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Research Article

Molecular events surrounding collagen fibril assembly in the early healing rabbit medial collateral ligament—failure to recapitulate normal ligament development

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Pages 301-312 | Received 28 May 2010, Accepted 13 Sep 2010, Published online: 30 Nov 2010

References

  • Amiel, D., Frank, C.B., Harwood, F.L., Akeson, W.H., and Kleiner, J.B. (1987). Collagen alteration in medial collateral ligament healing in a rabbit model. Connect. Tissue Res. 16:357–366.
  • Weiss, J.A., Woo, S.L., Ohland, K.J., Horibe, S., and Newton, P.O. (1991). Evaluation of a new injury model to study medial collateral ligament healing: Primary repair versus nonoperative treatment. J. Orthop. Res. 9:516–528.
  • Woo, S.L., Niyibizi, C., Matyas J., Kavalkovich, K., Weaver-Green, C., and Fox, R.J. (1997). Medial collateral knee ligament healing. Combined medial collateral and anterior cruciate ligament injuries studied in rabbits. Acta Orthop. Scand. 68:142–148.
  • Murphy, P.G., Frank, C.B., and Hart, D.A. (1993). The cell biology of ligament and ligament healing. In The Anterior Cruciate Ligament, S. Arnoczky, S.L. Woo, C.B. Frank, and D. Jackson ( eds.) pp. 165–167. New York: Raven Press.
  • Frank, C.B., Hart, D.A., and Shrive, N.G. (1999). Molecular biology and biomechanics of normal and healing ligaments – a review. Osteoarthr. Cartil. 7:130–140.
  • Liu, Z.Q., Rangayyan, R.M., and Frank, C.B. (1991). Statistical analysis of collagen alignment in ligaments by scale-space analysis. IEEE Trans. Biomed. Eng. 38:580–588.
  • Frank, C.B., Loitz, B.J., and Shrive, N.G. (1995). Injury location affects ligament healing. A morphologic and mechanical study of the healing rabbit medial collateral ligament. Acta Orthop. Scand. 66:455–462.
  • Frank, C.B., MacDonald, D., Bray, D.F., Rangayyan, R.M., Chimich, D.D., and Shrive, N.G. (1992). Collagen fibril diameters in the healing rabbit medial collateral ligament. Connect. Tissue Res. 27:251–263.
  • Plaas, A.H.K., Wong-Palms, S., Koob, T., Hernandez, D., Marchuk, L., and Frank, C.B. (2000). Proteoglycan metabolism during repair of the ruptured medial collateral ligament in skeletally mature rabbits. Arch. Biochem. Biophys. 374:35–41.
  • Lo, I.K.Y., Marchuk, L.L., Leatherbarrow, K.E., Frank, C.B., and Hart, D.A. (2004). Collagen fibrillogenesis and mRNA levels in the maturing rabbit medial collateral ligament and patellar tendon. Connect. Tissue Res. 45:11–22.
  • Nakamura, N., Hart, D.A., Boorman, R.S., Kaneda, Y., Shrive, N.G., Marchuk, L.L., Shino, K., Ochi, T., and Frank, C.B. (2000). Decorin antisense gene therapy improves functional healing of early rabbit ligament scar with enhanced collagen fibrillogenesis in vivo. J. Orthop. Res. 18(4):517–523.
  • Hart, D.A., Nakamura, N., Marchuk, L., Hiraoka, H., Boorman, R., Kaneda, Y., Shrive, N.G., and Frank, C.B. (2000). Complexity of determining cause and effect in vivo after antisense gene therapy. Clin. Orthop. Relat. Res. (Suppl. 379):S242–S251.
  • Funakoshi, Y., Hariu, M., Tapper, J.E., Marchuk, L.L., Shrive, N.G., Kanaya, F., Rattner, J.B., Hart, D.A., and Frank, C.B. (2007). Periarticular ligament changes following ACL/MCL transection in an ovine stifle joint model of osteoarthritis. J. Orthop. Res. 25(8):997–1006.
