824-2829.
5. Shoulders M.D., Raines R.T. Collagen structure and stability. Annu Rev Biochem 2009, 78:929-958.
6. Ramshaw J.A., Shah N.K., Brodsky B. Gly-X-Y tripeptide frequencies in collagen: a context for host-guest triple-helical peptides. J Struct Biol 1998, 122:86-91.
7. Orgel J.P.R.O., Irving T.C., Miller A., Wess T.J. Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci U S A 2006, 103:9001-9005.
8. Wagenaar-Miller R.A., Engelholm L.H., Gavard J., Yamada S.S., Gutkind J.S., Behrendt N., et al. Complementary roles of intracellular and pericellular collagen degradation pathways in vivo. Mol Cell Biol 2007, 27:6309-6322.
9. Verzijl N., DeGroot J., Thorpe S.R., Bank R.A., Shaw J.N., Lyons T.J., et al. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 2000, 275:39027-39031.
10. Fields G.B. Interstitial collagen catabolism. J Biol Chem 2013, 288:8785-8793.
11. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002, 22:51-86.
12. Balbín M., Fueyo A., Knäuper V., Pendás A.M., López J.M., Jiménez M.G., et al. Collagenase 2 (MMP-8) expression in murine tissue-remodeling processes. Analysis of its potential role in postpartum involution of the uterus. J Biol Chem 1998, 273:23959-23968.
13. Manka S.W., Carafoli F., Visse R., Bihan D., Raynal N., Farndale R.W., et al. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci U S A 2012, 109:12461-12466.
14. Nagase H., Fushimi K. Elucidating the function of non catalytic domains of collagenases and aggrecanases. Connect Tissue Res 2008, 49:169-174.
15. Tam E.M., Moore T.R., Butler G.S., Overall C.M. Characterization of the distinct collagen binding, helicase and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): the differential roles of the MMP hemopexin c domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities. J Biol Chem 2004, 279:43336-43344.
16. Pelman G.R., Morrison C.J., Overall C.M. Pivotal molecular determinants of peptidic and collagen triple helicase activities reside in the S3' subsite of matrix metalloproteinase 8 (MMP-8): the role of hydrogen bonding potential of ASN188 and TYR189 and the connecting cis bond. J Biol Chem 2005, 280:2370-2377.
17. Garnero P., Borel O., Byrjalsen I., Ferreras M., Drake F.H., McQueney M.S., et al. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem 1998, 273:32347-32352.
18. Kafienah W., Brömme D., Buttle D.J., Croucher L.J., Hollander A.P. Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem J 1998, 331(Pt 3):727-732.
19. Hatheway C.L. Toxigenic clostridia. Clin Microbiol Rev 1990, 3:66-98.
20. Wells C.L., Wilkins T.D. Clostridia: sporeforming anaerobic bacilli. Med Microbiol 1996, University of Texas Medical Branch at Galveston, Galveston (TX). S. Baron (Ed.).
21. Wessel D., Flügge U.I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984, 138:141-143.
22. Bond M.D., Van Wart H.E. Purification and separation of individual collagenases of Clostridium histolyticum using red dye ligand chromatography. Biochemistry (Mosc) 1984, 23:3077-3085.
23. Toyoshima T., Matsushita O., Minami J., Nishi N., Okabe A., Itano T. Collagen-binding domain of a Clostridium histolyticum collagenase exhibits a broad substrate spectrum both in vitro and in vivo. Connect Tissue Res 2001, 42:281-290.
24. French M.F., Bhown A., Van Wart H.E. Identification of Clostridium histolyticum collagenase hyperreactive sites in type I, II, and III collagens: lack of correlation with local triple helical stability. J Protein Chem 1992, 11:83-97.
25. Mookhtiar K.A., Van Wart H.E. Clostridium histolyticum collagenases: a new look at some old enzymes. Matrix Suppl 1992, 1:116-126.
