Structural Mechanism for Alteration of Collagen Gel Mechanics by Glutaraldehyde Crosslinking

References

• Brinckmann, J., Notbohm, H., and Müller, P.K., eds. (2005). Collagen – Primer in Structure, Processing and Assembly. Berlin : Springer.
   Google Scholar
• Stenzel, K.H., Miyata, T., and Rubin, A.L. (1974). Collagen as a biomaterial. Annu. Rev. Biophys. Bioeng. 3(1):231–253.
   PubMedGoogle Scholar
• Kadler, K.E., Holmes, D.F., Trotter, J.A., and Chapman, J.A. (1996). Collagen fibril formation. Biochem. J. 316(1):1–11.
   PubMed Web of Science ®Google Scholar
• Eyre, D.R., Paz, M.A., and Gallop, P.M. (1984). Cross-linking in collagen and Elastin. Annu. Rev. Biochem. 53(1):717–748.
   PubMedGoogle Scholar
• McCormick, R.J., and Thomas, D.P. (1998). Collagen crosslinking in the heart: Relationship to development and function. Basic Appl. Myol.8(2):143–150.
   Google Scholar
• Bailey, A.J., Light, N.D., and Atkins, E.D.T. (1980). Chemical cross-linking restrictions on models for the molecular organization of the collagen fibre. Nature 288(5789):408–410.
   PubMed Web of Science ®Google Scholar
• Eyre, D.R., Dickson, I.R., and Van Ness, K. (1988). Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem. J. 252(2):495–500.
   PubMed Web of Science ®Google Scholar
• Barnard, K., Light, N.D., Sims, T.J., and Bailey, A.J. (1987). Chemistry of the collagen cross-links. Origin and partial characterization of a putative mature cross-link of collagen. Biochem. J. 244(2):303–300.
   PubMed Web of Science ®Google Scholar
• Holmes, J.W., Borg, T.K., and Covell, J.W. (2005). Structure and mechanics of healing myocardial infarcts. Ann. Rev. Biomed. Eng. 7(1):223–253.
   PubMedGoogle Scholar
• Goissis, G., Yoshioka, S.A., Braile, D.M., and Ramirez, V.D.A. (1998). The chemical protecting group concept applied in crosslinking of natural tissues with glutaraldehyde acetals. Artifi. Organs. 22(3):210–214.
   PubMed Web of Science ®Google Scholar
• Naimark, W.A., Pereira, C.A., Tsang, K., and Lee, J.M. (1995). HMDC crosslinking of bovine pericardial tissue: A potential role of the solvent environment in the design of bioprosthetic materials. J. Mater. Sci. Mater. Med. 6(4):235–241.
   Web of Science ®Google Scholar
• Zilla, P., Bezuidenhout, D., Weissenstein, C., Walt, A., and Human, P. (2001). Diamine extension of glutaraldehyde crosslinks mitigates bioprosthetic aortic wall calcification in the sheep model. J. Biomed. Mater. Res. 56(1):56–64.
   PubMed Web of Science ®Google Scholar
• Thomopoulos, S., Fomovsky, G.M., Chandran, P.L., and Holmes, J.W. (2007). Collagen fiber alignment does not explain mechanical anisotropy in fibroblast populated collagen gels. J. Biomech. Eng. 129(5):642.
   PubMed Web of Science ®Google Scholar
• Thomopoulos, S., Fomovsky, G.M., and Holmes, J.W. (2005). The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J. Biomech. Eng. 127(5):742–750.
   PubMed Web of Science ®Google Scholar
• Bell, E., Ivarsson, B., and Merrill, C. (1979). Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vivo. In Proceedings of the National Academy of Sciences of the USA. 76:1274–1278.
   PubMed Web of Science ®Google Scholar
• Chandran, P.L., and Barocas, V.H. (2004). Microstructural mechanics of collagen gels in confined compression: Poroelasticity, viscoelasticity, and collapse. J. Biomech. Eng.126(2):152–166.
   PubMed Web of Science ®Google Scholar
• Olde Damink, L.H.H., Dijkstra, P.J., Van Luyn, M.J.A., Van Wachem, P.B., Nieuwenhuis, P., and Feijen, J. (1995). Glutaraldehyde as a crosslinking agent for collagen-based biomaterials. J. Mater. Sci. Mater. Med. 6(8):460–472.
   Web of Science ®Google Scholar
• Hopwood, D. (1972). Theoretical and practical aspects of glutaraldehyde fixation. Histochem. J. 4(4):1573–6865.