  • Majima, T., Lo, I.K., Randle, J.A., Marchuk, L.L., Shrive, N.G., Frank, C.B., and Hart, D.A. (2002). ACL transection influences mRNA levels for collagen type I and TNF-alpha in MCL scar. J. Orthop. Res. 20(3):520–525.
  • Lo, I.K., Marchuk, L., Majima, T., Frank, C.B., and Hart, D.A. (2003). Medial collateral ligament and partial anterior cruciate ligament transection: mRNA changes in uninjured ligaments of the sheep knee. J. Orthop. Sci. 8(5):707–713.
  • Murao, T., Ochi, M., Jitsuiki, J., and Ikuta. (1997). The adverse effects of sectioning the posterior cruciate ligament in rabbits. Changes in the structural and morphological properties of the femur-anterior cruciate ligament–tibia complex. Arch. Orthop. Trauma Surg. 116:1–5.
  • Kadler, K.E., Holmes, D.F., Trotter, J.A., and Chapman, J.A. (1996). Collagen fibril formation. Biochem. J. 316(Pt. 1):1–11.
  • Canty, E.G., and Kadler, K.E. (2005). Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 118:1341–1353.
  • Parry, D.A.D., Barnes, G.R.G., and Craig, A.S. (1978). A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B Biol. Sci. 203:305–321.
  • Moschcovich, L., Bernocco, S., Font, B., Rivkin, H., Eichenberger, D., Chejanovsky, N., Hulmes, D.J.S., and Kessler, E. (2001). Folding and activity of recombinant human procollagen C-proteinase enhancer. Eur. J. Biochem. 268:2991–2996.
  • Elbjeirami, W.M., Yonter, E.O., Starcher, B.C., and West, J.L. (2003). Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity. J. Biomed. Mater. Res. A 66A:513–521.
  • Border, W.A., and Noble, N.A. (1994). Transforming growth factor β in tissue fibrosis. N. Engl. J. Med. 331:1286–1292.
  • Bassols, A., and Massague, J. (1988). Transforming growth factor beta regulates the expression and structure of extracellular matrix chondroitin/dermatan sulfate proteoglycans. J. Biol. Chem. 263:3039–3045.
  • Boak, A.M., Roy, R., Berk, J., Taylor, L., Polgar, P., Goldstein, R.H., and Kagan, H.M. (1994). Regulation of lysyl oxidase expression in lung fibroblasts by transforming growth factor-beta 1 and prostaglandin E2. Am. J. Respir. Cell Mol. Biol. 11:751–755.
  • Ignotz, R.A., and Massague, J. (1986). Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261:4337–4345.
  • Lee, S., Solow-Cordero, D.E., Kessler, E., Takahara, K., and Greenspan, D.S. (1997). Transforming growth factor-beta regulation of bone morphogenetic protein-1/procollagen C‐proteinase and related proteins in fibrogenic cells and keratinocytes. J. Biol. Chem. 272(30):19059–19066.
  • Breitkreutz, D., Stark, H.J., Mirancea, N., Tomakidi, P., Steinbauer, H., and Fusenig, N.E. (1997). Integrin and basement membrane normalization in mouse grafts of human keratinocytes – implications for epidermal homeostasis. Differentiation 61(3):195–209.
  • Chimich, D., Frank, C.B, Shrive, N.G, Dougall, H., and Bray, R. (1991). The effects of initial end contact on medial collateral ligament healing: A morphological and biomechanical study in a rabbit model. J. Orthop. Res. 9:37–47.
  • Reno, C., Marchuk, L.L., Sciore, P., Frank, C.B., and Hart, D.A. (1997). Rapid isolation of total RNA from small samples of hypocellular, dense connective tissues. BioTechniques 22:1082–1086.
