Matrix metalloproteinase-1 cleavage site recognition and binding in full-length human type III collagen

Matrix Biology

Volumn 28, Issue 6, 2009, Pages 373-379

  Williams, Kim E ^a   Olsen, David R ^a  

^a FIBROGEN INC   (United States)

Author keywords

Collagenase; Matrix metalloproteinase; MMP 1; Recombinant collagen

Indexed keywords

COLLAGEN TYPE 3; COLLAGENASE 3; ELASTASE; INTERSTITIAL COLLAGENASE; NEUTROPHIL COLLAGENASE; PROLINE; TRYPSIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION;

COLLAGEN TYPE III; HUMANS; MATRIX METALLOPROTEINASE 1; PROTEIN BINDING; PROTEIN ISOFORMS; RECOMBINANT PROTEINS;

EID: 69949190843     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2009.04.009     Document Type: Article

References (45)

1. Baez J., Olsen D., and Polarek J. Recombinant microbial systems for the production of human collagen gelatin. Appl. Microbiol. Biotechnol. (2005) 245-252
2. Birkedal-Hansen H., Taylor R.E., Bhown A.S., Katz J., Lin H.Y., and Wells B.R. Cleavage of bovine skin type III collagen by proteolytic enzymes. Relative resistance of the fibrillar form. J. Biol. Chem. 260 (1985) 16411-16417
3. Bode W. A helping hand for collagenases: the haemopexin-like domain. Structure 3 (1995) 527-530
4. Brown R.A., Hukins D.W., Weiss J.B., and Twose T.M. Do mammalian collagenases and DNA restriction endonucleases share a similar mechanism for cleavage site recognition?. Biochem. Biophys. Res. Commun. 74 (1977) 1102-1108
5. Chung L., Dinakarpandian D., Yoshida N., Lauer-Fields J.L., Fields G.B., Visse R., and Nagase H. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 23 (2004) 3020-3030
6. Fan P., Li M.H., Brodsky B., and Baum J. Backbone dynamics of (Pro-Hyp-Gly)10 and a designed collagen-like triple-helical peptide by 15 N NMR relaxation and hydrogen-exchange measurements. Biochemistry 32 (1993) 13299-13309
7. Fields G.B. A model for interstitial collagen catabolism by mammalian collagenases. J. Theor. Biol. 153 (1991) 585-602
8. Fields G.B., and Van Wart H.E. Unique features of the tissue collagenase cleavage site in interstitial collagens. Matrix, Suppl. 1 (1992) 68-70
9. Fields G.B., Van Wart H.E., and Birkedal-Hansen H. Sequence specificity of human skin fibroblast collagenase. Evidence for the role of collagen structure in determining the collagenase cleavage site. J. Biol. Chem. 262 (1987) 6221-6226
10. Fiori S., Sacca B., and Moroder L. Structural properties of a collagenous heterotrimer that mimics the collagenase cleavage site of collagen type I. J. Mol. Biol. 319 (2002) 1235-1242
11. Hasty K.A., Wu H., Byrne M., Goldring M.B., Seyer J.M., Jaenisch R., Krane S.M., and Mainardi C.L. Susceptibility of type I collagen containing mutated alpha 1(1) chains to cleavage by human neutrophil collagenase. Matrix 13 (1993) 181-186
12. Highberger J.H., Corbett C., and Gross J. Isolation and characterization of a peptide containing the site of cleavage of the chick skin collagen alpha 1[I] chain by animal collagenases. Biochem. Biophys. Res. Commun. 89 (1979) 202-208
13. Issa R., Zhou X., Trim N., Millward-Sadler H., Krane S., Benyon C., and Iredale J. Mutation in collagen-I that confers resistance to the action of collagenase results in failure of recovery from CCl4-induced liver fibrosis, persistence of activated hepatic stellate cells, and diminished hepatocyte regeneration. FASEB J. 17 (2003) 47-49
14. Jaenisch R., Harbers K., Schnieke A., Lohler J., Chumakov I., Jahner D., Grotkopp D., and Hoffmann E. Germline integration of moloney murine leukemia virus at the Mov13 locus leads to recessive lethal mutation and early embryonic death. Cell 32 (1983) 209-216
15. Kramer R.Z., Bella J., Brodsky B., and Berman H.M. The crystal and molecular structure of a collagen-like peptide with a biologically relevant sequence. J. Mol. Biol. 311 (2001) 131-147
16. Krane S.M., and Jaenisch R. Site-directed mutagenesis of type I collagen: effect on susceptibility to collagenase. Matrix, Suppl. 1 (1992) 64-67
17. Lauer-Fields J.L., Kele P., Sui G., Nagase H., Leblanc R.M., and Fields G.B. Analysis of matrix metalloproteinase triple-helical peptidase activity with substrates incorporating fluorogenic l- or d-amino acids. Anal. Biochem. 321 (2003) 105-115
18. Li F., Moake J.L., and McIntire L.V. Characterization of von Willebrand factor interaction with collagens in real time using surface plasmon resonance. Ann. Biomed. Eng. 30 (2002) 1107-1116
19. Liu X., Wu H., Byrne M., Jeffrey J., Krane S., and Jaenisch R. A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J. Cell Biol. 130 (1995) 227-237
20. Lohler J., Timpl R., and Jaenisch R. Embryonic lethal mutation in mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death. Cell 38 (1984) 597-607
21. Mainardi C.L., Hasty D.L., Seyer J.M., and Kang A.H. Specific cleavage of human type III collagen by human polymorphonuclear leukocyte elastase. J. Biol. Chem. 255 (1980) 12006-12010