   Google Scholar
• Hopwood, D. (1967). Some aspects of fixation with glutaraldehyde. A biochemical and histochemical comparison of the effects of formaldehyde and glutaraldehyde fixation on various enzymes and glycogen, with a note on penetration of glutaraldehyde into liver. J Anat. 10(1):83–92.
   Google Scholar
• Knezevic, V., Sim, A.J., Borg, T.K., and Holmes J.W. (2002). Isotonic biaxial loading of fibroblastpopulated collagen gels: A versatile, low-cost system for the study of mechanobiology. Biomech. Model. Mechanobiol. 1:59–67.
   PubMed Web of Science ®Google Scholar
• Grinnell, F., and Lamke, C.R. (1984). Reorganization of hydrated collagen lattices by human skin fibroblasts. J. Cell Sci. 66:51–63.
   PubMed Web of Science ®Google Scholar
• Hayat, M. (1986). Glutaraldehyde: Role in electron microscopy. Micron Microsc. Acta. 17(22):15–35.
   Google Scholar
• Sacks, M.S., and Sun, W. (2003). Multiaxial mechanical behavior of biological materials. Annu. Rev. Biomed. Eng. 5(1):251–284.
   PubMedGoogle Scholar
• Sacks, M.S. (2000). Biaxial mechanical evaluation of planar biological materials. J. Elast. 61:199–246.
   Web of Science ®Google Scholar
• Waldman, S.D., Sacks, M.S., and Lee, J.M., (2002). Boundary conditions during biaxial testing of planar connective tissues Part II Fiber orientation. J. Mater. Sci. Lett. 21(15):1215–1221.
   Google Scholar
• Moore, M.A., Chen, W., Phillips, R.E., Bohachevsky, I.K., and McIlroy, B.K. (1996). Shrinkage temperature versus protein extraction as a measure of stabilization of photooxidized tissue. J. Biomed. Mater. Res. 32(2):209–214.
   PubMed Web of Science ®Google Scholar
• Simionescu, A., Simionescu, D., and Deac, R. (1991). Lysine-enhanced glutaraldehyde crosslinking of collagenous biomaterials. J. Biomed. Mater. Res. 25(12):1495–505.
   PubMed Web of Science ®Google Scholar
• Duncan, A.C., Boughner, D., and Vesely, I. (1997). Viscoelasticity of dynamically fixed bioprosthetic valves. II. Effect of glutaraldehyde concentration. J. Thorac. Cardiovasc. Surg. 113(2):302–310.
   PubMed Web of Science ®Google Scholar
• Korn, A.H., Feairheller, S.H., and Filachione, E.M. (1972). Glutaraldehyde: Nature of the reagent. J. Mol. Biol. 65(3):525–529.
   PubMed Web of Science ®Google Scholar
• Anderson, P.J. (1967). Purification and quantification of glutaraldehyde and its effect on several enzyme activities in skeletal muscle 652. J. Histochem. Cytochem. 15:652.
   PubMed Web of Science ®Google Scholar
• Tashima, T., Kawakami, U., Satoh, N., Nakagawa, T., and Tanaka, H. (1987). Detection of impurities in aqueous solution of glutaraldehyde by high performance liquid chromatography with a multichannel photodiode array UV detector. J. Electron. Microscopy 36(3):136–138.
   PubMed Web of Science ®Google Scholar
• Lastowka, A., and Maffia, G. (2005). A comparison of chemical, physical and enzymatic crosslinking of bovine type 1 collagen fibrils. J. Am. Leather Chem. Assoc. 100:196–02.
   Google Scholar
• Jarman-Smith, M.L., Bodamyali, T., Stevens, C., Howell, J.A., Horrocks, M., and Chaudhuri, J.B. (2004). Porcine collagen crosslinking, degradation and its capability for fibroblast adhesion 34 and proliferation. J. Mater. Sci. Mater. Med. 15(8):925–932.
   PubMed Web of Science ®Google Scholar
• Stegeman, H., and Stalder, K. (1967). Determination of hydroxyproline. Clin. Chim. Acta. 1967;18:267–273.
   Google Scholar
• Fung, Y.C. (1993). Biomechanics: Mechanical Properties of Living Tissues. New York: Springer.
   Google Scholar
• Misof, K., Rapp, G., and Fratzl, P. (1997). A new molecular model for collagen elasticity based on synchrotron X-ray scattering evidence. Biophys. J. 72(3):1376–1381.
   PubMed Web of Science ®Google Scholar
• Puxkandl, R., Zizak, I., Paris, O., Keckes, J., Tesch, W., Bernstorff, S., Purslow. P., and Fratzl, P. (2002). Viscoelastic properties of collagen: Synchrotron radiation investigations and structural model. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357(1418):191–197.