  • Boykiw, R., Sciore, P., Reno, C., Marchuk, L., Frank, C.B., and Hart, D.A. (1998). Altered levels of extracellular matrix molecule mRNA in healing rabbit ligaments. Matrix Biol. 17:371–378.
  • Leighton, M., and Kadler, K.E. (2003). Paired basic/Furin-like proprotein convertase cleavage of Pro-BMP-1 in the trans-Golgi network. J. Biol. Chem. 278(20):18478–18484.
  • Frank, C., Bray, D., Radmaker, A., Chrusch, C., Sabiston, P., Bodie, D., and Rangayyan, R. (1989). Electron microscopic quantification of collagen fibril diameters in the rabbit medial collateral ligament: A baseline for comparison. Connect. Tiss. Res. 19:11–25.
  • Kessler, E., Takahara, K., Biniaminov, L., Brusel, M., and Greenspan, D.S. (1996). Bone morphogenic protein-1: The type I procollagen C-proteinase. Science 271:360–362.
  • Li, S.W., Sieron, A.L., Fertala, A., Hojima, Y., Arnold, W.V., and Prockop, D.J. (1996). The Cproteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenic protein-1. Proc. Natl. Acad. Sci. U.S.A. 93(10):5127–5130.
  • Moali, C., Font, B., Ruggiero, F., Eichenberger, D., Rousselle, P., Vincent, F., Oldberg, A., Leena Bruckner-Tuderman, L., and Hulmes, D.J.S. (2005). C-terminal processing of fibrillar procollagens is the only bmp-1-dependent activity to be enhanced by pcpe-1. J. Biol. Chem. 280(25): 24188–24194.
  • Smith-Mungo, L.I., and Kagan, H.M. (1998). Lysyl oxidase: Properties, regulation and multiple functions in biology. Matrix Biol. 16:387–398.
  • Fujimoto, E., and Tajima, S. (2009). Reciprocal regulation of LOX and LOXL2 expression during cell adhesion and terminal differentiation in epidermal keratinocytes. J. Dermatol. Sci. 55(2):91–99.
  • Prockop, D.J., and Kivirikko, K.I. (1995). Collagens: Molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64:403–434.
  • Kagan, H.M., and Li, W. (2003). Lysyl oxidase: Properties, specificity, and biological roles inside and outside of the cell. J. Cell Biochem. 88(4):660–672.
  • Molnar, J., Fong, K.S., He, Q.P., Hayashi, K., Kim, Y., Fong, S.F., Fogelgren, B., Szauter, K.M., Mink, M., and Csiszar, K. (2003). Structural and functional diversity of lysyl oxidase and the LOX-like proteins. Biochim. Biophys. Acta 1647(1–2):224.
  • Noble, N.A., Harper, J.R., and Border, W.A. (1992). In vivo interactions of TGF-beta and extracellular matrix. Prog. Growth Factor Res. 4(4):369–382.
  • Annes, J.P., Munger, J.S., and Rifkin, D.B. (2003). Making sense of latent TGFbeta activation. J. Cell Sci. 116(Pt. 2): 217–224.
  • Ge, G., and Greenspan, D.S. (2006). BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J. Cell Biol. 175(1):111–120.
  • Terrell, T., Working, P., Chow, C., and Green, J. (1993). Pathology of recombinant human transforming growth factor-beta 1 in rats and rabbits. Int. Rev. Exp. Pathol. 34(Pt. B):43–67.
  • Zugmaier, G., Paik, S., Wilding, G., Knabbe, C., Bano, M., Lupu, R., Deschauer, B., Simpson, S., Dickson, R.B., and Lippman, M. (1991). Transforming growth factor b1 induces cachexia and systemic fibrosis without an antitumor effect in nude mice. Cancer Res. 51:3590–3594.
  • Lau, Y.-K., Gobin, A., and West, J. (2006). Overexpression of lysyl oxidase to increase matrix crosslinking and improve tissue strength in dermal wound healing. Ann. Biomed. Eng. 34: 1239–1246.
