Molecular mechanism of force induced stabilization of collagen against enzymatic breakdown

Biomaterials

Volumn 33, Issue 15, 2012, Pages 3852-3859

  Chang, Shu Wei ^a   Flynn, Brendan P ^b   Ruberti, Jeffrey W ^b   Buehler, Markus J ^a  

^a Massachusetts Institute of Technology   (United States)

^b Northeastern University   (United States)

Author keywords

Collagen; Collagen degradation; Collagenolysis; Local unfolding; Molecular mechanics; Protein structure

Indexed keywords

APPLIED FORCES; CANCER INVASION; CLEAVAGE RATES; CLEAVAGE SITES; COLLAGENOLYSIS; COLLAGENOUS TISSUES; DEGRADATION RATE; EQUILIBRIUM STATE; HETEROTRIMERS; HOMOTRIMERS; LOCAL UNFOLDING; MATRIX METALLOPROTEINASES; MECHANICAL FORCE; MECHANICAL LOADING; MOLECULAR MECHANISM; PATHOLOGICAL PROCESS; PROTEIN STRUCTURE; TISSUE REMODELING; TRIPLE HELICAL STRUCTURES; TYPE I COLLAGEN; WOUND HEALING;

DEGRADATION; MECHANICAL ENGINEERING; MOLECULAR MECHANICS; TISSUE;

COLLAGEN;

COLLAGEN; COLLAGEN TYPE 1; HETERODIMER;

ARTICLE; FORCE; HYDROLYSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN UNFOLDING;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; COLLAGEN; COLLAGENASES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STRESS, MECHANICAL;

EID: 84862813497     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.02.001     Document Type: Article

References (44)

