Structural and mechanistic insights into collagen degradation by a bacterial collagenolytic serine protease in the subtilisin family

Molecular Microbiology

Volumn 90, Issue 5, 2013, Pages 997-1010

  Ran, Li Yuan ^a   Su, Hai Nan ^a   Zhao, Guo Yan ^a   Gao, Xiang ^a   Zhou, Ming Yang ^a   Wang, Peng ^a   Zhao, Hui Lin ^a   Xie, Bin Bin ^a   Zhang, Xi Ying ^a   Chen, Xiu Lan ^a   Zhou, Bai Cheng ^a   Zhang, Yu Zhong ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER; COLLAGEN TYPE 1; GLYCINE; HISTIDINE; PROLINE; PROTEIN MCP 01; PROTEOGLYCAN; SERINE PROTEINASE; SUBTILISIN; TELOPEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CHEMICAL ANALYSIS; COLLAGEN DEGRADATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STRUCTURE; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HYDROLYSIS; PSEUDOALTEROMONAS;

BACTERIA (MICROORGANISMS); PSEUDOALTEROMONAS SP.;

AMINO ACID SEQUENCE; AMINO ACIDS; CATALYTIC DOMAIN; COLLAGEN TYPE I; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASES; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; PSEUDOALTEROMONAS; SUBSTRATE SPECIFICITY; SUBTILISIN;

EID: 84888388168     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12412     Document Type: Article