  • Avery, N.C., and Bailey, A.J. (2005). Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: Relevance to aging and exercise. Scand. J. Med. Sci. Sports 15:231–240.
  • Hulmes, D.J.S., Kadler, K.E., Mould, A.P., Hojima, Y., Holmes, D.F., Cummings, C., Chapman, J.A., and Prockop, D.J. (1989). Pleomorphism in type I collagen fibrils produced by persistence of the procollagen N-propeptide. J. Mol. Biol. 210:337–345.
  • Kadler, K.E., Hojima, Y., and Prockop, D.J. (1987). Assembly of collagen fibrils de novo by cleavage of the type I pC-collagen with procollagen C-proteinase. Assay of critical concentration demonstrates that collagen self-assembly is a classical example of an entropy-driven process. J. Biol. Chem. 262(32):15696–15701.
  • Leung, M.K., Fessler, L.I., Greenberg, D.B., and Fessler, J.H. (1979). Separate amino and carboxyl procollagen peptidases in chick embryo tendon. J. Biol. Chem. 254:224–232.
  • Prockop, D.J., Sieron, A.L., Li, S.W. (1998). Procollagen N‐proteinase and procollagen C-proteinase. Two unusual metalloproteinases that are essential for procollagen processing probably have important roles in development and cell signaling. Matrix Biol. 16(7):399–408.
  • Adar, R., Kessler, E., and Goldberg, B. (1986). Evidence for a protein that enhances the activity of type I procollagen C-proteinase. Coll. Relat. Res. 6:267–277.
  • Kessler, E., and Adar, R. (1989). Type I procollagen C-proteinase from mouse fibroblasts. Eur. J. Biochem. 186:115–121.
  • Ricard-Blum, S., Bernocco, S., Font, B., Moali, C., Eichenberger, D., Farjanel, J., Burchardt, E.R., van der Rest, M., Kessler, E., and Hulmes, D.J.S. (2002). Interaction properties of the procollagen C-proteinase enhancer protein shed light on the mechanism of stimulation of BMP-1. J. Biol. Chem. 277:33864–33869.
  • Steiglitz, B.M., Kreider, J.M., Frankenburg, E.P., Pappano, W.N., Hoffman, G.G., Meganck, J.A., Liang, X., Hook, M., Birk, D.E., Goldstein, S.A., and Greenspan, D.S. (2006). Procollagen C proteinase enhancer 1 genes are important determinants of the mechanical properties and geometry of bone and the ultrastructure of connective tissues. Mol. Cell. Biol. 26:238–249.
  • Frank, C., McDonald, D., and Shrive, N. (1997). Collagen fibril diameters in the rabbit medial collateral ligament scar: A longer term assessment. Connect. Tissue Res. 36:261–269.
  • Shalitin, N., Schlesinger, H., Levy, M.J., Kessler, E., and Kessler-Icekson, G. (2003). Expression of procollagen C‐proteinase enhancer in cultured rat heart fibroblasts: Evidence for co-regulation with type I collagen. J. Cell. Biochem. 90:397–407.
  • Zhang, G., Young, B.B., Ezura, Y., Favata, M., Soslowsky, L.J., Chakravarti, S., and Birk, D.E. (2005). Development of tendon structure and function: Regulation of collagen fibrillogenesis. J. Musculoskelet. Neuronal. Interact. 5(1):5–21.
  • Murphy, P.G., Loitz, B.J., Frank, C.B., and Hart, D.A. (1994). Influence of exogenous growth factors on the synthesis and secretion of collagen types I and III by explants of normal and healing rabbit ligaments. Biochem. Cell Biol. 72(9–10): 403–409.
  • Frank, C.B. (2004). Ligament structure, physiology and function. J. Musculoskelet. Neuronal. Interact. 4(2):199–201.

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