1. Fratzl P. Collagen: structure and mechanics 2008, Springer.
2. Buehler M.J., Yung Y.C. Deformation and failure of protein materials in physiologically extreme conditions and disease. Nat Mater 2009, 8:175-188.
3. Nagase H., Visse R. Matrix metalloproteinases and tissue inhibitors of metalloproteinases:structure, function, and biochemistry. Circ Res 2003, 92:827-839.
4. Baragi V.M., Qiu L., GunjaSmith Z., Woessner J.F., Lesch C.A., Guglietta A. Role of metalloproteinases in the development and healing of acetic acid-induced gastric ulcer in rats. Scand J Gastroenterol 1997, 32:419-426.
5. Helary C., Ovtracht L., Coulomb B., Godeau G., Giraud-Guille M.M. Dense fibrillar collagen matrices: a model to study myofibroblast behaviour during wound healing. Biomaterials 2006, 27:4443-4452.
6. Barnes M.J., Farndale R.W. Collagens and atherosclerosis. Exp Gerontol 1999, 34:513-525.
7. Bode M.K., Mosorin M., Satta J., Risteli L., Juvonen T., Risteli J. Complete processing of type III collagen in atherosclerotic plaques. Arterioscler Thromb Vasc Biol 1999, 19:1506-1511.
8. McDonnell S., Morgan M., Lynch C. Role of matrix metalloproteinases in normal and disease processes. Biochem Soc Trans 1999, 27:734-740.
9. Riley G.P., Harrall R.L., Watson P.G., Cawston T.E., Hazleman B.L. Collagenase (MMP-1) and TIMP-1 in destructive corneal disease associated with rheumatoid arthritis. Eye 1995, 9:703-718.
10. Stickens D., Behonick D.J., Ortega N., Heyer B., Hartenstein B., Yu Y., et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004, 131:5883-5895.
11. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006, 69:562-573.
12. Xiao J., Addabbo R.M., Lauer J.L., Fields G.B., Baum J. Local conformation and dynamics of isoleucine in the collagenase cleavage site provide a recognition signal for matrix metalloproteinases. J Biol Chem 2010, 285:34181-34190.
13. Jimenez S.A., Bashey R.I., Benditt M., Yankowski R. Identification of collagen alpha1(I) trimer in embryonic chick tendons and calvaria. Biochem Biophys Res Commun 1977, 78:1354-1361.
14. Ehrlich H.P., Brown H., White B.S. Evidence for type V and I trimer collagens in Dupuytren's Contracture palmar fascia. Biochem Med 1982, 28:273-284.
15. Makareeva E., Han S., Vera J.C., Sackett D.L., Holmbeck K., Phillips C.L., et al. Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion. Cancer Res 2010, 70:4366-4374.
16. Minafra S., Luparello C., Rallo F., Pucci-Minafra I. Collagen biosynthesis by a breast carcinoma cell strain and biopsy fragments of the primary tumour. Cell Biol Int Rep 1988, 12:895-905.
17. Misof K., Landis W.J., Klaushofer K., Fratzl P. Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J Clin Invest 1997, 100:40-45.
18. McBride D.J., Choe V., Shapiro J.R., Brodsky B. Altered collagen structure in mouse tail tendon lacking the alpha2(I) chain. J Mol Biol 1997, 270:275-284.
19. Narayanan A.S., Meyers D.F., Page R.C., Welgus H.G. Action of mammalian collagenases on type I trimer collagen. Coll Relat Res 1984, 4:289-296.
20. Han S., Makareeva E., Kuznetsova N.V., DeRidder A.M., Sutter M.B., Losert W., et al. Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases. J Biol Chem 2010, 285:22276-22281.
21. Adhikari A.S., Chai J., Dunn A.R. Mechanical load induces a 100-fold increase in the rate of collagen proteolysis by MMP-1. J Am Chem Soc 2011, 133:1686-1689.
22. Flynn B.P., Bhole A.P., Saeidi N., Liles M., Dimarzio C.A., Ruberti J.W. Mechanical strain stabilizes reconstituted collagen fibrils against enzymatic degradation by mammalian collagenase matrix metalloproteinase 8 (MMP-8). PLoS One 2010, 5:e12337.
23. Ellsmere J.C., Khanna R.A., Lee J.M. Mechanical loading of bovine pericardium accelerates enzymatic degradation. Biomaterials 1999, 20:1143-1150.
24. Rainey J., Goh M. An interactive triple-helical collagen builder. Bioinformatics 2004, 20:2458-2459.
25. Humphrey W., Dalke A., Schulten K.V.M.D. Visual molecular dynamics. J Mol Graph 1996, 14:33.
26. Nelson M.T., Humphrey W., Gursoy A., Dalke A., Kale L.V., Skeel R.D., et al. NAMD: a parallel, object oriented molecular dynamics program. Int J High Perform Comput Appl 1996, 10:251-268.
27. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., Field M.J., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998, 102:3586-3616.
28. Anderson D. Collagen self-assembly: a complementary experimental and theoretical perspective 2005, University of Toronto, Toronto, Canada.
29. Gautieri A., Buehler M.J., Redaelli A. Deformation rate controls elasticity and unfolding pathway of single tropocollagen molecules. J Mech Behav Biomed Mater 2009, 2:130-137.
30. Gautieri A., Uzel S., Vesentini S., Redaelli A., Buehler M.J. Molecular and mesoscale mechanisms of osteogenesis imperfecta disease in collagen fibrils. Biophys J 2009, 97:857-865.
31. Srinivasan M., Uzel S.G.M., Gautieri A., Keten S., Buehler M.J. Alport syndrome mutations in type IV tropocollagen alter molecular structure and nanomechanical properties. J Struct Biol 2009, 168:503-510.
32. Stultz C.M., Nerenberg P.S., Salsas-Escat R. Do collagenases unwind triple-helical collagen before peptide bond hydrolysis? Reinterpreting experimental observations with mathematical models. Proteins 2008, 70:1154-1161.
33. Chang S.W., Shefelbine S.J., Buehler M.J. Structural and mechanical differences between collagen homo- and heterotrimers: Relevance for the molecular origin of brittle bone disease. Biophys J 2012, 102(2):640-648.
34. Flynn BP, Tilburey GE, Ruberti JW. Highly sensitive single fibril erosion assay demonstrates mechanochemical switch in native collagen fibrils. Biomech Model Mechanobiol. submitted for publication.
35. Meek K.M., Leonard D.W. Ultrastructure of the corneal stroma: a comparative study. Biophys J 1993, 64:273-280.
36. Tzafriri A.R., Bercovier M., Parnas H. Reaction diffusion model of the enzymatic erosion of insoluble fibrillar matrices. Biophys J 2002, 83:776-793.
37. Rainey J., Goh M. A statistically derived parameterization for the collagen triple-helix. Protein Sci 2002, 11:2748-2754.
38. Sasaki N., Odajima S. Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. J Biomech 1996, 29:655-658.
39. Gautieri A., Vesentini S., Redaelli A., Buehler M.J. Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett 2011, 11:757-766.
40. Humphrey J.D., Wells P.B., Thomsen S., Jones M.A., Baek S. Histological evidence for the role of mechanical stress in modulating thermal denaturation of collagen. Biomech Model Mechanobiol 2005, 4:201-210.
41. Gioia M., Fasciglione G.F., Marini S., D'Alessio S., De Sanctis G., Diekmann O., et al. Modulation of the catalytic activity of neutrophil collagenase MMP-8 on bovine collagen I. Role of the activation cleavage and of the hemopexin-like domain. J Biol Chem 2002, 277:23123-23130.
42. Marini S., Fasciglione G.F., de Sanctis G., D'Alessio S., Politi V., Coletta M. Cleavage of bovine collagen I by neutrophil collagenase MMP-8-Effect of pH on the catalytic properties as compared to synthetic substrates. J Biol Chem 2000, 275:18657-18663.
43. Stultz C.M. Localized unfolding of collagen explains collagenase cleavage near imino-poor sites. J Mol Biol 2002, 319:997-1003.
44. 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.