References (57)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., etal. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Almog, O., Gallagher, D.T., Ladner, J.E., Strausberg, S., Alexander, P., Bryan, P., and Gilliland, G.L. (2002) Structural basis of thermostability: analysis of stabilizing mutations in subtilisin BPN'. J Biol Chem 277: 27553-27558.
3. Ballinger, M.D., Tom, J., and Wells, J.A. (1995) Designing subtilisin BPN' to cleave substrates containing dibasic residues. Biochemistry 34: 13312-13319.
4. Bertini, I., Fragai, M., Luchinat, C., Melikian, M., Toccafondi, M., Lauer, J.L., and Fields, G.B. (2012) Structural basis for matrix metalloproteinase 1 catalyzed collagenolysis. J Am Chem Soc 134: 2100-2110.
5. Bode, W., Papamokos, E., Musil, D., Seemueller, U., and Fritz, H. (1986) Refined 1.2 A crystal structure of the complex formed between subtilisin Carlsberg and the inhibitor eglin c: molecular structure of eglin and its detailed interaction with subtilisin. EMBO J 5: 813-818.
6. Catara, G., Ruggiero, G., La Cara, F., Digilio, F.A., Capasso, A., and Rossi, M. (2003) A novel extracellular subtilisin-like protease from the hyperthermophile Aeropyrum pernix K1: biochemical properties, cloning, and expression. Extremophiles 7: 391-399.
7. Chen, X.L., Zhang, Y.Z., Gao, P.J., and Luan, X.W. (2003) Two different proteases produced by a deep-sea psychrotrophic bacterial strain, Pseudoaltermonas sp. SM9913. Mar Biol 143: 989-993.
8. Chen, X.L., Xie, B.B., Lu, J.T., He, H.L., and Zhang, Y.Z. (2007) A novel type of subtilase from the psychrotolerant bacterium Pseudoalteromonas sp. SM9913: catalytic and structural properties of deseasin MCP-01. Microbiology 153: 2116-2125.
9. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fields, J.L., Fields, G.B., Visse, R., and Nagase, H. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23: 3020-3030.
10. Corvo, I., Cancela, M., Cappetta, M., Pi-Denis, N., Tort, J.F., and Roche, L. (2009) The major cathepsin L secreted by the invasive juvenile Fasciola hepatica prefers proline in the S2 subsite and can cleave collagen. Mol Biochem Parasitol 167: 41-47.
11. Cowtan, K., Emsley, P., and Wilson, K.S. (2011) From crystal to structure with CCP4. Acta Crystallogr D 67: 233-234.
12. Dejica, V.M., Mort, J.S., Laverty, S., Percival, M.D., Antoniou, J., Zukor, D.J., and Poole, A.R. (2008) Cleavage of type II collagen by cathepsin K in human osteoarthritic cartilage. Am J Pathol 173: 161-169.
13. Eckhard, U., Schonauer, E., Nuss, D., and Brandstetter, H. (2011) Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Nat Struct Mol Biol 18: 1109-1114.
14. Eisen, A.Z., Henderson, K.O., Jeffrey, J.J., and Bradshaw, R.A. (1973) A collagenolytic protease from the hepatopancreas of the fiddler crab, Uca pugilator. Purification and properties. Biochemistry 12: 1814-1822.
15. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132.
16. Exposito, J.Y., Valcourt, U., Cluzel, C., and Lethias, C. (2010) The fibrillar collagen family. Int J Mol Sci 11: 407-426.
17. Fields, G.B. (2013) Interstitial collagen catabolism. J Biol Chem 288: 8785-8793.
18. Garnero, P. (1998) The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem 273: 32347-32352.
19. Gordon, M.K., and Hahn, R.A. (2010) Collagens. Cell Tissue Res 339: 247-257.
20. Huber, R., and Bode, W. (1978) Structural basis of the activation and action of trypsin. Acc Chem Res 11: 114-122.
21. Jang, H., Kim, B., Pyun, Y., and Kim, Y. (2002) A novel subtilisin-like serine protease from Thermoanaerobacter yonseiensis KB-1: its cloning, expression, and biochemical properties. Extremophiles 6: 233-243.
22. Kafienah, W., Brömme, D., Buttle, D.J., Croucher, L.J., and Hollander, A.P. (1998) Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem J 331: 727-732.
23. Kim, H.K., Ha, Y.R., Yu, H.S., Kong, H.H., and Chung, D.I. (2003) Purification and characterization of a 33kDa serine protease from Acanthamoeba lugdunensis KA/E2 isolated from a Korean keratitis patient. Korean J Parasitol 41: 189-196.
24. Kim, W.T., Kong, H.H., Ha, Y.R., Hong, Y.C., Jeong, H.J., Yu, H.S., and Chung, D.I. (2006) Comparison of specific activity and cytopathic effects of purified 33kDa serine proteinase from Acanthamoeba strains with different degree of virulence. Korean J Parasitol 44: 321-330.
25. Kulakova, L. (1999) Cold-active serine alkaline protease from the psychrotrophic bacterium Shewanella strain ac10: gene cloning and enzyme purification and characterization. Appl Environ Microbiol 65: 611-617.
26. Kurata, A., Uchimura, K., Kobayashi, T., and Horikoshi, K. (2010) Collagenolytic subtilisin-like protease from the deep-sea bacterium Alkalimonas collagenimarina AC40T. Appl Microbiol Biotechnol 86: 589-598.
27. Laskowski, R.A., Rullmann, J.A.C., MacArthur, M.W., Kaptein, R., and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
28. Li, Z., Yasuda, Y., Li, W., Bogyo, M., Katz, N., Gordon, R.E., and Brömme, D. (2004) Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J Biol Chem 279: 5470-5479.