   PubMed Web of Science ®Google Scholar
• Chandran, P.L., and Barocas, V.H. (2006). Affine versus non-affine fibril kinematics in collagen networks: Theoretical studies of network behavior. J. Biomech. Eng. 128(2):259–270.
   PubMed Web of Science ®Google Scholar
• Chandran, P.L., and Barocas, V.H. (2007). Deterministic material-based averaging theory model of collagen gel micromechanics. J. Biomech. Eng. 129(2):137–147.
   PubMed Web of Science ®Google Scholar
• Tower, T.T., Neidert, M.R., and Tranquillo, R.T. (2002). Fiber alignment imaging during mechanical testing of soft tissues. Ann. Biomed. Eng. 30(10):1221–1233.
   PubMed Web of Science ®Google Scholar
• Billiar, K.L., and Sacks, M.S. (2000). Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp–Part I: Experimental results. J. Biomech. Eng. 122(1):23–30.
   PubMed Web of Science ®Google Scholar
• Billiar, K.L., and Sacks, M.S. (2000). Biaxial mechanical properties of the fresh and glutaraldehyde treated porcine aortic valve: Part II - A structurally guided constitutive model. J. Biomech. Eng. 122(4):327–335.
   PubMed Web of Science ®Google Scholar
• Zioupos, P., Barbenel, J.C., and Fisher, J. (1994). Anisotropic elasticity and strength of glutaraldehyde fixed bovine pericardium for use in pericardial bioprosthetic valves. J. Biomed. Mater. Res. 28(1):49–57.
   PubMed Web of Science ®Google Scholar
• van Noort, R., Yates, S.P., Martin, T.R., Barker, A.T., and Black, M.M. (1982). A study of the effects of glutaraldehyde and formaldehyde on the mechanical behaviour of bovine pericardium. Biomaterials 3(1):21–26.
   PubMed Web of Science ®Google Scholar
• Mayne, A.S., Christie, G.W., Smaill, B.H., Hunter, P.J., and Barratt-Boyes, B.G. (1989). An assessment of the mechanical properties of leaflets from four second- generation porcine bioprostheses with biaxial testing techniques. J. Thorac. Cardiovasc. Surg. 98(2):170–180.
   PubMed Web of Science ®Google Scholar
• Sacks, M.S., and Chuong, C.J. (1998). Orthotropic mechanical properties of chemically treated bovine pericardium. Ann. Biomed. Eng. 26(5):892–902.
   PubMed Web of Science ®Google Scholar
• Migneault, I., Dartiguenave, C., Bertrand, M.J., and Waldron, K.C. (2004). Glutaraldehyde: Behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. BioTechniques 37(5):790–802.
   PubMed Web of Science ®Google Scholar
• Richards, F.M., and Knowles, J.R. (1968). Glutaraldehyde as a protein crosslinking reagent. J. Mol. Biol. 37:231–335.
   PubMed Web of Science ®Google Scholar
• Wine Y., Cohen-Hadar, N, Freeman, A., and Frolow, F. (2007). Elucidation of the mechanism and end products of glutaraldehyde crosslinking reaction by X-ray structure analysis. Biotechnol. Bioeng. 98(3):711–718.
   PubMed Web of Science ®Google Scholar
• Bowes, J.H., and Cater, C.W. (1965). Cross-linking of collagen. J. Appl. Chem. 15:296.
   Google Scholar
• Bowes, J.H., and Cater, C.W. (1968). The interaction of aldehydes with collagen. Biochem. Biophys. Acta. 168:341.
   PubMed Web of Science ®Google Scholar
• Cheung, D.T., and Nimni, M.E. (1982). Mechanism of crosslinking of proteins by glutaraldehyde II. Reaction with monomeric and polymeric collagen. Connect. Tissue. Res. 10:201–216.
   PubMed Web of Science ®Google Scholar
• Aso. C., and Aito, Y. (1962). Studies on the polymerization of bifunctional monomers. II. Polymerization of glutaraldehyde. Makromol. Chem. 58(1):195–203.
   Google Scholar
• Tower, T.T., Neidert, M.R., and Tranquillo, R.T. (2002). Fiber alignment imaging during mechanical testing of soft tissues. Ann. Biomed. Eng. 30(10):1221–1233.
   PubMed Web of Science ®Google Scholar
• Duncan, A.C., Boughner, D., and Vesely, I. (1996). Dynamic glutaraldehyde fixation of a porcine aortic valve xenograft. I. Effect of fixation conditions on the final tissue viscoelastic properties. Biomaterials. 17(19):1849–1856.
   PubMed Web of Science ®Google Scholar