The influence of discoidin domain receptor 2 on the persistence length of collagen type I fibers

Biomaterials

Volumn 31, Issue 18, 2010, Pages 4802-4808

  Sivakumar, Lalitha ^a   Agarwal, Gunjan ^a,b  

^a The Ohio State University   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Collagen; ECM (extracellular matrix); Mechanical properties; Recombinant protein; Transmission electron microscopy (TEM)

Indexed keywords

ANALYTICAL APPROACH; CELLULAR PROCESS; COLLAGEN CONCENTRATION; COLLAGEN FIBER; COLLAGEN TYPE I; DIAMETER MEASUREMENT; DISCOIDIN DOMAIN RECEPTOR 2; ECM (EXTRACELLULAR MATRIX); EXTRACELLULAR MATRICES; FIBER DIAMETERS; IMPACT TENSILE STRENGTH; IN-VITRO; MEDICAL IMPLANTS; NATIVE COLLAGEN; NATIVE STRUCTURES; PERSISTENCE LENGTH; RECOMBINANT PROTEIN; TEM; TRANSMISSION ELECTRON MICROSCOPE; YOUNG'S MODULUS;

BIOMECHANICS; FIBERS; IMPACT STRENGTH; MECHANICAL PROPERTIES; SCANNING ELECTRON MICROSCOPY; STIFFNESS MATRIX; TENSILE STRENGTH; TISSUE ENGINEERING; TRANSMISSION ELECTRON MICROSCOPY;

COLLAGEN;

COLLAGEN BINDING PROTEIN; COLLAGEN FIBER; COLLAGEN TYPE 1; DISCOIDIN DOMAIN RECEPTOR 2; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EXTRACELLULAR MATRIX; IMPLANT; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; RECEPTOR UPREGULATION; RIGIDITY; TENSILE STRENGTH; TISSUE ENGINEERING; TRANSMISSION ELECTRON MICROSCOPY; TURBIDITY; YOUNG MODULUS;

ANIMALS; CATTLE; CERCOPITHECUS AETHIOPS; COLLAGEN TYPE I; COS CELLS; ELASTIC MODULUS; EXTRACELLULAR MATRIX; HUMANS; MICE; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; RECOMBINANT PROTEINS;

VERTEBRATA;

EID: 77951975626     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.02.070     Document Type: Article

References (41)