26. Brüggemann H., Gottschalk G. Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani. Anaerobe 2004, 10:53-68.
27. Mookhtiar K.A., Steinbrink D.R., Van Wart H.E. Mode of hydrolysis of collagen-like peptides by class I and class II Clostridium histolyticum collagenases: evidence for both endopeptidase and tripeptidylcarboxypeptidase activities. Biochemistry (Mosc) 1985, 24:6527-6533.
28. Kaplan F.T.D. Collagenase clostridium histolyticum injection for the treatment of Dupuytren's contracture. Drugs Today (Barc) 2011, 47:653-667.
29. Desai S.S., Hentz V.R. The treatment of Dupuytren disease. J Hand Surg 2011, 36:936-942.
30. Shi L., Carson D. Collagenase Santyl ointment: a selective agent for wound debridement. J Wound Ostomy Continence Nurs 2009, 36:S12-S16.
31. Ramundo J., Gray M. Collagenase for enzymatic debridement: a systematic review. J Wound Ostomy Continence Nurs 2009, 36:S4-S11.
32. Brandhorst H., Brandhorst D., Hesse F., Ambrosius D., Brendel M., Kawakami Y., et al. Successful human islet isolation utilizing recombinant collagenase. Diabetes 2003, 52:1143-1146.
33. Balamurugan A.N., Breite A.G., Anazawa T., Loganathan G., Wilhelm J.J., Papas K.K., et al. Successful human islet isolation and transplantation indicating the importance of class 1 collagenase and collagen degradation activity assay. Transplantation 2010, 89:954-961.
34. Matsushita O., Okabe A. Clostridial hydrolytic enzymes degrading extracellular components. Toxicon 2001, 39:1769-1780.
35. Ducka P., Eckhard U., Schönauer E., Kofler S., Gottschalk G., Brandstetter H., et al. A universal strategy for high-yield production of soluble and functional clostridial collagenases in E. coli. Appl Microbiol Biotechnol 2009, 83:1055-1065.
36. Eckhard U., Schönauer E., Nüss D., Brandstetter H. Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Nat Struct Mol Biol 2011, 18:1109-1114.
37. Eckhard U., Brandstetter H. Polycystic kidney disease-like domains of clostridial collagenases and their role in collagen recruitment. Biol Chem 2011, 392:1039-1045.
38. Wang Y.K., Zhao G.Y., Li Y., Chen X.L., Xie B.B., Su H.N., et al. 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 collagen triple helix. J Biol Chem 2010, 285:14285-14291.
39. Bond M.D., Van Wart H.E. Characterization of the individual collagenases from Clostridium histolyticum. Biochemistry (Mosc) 1984, 23:3085-3091.
40. Eckhard U., Schönauer E., Ducka P., Briza P., Nüss D., Brandstetter H. Biochemical characterization of the catalytic domains of three different clostridial collagenases. Biol Chem 2009, 390:11-18.
41. Eckhard U., Schönauer E., Brandstetter H. Structural basis for activity regulation and substrate preference of clostridial collagenases G, H, and T. J Biol Chem 2013, 288:20184-20194.
42. Gomis-Rüth F.X., Stöcker W., Huber R., Zwilling R., Bode W. Refined 1.8 A X-ray crystal structure of astacin, a zinc-endopeptidase from the crayfish Astacus astacus L. Structure determination, refinement, molecular structure and comparison with thermolysin. J Mol Biol 1993, 229:945-968.
43. Schechter I., Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 1967, 27:157-162.
44. Auf dem Keller U., Schilling O. Proteomic techniques and activity-based probes for the system-wide study of proteolysis. Biochimie 2010, 92:1705-1714.
45. Schilling O., Overall C.M. Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat Biotechnol 2008, 26:685-694.
46. Wilkins M.R., Gasteiger E., Bairoch A., Sanchez J.C., Williams K.L., Appel R.D., et al. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 1999, 112:531-552.