29. McCawley, L.J., and Matrisian, L.M. (2001) Matrix metalloproteinases: they're not just for matrix anymore!. Curr Opin Cell Biol 13: 534-540.
30. McPhalen, C.A., and James, M.N. (1988) Structural comparison of two serine proteinase-protein inhibitor complexes: eglin-c-subtilisin Carlsberg and CI-2-subtilisin Novo. Biochemistry 27: 6582-6598.
31. Manka, S.W., Carafoli, F., Visse, R., Bihan, D., Raynal, N., Farndale, R.W., etal. (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci USA 109: 12461-12466.
32. Nagase, H., and Visse, R. (2011) Triple helicase activity and the structural basis of collagenolysis. In Biology of Extracellular Matrix. Parks, W.C., and Mecham, R.P. (eds). Heidelberg: Springer, pp. 95-122.
33. O'Farrell, T.J., Guo, R., Hasegawa, H., and Pourmotabbed, T. (2006) Matrix metalloproteinase-1 takes advantage of the induced fit mechanism to cleave the triple-helical type I collagen molecule. Biochemistry 45: 15411-15418.
34. Okamoto, M., Yonejima, Y., Tsujimoto, Y., Suzuki, Y., and Watanabe, K. (2001) A thermostable collagenolytic protease with a very large molecular mass produced by thermophilic Bacillus sp. strain MO-1. Appl Microbiol Biotechnol 57: 103-108.
35. Orgel, J.P., Irving, T.C., Miller, A., and Wess, T.J. (2006) Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci USA 103: 9001-9005.
36. Page-McCaw, A., Ewald, A.J., and Werb, Z. (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8: 221-233.
37. Panwar, P., Du, X., Sharma, V., Lamour, G., Castro, M., Li, H., and Brömme, D. (2013) Effects of cysteine proteases on the structural and mechanical properties of collagen fibers. J Biol Chem 288: 5940-5950.
38. Parks, W.C., and Mecham, R.P. (eds) (1998) Matrix Metalloproteinases. San Diego, CA: Academic Press.
39. Perez-Tamayo, R. (1978) Pathology of collagen degradation. Am J Pathol 92: 508-566.
40. Perona, J.J., and Craik, C.S. (1995) Structural basis of substrate specificity in the serine proteases. Protein Sci 4: 337-360.
41. Perona, J.J., Tsu, C.A., Craik, C.S., and Fletterick, R.J. (1997) Crystal structure of an ecotin-collagenase complex suggests a model for recognition and cleavage of the collagen triple helix. Biochemistry 36: 5381-5392.
42. Rawlings, N.D., Barrett, A.J., and Bateman, A. (2010) MEROPS: the peptidase database. Nucleic Acids Res 38: D227-D233.
43. Ricard-Blum, S. (2011) The collagen family. Cold Spring Harb Perspect Biol 3: a004978.
44. Robinson, M.W., Corvo, I., Jones, P.M., George, A.M., Padula, M.P., To, J., and Dalton, J.P. (2011) Collagenolytic activities of the major secreted cathepsin L peptidases involved in the virulence of the helminth pathogen, Fasciola hepatica. PLoS Negl Trop Dis 5: e1012.
45. Ruan, B., London, V., Fisher, K.E., Gallagher, D.T., and Bryan, P.N. (2008) Engineering substrate preference in subtilisin: structural and kinetic analysis of a specificity mutant. Biochemistry 47: 6628-6636.
46. Sarkar, S.K., Marmer, B., Goldberg, G., and Neuman, K.C. (2012) Single molecule tracking of collagenase on native type I collagen fibrils reveals degradation mechanism. Curr Biol 22: 1047-1056.
47. Takeuchi, H., Shibano, Y., Morihara, K., Fukushima, J., Inami, S., Keil, B., and Okuda, K. (1992) Structural gene and complete amino acid sequence of Vibrio alginolyticus collagenase. Biochem J 281: 703-708.
48. Tam, E.M., Moore, T.R., Butler, G.S., and Overall, C.M. (2004) 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 279: 43336-43344.
49. Toogood, H.S., Smith, C.A., Baker, E.N., and Daniel, R.M. (2000) Purification and characterization of Ak.1 protease, a thermostable subtilisin with a disulphide bond in the substrate-binding cleft. Biochem J 350: 321-328.
50. Tsu, C.A., Perona, J.J., Fletterick, R.J., and Craik, C.S. (1997) Structural basis for the broad substrate specificity of fiddler crab collagenolytic serine protease 1. Biochemistry 36: 5393-5401.
51. Visse, R., and Nagase, H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92: 827-839.
52. Wan, M.Y., Wang, H.Y., Zhang, Y.Z., and Feng, H. (2009) Substrate specificity and thermostability of the dehairing alkaline protease from Bacillus pumilus. Appl Biochem Biotechnol 159: 394-403.
53. Wang, Y.K., Zhao, G.Y., Li, Y., Chen, X.L., Xie, B.B., Su, H.N., and 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 collagen triple helix. J Biol Chem 285: 14285-14291.
54. Windhorst, S., Frank, E., Georgieva, D.N., Genov, N., Buck, F., Borowski, P., and Weber, W. (2002) The major extracellular protease of the nosocomial pathogen Stenotrophomonas maltophilia: characterization of the protein and molecular clonning of the gene. J Biol Chem 277: 11042-11049.
55. Worthington Biochemical Corp. (1972) Worthington Enzyme Manual. Freehold, NJ: Worthington Biochemical Corp., pp. 43-45.
56. Yoshida, E., and Noda, H. (1965) Isolation and characterization of collagenases I and II from Clostridium histolyticum. Biochim Biophys Acta 105: 562-574.
57. Zhao, G.Y., Chen, X.L., Zhao, H.L., Xie, B.B., Zhou, B.C., and 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 particulate organic nitrogen degradation. J Biol Chem 283: 36100-36107.