1. Neame P.J.C., Kay J., McQuillan D.J., Beales M.P., Hassell J.R. Independent modulation of collagen fibrillogenesis by decorin and lumican. Cell Mol Life Sci 2000, 57:859-863.
2. Halasz K., Kassner A., Morgelin M., Heinegard D. COMP acts as a catalyst in collagen fibrillogenesis. J Biol Chem 2007, 282:31166-31173.
3. Kalamajski S., Oldberg A. Fibromodulin binds collagen type I via Glu-353 and Lys-355 in leucine-rich repeat 11. J Biol Chem 2007, 282:26740-26745.
4. Rentz T.J., Poobalarahi F., Bornstein P., Sage E.H., Bradshaw A.D. SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 2007, 282:22062-22071.
5. Nicolae C., Ko Y.P., Miosge N., Niehoff A., Studer D., Enggist L., et al. Abnormal collagen fibrils in cartilage of matrilin-1/matrilin-3-deficient mice. J Biol Chem 2007, 282:22163-22175.
6. Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T.E., et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1997, 1:25-34.
7. Vogel W., Gish G.D., Alves F., Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997, 1:13-23.
8. Mihai C., Iscru D.F., Druhan L.J., Elton T.S., Agarwal G. Discoidin domain receptor 2 inhibits fibrillogenesis of collagen type 1. J Mol Biol 2006, 361:864-876.
9. Blissett A.R., Garbellini D., Calomeni E.P., Mihai C., Elton T.S., Agarwal G. Regulation of collagen fibrillogenesis by cell-surface expression of kinase dead DDR2. J Mol Biol 2009, 385:902-911.
10. Flynn L.A., Blissett A.R., Calomeni E.P., Agarwal G. Inhibition of collagen fibrillogenesis by cells expressing soluble extracellular domains of DDR1 and DDR2. J Mol Biol 2010, 395:533-543.
11. Sun Y.L., Luo Z.P., Fertala A., An K.N. Direct quantification of the flexibility of type I collagen monomer. Biochem Biophys Res Comm 2002, 295:382-386.
12. Sasaki N., Odajima S. Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. J Biomech 1996, 29:1131-1136.
13. Hofmann H., Voss T., Kuhn K., Engel J. Localization of flexible sites in thread-like molecules from electron micrographs: comparison of interstitial, basement membrane and intima collagens. J Mol Biol 1984, 172:325-343.
14. Utiyama H., Sakato K., Ikehara K., Setsuiye T., Kurata M. Flexibility of tropocollagen from sedimentation and viscosity. Biopolymers 1973, 12:53-64.
15. Nestler F.H., Hvidt S., Ferry J.D., Veis A. Flexibility of collagen determined from dilute solution viscoelastic measurements. Biopolymers 1983, 22:1747-1758.
16. Buehler M.J. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc Natl Acad Sci U S A 2006, 103:12285-12290.
17. Claire K. Translational and rotational dynamics of collagen in dilute solution. J Phys Chem 1997, 101:8.
18. Van der Rijt J.A., Van der Werf K.O., Bennink M.L., Dijkstra P.J., Feijen J. Micromechanical testing of individual collagen fibrils. Macromol Biosci 2006, 6:697-702.
19. Graham J.S., Vomund A.N., Phillips C.L., Grandbois M. Structural changes in human type I collagen fibrils investigated by force spectroscopy. Exp Cell Res 2004, 299:335-342.
20. Cavalcante F.S., Ito S., Brewer K., Sakai H., Alencar A.M., Almeida M.P., et al. Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J Appl Physiol 2005, 98:672-679.
21. Shen Z.L., Dodge M.R., Kahn H., Ballarini R., Eppell S.J. Stress-strain experiments on individual collagen fibrils. Biophys J 2008, 95:3956-3963.
22. Buehler M.J. Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies. J Mech Behav Biomed Mater 2008, 1:59-67.
23. Bednar J., Furrer P., Katritch V., Stasiak A.Z., Dubochet J., Stasiak A. Determination of DNA persistence length by cryo-electron microscopy. Separation of the static and dynamic contributions to the apparent persistence length of DNA. J Mol Biol 1995, 254:579-594.
24. Frontali C., Dore E., Ferrauto A., Gratton E., Bettini A., Pozzan M.R., et al. An absolute method for the determination of the persistence length of native DNA from electron micrographs. Biopolymers 1979, 18:1353-1373.
25. Landau L.D., Lifshitz E.M. Fluctuations in the curvature of long molecules. Statistical physics part I 1980, Pergamon Press, Oxford.
26. Guthold M., Liu W., Sparks E.A., Jawerth L.M., Peng L., Falvo M., et al. A comparison of the mechanical and structural properties of fibrin fibers with other protein fibers. Cell Biochem Biophys 2007, 49:165-181.
27. Gittes F., Mickey B., Nettleton J., Howard J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 1993, 120:923-934.
28. Abels J.A., Moreno-Herrero F., Van der Heijden T., Dekker C., Dekker N.H. Single-molecule measurements of the persistence length of double-stranded RNA. Biophys J 2005, 88:2737-2744.
29. Guarnieri D., Battista S., Borzacchiello A., Mayol L., De Rosa E., Keene D.R., et al. Effects of fibronectin and laminin on structural, mechanical and transport properties of 3D collageneous network. J Mater Sci: Mater Med 2007, 18:245-253.
30. Georges P.C., Hui J.J., Gombos Z., McCormick M.E., Wang A.Y., Uemura M., et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 2007, 293:G1147-G1154.
31. Kuhl E. Remodeling of biological tissue: mechanically induced reorientation of a transversely isotropic chain network. J Mech Phys of Solids 2005, 53:22.
32. Stein A.M., Vader D.A., Jawerth L.M., Weitz D.A., Sander L.M. An algorithm for extracting the network geometry of three-dimensional collagen gels. J Microsc 2008, 232:463-475.
33. Stuart K., Panitch A. Influence of chondroitin sulfate on collagen gel structure and mechanical properties at physiologically relevant levels. Biopolymers 2008, 89:841-851.
34. Mihai C., Chotani M., Elton T.S., Agarwal G. Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J Mol Biol 2009, 385:432-445.
35. Bhadriraju K., Chung K.H., Spurlin T.A., Haynes R.J., Elliott J.T., Plant A.L. The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the downregulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 2009, 30(35):6687-6694.
36. Ichikawa O., Osawa M., Nishida N., Goshima N., Nomura N., Shimada I. Structural basis of the collagen-binding mode of discoidin domain receptor 2. EMBO J 2007, 26:4168-4176.
37. Konitsiotis A.D., Raynal N., Bihan D., Hohenester E., Farndale R.W., Leitinger B. Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J Biol Chem 2008, 283:6861-6868.
38. Agarwal G., Kovac L., Radziejewski C., Samuelsson S.J. Binding of discoidin domain receptor 2 to collagen I: an atomic force microscopy investigation. Biochemistry 2002, 41:11091-11098.
39. 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.
40. Perumal S., Antipova O., Orgel J.P. Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proc Natl Acad Sci U S A 2008, 105:2824-2829.
41. Sejin Han C.P., McBride D., Visse R., Nagase H., Losert W., Leikin S. Bending rigidity of type I collagen homotrimer fibrils. Biophys J 2009, 96.