47. Van Wart H.E., Steinbrink D.R. A continuous spectrophotometric assay for Clostridium histolyticum collagenase. Anal Biochem 1981, 113:356-365.
48. Schilling O., Huesgen P.F., Barré O., Auf dem Keller U., Overall C.M. Characterization of the prime and non-prime active site specificities of proteases by proteome-derived peptide libraries and tandem mass spectrometry. Nat Protoc 2011, 6:111-120.
49. Olsen J.V., de Godoy L.M.F., Li G., Macek B., Mortensen P., Pesch R., et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005, 4:2010-2021.
50. Kessner D., Chambers M., Burke R., Agus D., Mallick P. ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 2008, 24:2534-2536.
51. Craig R., Beavis R.C. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 2004, 20:1466-1467.
52. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
53. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
54. Shteynberg D., Deutsch E.W., Lam H., Eng J.K., Sun Z., Tasman N., et al. iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates. Mol Cell Proteomics 2011, 10. [M111.007690].
55. Keller A., Eng J., Zhang N., Li X., Aebersold R. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol 2005, 1. [2005.0017].
56. Schilling O., Auf dem Keller U., Overall C.M. Factor Xa subsite mapping by proteome-derived peptide libraries improved using WebPICS, a resource for proteomic identification of cleavage sites. Biol Chem 2011, 392:1031-1037.
57. Colaert N., Helsens K., Martens L., Vandekerckhove J., Gevaert K. Improved visualization of protein consensus sequences by iceLogo. Nat Methods 2009, 6:786-787.
58. Spurlino J.C., Smallwood A.M., Carlton D.D., Banks T.M., Vavra K.J., Johnson J.S., et al. 1.56A structure of mature truncated human fibroblast collagenase. Proteins 1994, 19:98-109.
59. London N., Raveh B., Cohen E., Fathi G., Schueler-Furman O. Rosetta FlexPepDock web server-high resolution modeling of peptide-protein interactions. Nucleic Acids Res 2011, 39:W249-W253.
60. Raveh B., London N., Schueler-Furman O. Sub-angstrom modeling of complexes between flexible peptides and globular proteins. Proteins 2010, 78:2029-2040.
61. DeLano W.L. The case for open-source software in drug discovery. Drug Discov Today 2005, 10:213-217.
62. Hu Y., Webb E., Singh J., Morgan B.A., Gainor J.A., Gordon T.D., et al. Rapid determination of substrate specificity of Clostridium histolyticum beta-collagenase using an immobilized peptide library. J Biol Chem 2002, 277:8366-8371.
63. Dufour A., Overall C.M. Missing the target: matrix metalloproteinase antitargets in inflammation and cancer. Trends Pharmacol Sci 2013, 34:233-242.
64. Scozzafava A., Ilies M.A., Manole G., Supuran C.T. 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 2000, 11:69-79.
65. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006, 69:562-573.
66. Bauer E.A., Eisen A.Z., Jeffrey J.J. Immunologic relationship of a purified human skin collagenase to other human and animal collagenases. Biochim Biophys Acta 1970, 206:152-160.
67. Goldberg G.I., Wilhelm S.M., Kronberger A., Bauer E.A., Grant G.A., Eisen A.Z. Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J Biol Chem 1986, 261:6600-6605.
68. Pardo A., Selman M. MMP-1: the elder of the family. Int J Biochem Cell Biol 2005, 37:283-288.
69. Gomis-Rüth F.X., Botelho T.O., Bode W. A standard orientation for metallopeptidases. Biochim Biophys Acta 1824, 2012:157-163.
70. Hooper N.M. Families of zinc metalloproteases. FEBS Lett 1994, 354:1-6.
71. Knight C.G., Willenbrock F., Murphy G. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett 1992, 296:263-266.
72. Maskos K. Crystal structures of MMPs in complex with physiological and pharmacological inhibitors. Biochimie 2005, 87:249-263.