22. Miller E.J., Harris Jr. E.D., Chung E., Finch Jr. J.E., McCroskery P.A., and Butler W.T. Cleavage of Type II and III collagens with mammalian collagenase: site of cleavage and primary structure at the NH2-terminal portion of the smaller fragment released from both collagens. Biochemistry 15 (1976) 787-792
23. Minond D., Lauer-Fields J.L., Nagase H., and Fields G.B. Matrix metalloproteinase triple-helical peptidase activities are differentially regulated by substrate stability. Biochemistry 43 (2004) 11474-11481
24. 1 subsite identity on matrix metalloproteinase triple-helical peptidase activity and collagen specificity. J. Biol. Chem. 281 (2006) 38302-38313
25. Myllyharju J., Nokelainen M., Vuorela A., and Kivirikko K.I. Expression of recombinant human type I-III collagens in the yeast Pichia pastoris. Biochem. Soc. Trans. 28 (2000) 353-357
26. Nagase H., and Fields G.B. Human matrix metalloproteinase specificity studies using collagen sequence-based synthetic peptides. Biopolymers 40 (1996) 399-416
27. Natsume T., Koide T., Yokota S., Hirayoshi K., and Nagata K. Interactions between collagen-binding stress protein HSP47 and collagen. Analysis of kinetic parameters by surface plasmon resonance biosensor. J. Biol. Chem. 269 (1994) 31224-31228
28. Nimni M.E. Collagen: structure, function, and metabolism in normal and fibrotic tissues. Semin. Arthritis Rheum. 13 (1983) 1-86
29. Olsen D., Leigh S., Chang R., McMullin H., Ong W., Tai E., Chisholm G., Birk D., Berg R., Hitzeman R., and Toman P. Production of human type I collagen in yeast reveals unexpected new insights into the molecular assembly of collagen trimers. J. Biol. Chem. 276 (2001) 24038-24043
30. Ottl J., Gabriel D., Murphy G., Knauper V., Tominaga Y., Nagase H., Kroger M., Tschesche H., Bode W., and Moroder L. Recognition and catabolism of synthetic heterotrimeric collagen peptides by matrix metalloproteinases. Chem. Biol. 7 (2000) 119-132
31. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22 (2002) 51-86
32. Pilcher B.K., Dumin J.A., Sudbeck B.D., Krane S.M., Welgus H.G., and Parks W.C. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J. Cell Biol. 137 (1997) 1445-1457
33. Qian J., Xie P., Dou S.X., and Wang P.Y. A model for biased diffusion of collagenase along collagen fibrils. J. Theor. Biol. 243 (2006) 322-327
34. Ricard-Blum S., Bernocco S., Font B., Moali C., Eichenberger D., Farjanel J., Burchardt E.R., van der R.M., Kessler E., and Hulmes D.J. Interaction properties of the procollagen C-proteinase enhancer protein shed light on the mechanism of stimulation of BMP-1. J. Biol. Chem. 277 (2002) 33864-33869
35. Saffarian S., Collier I.E., Marmer B.L., Elson E.L., and Goldberg G. Interstitial collagenase is a Brownian ratchet driven by proteolysis of collagen. Science 306 (2004) 108-111
36. Saffarian S., Qian H., Collier I., Elson E., and Goldberg G. Powering a burnt bridges Brownian ratchet: a model for an extracellular motor driven by proteolysis of collagen. Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys. 73 (2006) 041909
37. Schnieke A., Harbers K., and Jaenisch R. Embryonic lethal mutation in mice induced by retrovirus insertion into the alpha 1(I) collagen gene. Nature 304 (1983) 315-320
38. Stultz C.M. Localized unfolding of collagen explains collagenase cleavage near imino-poor sites. J. Mol. Biol. 319 (2002) 997-1003
39. Sun H.B., Smith Jr. G.N., Hasty K.A., and Yokota H. Atomic force microscopy-based detection of binding and cleavage site of matrix metalloproteinase on individual type II collagen helices. Anal. Biochem. 283 (2000) 153-158
40. Tam E.M., Moore T.R., Butler G.S., and 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. 279 (2004) 43336-43344
41. Visse R., and Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92 (2003) 827-839
42. Vuorela A., Myllyharju J., Nissi R., Pihlajaniemi T., and Kivirikko K.I. Assembly of human prolyl 4-hydroxylase and type III collagen in the yeast Pichia pastoris: formation of a stable enzyme tetramer requires coexpression with collagen and assembly of a stable collagen requires coexpression with prolyl 4-hydroxylase. EMBO J. 16 (1997) 6702-6712
43. Welgus H.G., Burgeson R.E., Wootton J.A., Minor R.R., Fliszar C., and Jeffrey J.J. Degradation of monomeric and fibrillar type III collagens by human skin collagenase. Kinetic constants using different animal substrates. J. Biol. Chem. 260 (1985) 1052-1059
44. Welgus H.G., Jeffrey J.J., and Eisen A.Z. The collagen substrate specificity of human skin fibroblast collagenase. J. Biol. Chem. 256 (1981) 9511-9515
45. Wu H., Byrne M.H., Stacey A., Goldring M.B., Birkhead J.R., Jaenisch R., and Krane S.M. Generation of collagenase-resistant collagen by site-directed mutagenesis of murine pro alpha 1(I) collagen gene. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 5888-5892