73. Ohbayashi N., Matsumoto T., Shima H., Goto M., Watanabe K., Yamano A., et al. Solution structure of clostridial collagenase H and its calcium-dependent global conformation change. Biophys J 2013, 104:1538-1545.
74. Ohbayashi N., Yamagata N., Goto M., Watanabe K., Yamagata Y., Murayama K. Enhancement of the structural stability of full-length clostridial collagenase by calcium ions. Appl Environ Microbiol 2012, 78:5839-5844.
75. Bauer R., Wilson J.J., Philominathan S.T.L., Davis D., Matsushita O., Sakon J. Structural comparison of ColH and ColG collagen-binding domains from Clostridium histolyticum. J Bacteriol 2013, 195:318-327.
76. Philominathan S.T.L., Koide T., Matsushita O., Sakon J. Bacterial collagen-binding domain targets undertwisted regions of collagen. Protein Sci 2012, 21:1554-1565.
77. Wilson J.J., Matsushita O., Okabe A., Sakon J. A bacterial collagen-binding domain with novel calcium-binding motif controls domain orientation. EMBO J 2003, 22:1743-1752.
78. Eckhard U., Nüss D., Ducka P., Schönauer E., Brandstetter H. Crystallization and preliminary X-ray characterization of the catalytic domain of collagenase G from Clostridium histolyticum. Acta Crystallogr Sect F Struct Biol Cryst Commun 2008, 64:419-421.
79. Lu K.G., Stultz C.M. Insight into the degradation of type-I collagen fibrils by MMP-8. J Mol Biol 2013, 425:1815-1825.
80. Chung L., Dinakarpandian D., Yoshida N., Lauer-Fields J.L., Fields G.B., Visse R., et al. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 2004, 23:3020-3030.
81. Welgus H.G., Jeffrey J.J., Eisen A.Z. The collagen substrate specificity of human skin fibroblast collagenase. J Biol Chem 1981, 256:9511-9515.
82. Hasty K.A., Jeffrey J.J., Hibbs M.S., Welgus H.G. The collagen substrate specificity of human neutrophil collagenase. J Biol Chem 1987, 262:10048-10052.
83. Ramachandran G.N., Lakshminarayanan A.V., Balasubramanian R., Tegoni G. Studies on the conformation of amino acids. XII. Energy calculations on prolyl residue. Biochim Biophys Acta 1970, 221:165-181.
84. MacArthur M.W., Thornton J.M. Influence of proline residues on protein conformation. J Mol Biol 1991, 218:397-412.
85. Schimmel P.R., Flory P.J. Conformational energies and configurational statistics of copolypeptides containing L-proline. J Mol Biol 1968, 34:105-120.
86. Butler G.S., Overall C.M. Updated biological roles for matrix metalloproteinases and new "intracellular" substrates revealed by degradomics. Biochemistry (Mosc) 2009, 48:10830-10845.
87. Cox T.R., Erler J.T. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 2011, 4:165-178.
88. Lu P., Weaver V.M., Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012, 196:395-406.
89. Shi F., Harman J., Fujiwara K., Sottile J. Collagen I matrix turnover is regulated by fibronectin polymerization. Am J Physiol Cell Physiol 2010, 298:C1265-C1275.
90. Gilpin D., Coleman S., Hall S., Houston A., Karrasch J., Jones N. Injectable collagenase Clostridium histolyticum: a new nonsurgical treatment for Dupuytren's disease. J Hand Surg 2010, 35:2027-2038.e1.
91. Becker-Pauly C., Barré O., Schilling O., Auf dem Keller U., Ohler A., Broder C., et al. Proteomic analyses reveal an acidic prime side specificity for the astacin metalloprotease family reflected by physiological substrates. Mol Cell Proteomics 2011, 10. [M111.009233].
92. Biniossek M.L., Nägler D.K., Becker-Pauly C., Schilling O. Proteomic identification of protease cleavage sites characterizes prime and non-prime specificity of cysteine cathepsins B, L, and S. J Proteome Res 2011, 10:5363-5373.