Growth/differentiation factor-5 modulates the synthesis and expression of extracellular matrix and cell-adhesion-related molecules of rat Achilles tendon fibroblasts

REFERENCES

• Sharma, P., and Maffulli, N. (2005). Tendon injury and tendinopathy: Healing and repair. J. Bone Joint Surg. Am. 87: 187–202.
   PubMed Web of Science ®Google Scholar
• Wang, J.H. (2006). Mechanobiology of tendon. J. Biomech. 39:1563–1582.
   PubMed Web of Science ®Google Scholar
• Reddy, G.K., Stehno-Bittel, L., and Enwemeka, C.S. (1999). Matrix remodeling in healing rabbit Achilles tendon. Wound Repair Regen. 7:518–527.
   PubMed Web of Science ®Google Scholar
• Manske, P.R., and Lesker, P.A. (1984). Biochemical evidence of flexor tendon participation in the repair process–an in vitro study. J. Hand Surg. Br. 9:117–120.
   PubMedGoogle Scholar
• Gelberman, R.H., Manske, P.R., Vande Berg, J.S., Lesker, P.A., and Akeson, W.H. (1984). Flexor tendon repair in vitro: A comparative histologic study of the rabbit, chicken, dog, and monkey. J. Orthop. Res. 2:39–48.
   PubMedGoogle Scholar
• Potenza, A.D. (1962). Tendon healing within the flexor digital sheath in the dog. J. Bone Joint Surg. Am. 44–A:49–64.
   PubMed Web of Science ®Google Scholar
• Bruns, J., Kampen, J., Kahrs, J., and Plitz, W. (2000). Achilles tendon rupture: Experimental results on spontaneous repair in a sheep-model. Knee Surg. Sports Traumatol. Arthrosc. 8:364–369.
   PubMed Web of Science ®Google Scholar
• Mehta, V., and Mass, D. (2005). The use of growth factors on tendon injuries. J. Hand Ther. 18:87,92; quiz 93.
   PubMedGoogle Scholar
• Chan, B.P., Fu, S.C., Qin, L., Rolf, C., and Chan, K.M. (2006). Supplementation-time dependence of growth factors in promoting tendon healing. Clin. Orthop. Relat. Res. 448: 240–247.
   PubMedGoogle Scholar
• Thomopoulos, S., Harwood, F.L., Silva, M.J., Amiel, D., and Gelberman, R.H. (2005). Effect of several growth factors on canine flexor tendon fibroblast proliferation and collagen synthesis in vitro. J. Hand Surg. Am. 30:441–447.
   PubMed Web of Science ®Google Scholar
• Wang, J.H., Iosifidis, M.I., and Fu, F.H. (2006). Biomechanical basis for tendinopathy. Clin. Orthop. Relat. Res. 443:320–332.
   PubMed Web of Science ®Google Scholar
• Tsubone, T., Moran, S.L., Amadio, P.C., Zhao, C., and An, K.N. (2004). Expression of growth factors in canine flexor tendon after laceration in vivo. Ann. Plast. Surg. 53:393–397.
   PubMed Web of Science ®Google Scholar
• Molloy, T., Wang, Y., and Murrell, G. (2003). The roles of growth factors in tendon and ligament healing. Sports Med. 33:381–394.
   PubMed Web of Science ®Google Scholar
• Aspenberg, P., and Forslund, C. (1999). Enhanced tendon healing with GDF 5 and 6. Acta Orthop. Scand. 70:51–54.
   PubMed Web of Science ®Google Scholar
• Wolfman, N.M., Hattersley, G., Cox, K., Celeste, A.J., Nelson, R., Yamaji, N., Dube, J.L., DiBlasio-Smith, E., Nove, J., Song, J.J., Wozney, J.M., and Rosen, V. (1997). Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J. Clin. Invest. 100: 321–330.
   PubMed Web of Science ®Google Scholar
• Tsumaki, N., Tanaka, K., Arikawa-Hirasawa, E., Nakase, T., Kimura, T., Thomas, J.T., Ochi, T., Luyten, F.P., and Yamada, Y. (1999). Role of CDMP-1 in skeletal morphogenesis: Promotion of mesenchymal cell recruitment and chondrocyte differentiation. J. Cell Biol. 144:161–173.
   PubMed Web of Science ®Google Scholar
• Upton, P.D., Long, L., Trembath, R.C., and Morrell, N.W. (2008). Functional characterization of bone morphogenetic protein binding sites and Smad1/5 activation in human vascular cells. Mol.Pharmacol. 73:539–552.
   PubMed Web of Science ®Google Scholar
• Miyazono, K., Kusanagi, K., and Inoue, H. (2001). Divergence and convergence of TGF-beta/BMP signaling. J. Cell. Physiol. 187:265–276.
   PubMed Web of Science ®Google Scholar
• Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y.I., and Knaus, P. (2002). The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem. 277:5330–5338.
   PubMed Web of Science ®Google Scholar
• Heinecke, K., Seher, A., Schmitz, W., Mueller, T.D., Sebald, W., and Nickel, J. (2009). Receptor oligomerization and beyond: A case study in bone morphogenetic proteins. BMC Biol. 7:59.
   PubMed Web of Science ®Google Scholar
• Storm, E.E., and Kingsley, D.M. (1999). GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 209:11–27.
   PubMed Web of Science ®Google Scholar
• Francis-West, P.H., Abdelfattah, A., Chen, P., Allen, C., Parish, J., Ladher, R., Allen, S., MacPherson, S., Luyten, F.P., and Archer, C.W. (1999). Mechanisms of GDF-5 action during skeletal development. Development 126:1305–1315.
   PubMed Web of Science ®Google Scholar
• Chhabra, A., Tsou, D., Clark, R.T., Gaschen, V., Hunziker, E.B., and Mikic, B. (2003). GDF-5 deficiency in mice delays Achilles tendon healing. J. Orthop. Res. 21:826–835.
   PubMed Web of Science ®Google Scholar
• Rickert, M., Jung, M., Adiyaman, M., Richter, W., and Simank, H.G. (2001). A growth and differentiation factor-5 (GDF-5)-coated suture stimulates tendon healing in an Achilles tendon model in rats. Growth Factors 19:115–126.
   PubMed Web of Science ®Google Scholar
• Nakase, T., Sugamoto, K., Miyamoto, T., Tsumaki, N., Luyten, F.P., Inui, H., Myoui, A., Tomita, T., and Yoshikawa, H. (2002). Activation of cartilage-derived morphogenetic protein-1 in torn rotator cuff. Clin. Orthop. Relat. Res. 399:140–145.
   PubMedGoogle Scholar
• Hogan, M., Girish, K., James, R., Balian, G., Hurwitz, S., and Chhabra, A.B. (2010). Growth differentiation factor-5 regulation of extracellular matrix gene expression in murine tendon fibroblasts. J. Tissue Eng. Regen. Med. [Epub ahead of print].
   Google Scholar
• Park, A., Hogan, M.V., Kesturu, G.S., James, R., Balian, G., and Chhabra, A.B. (2010). Adipose-derived mesenchymal stem cells treated with growth differentiation factor-5 express tendon-specific markers. Tissue Eng. A. 16:2941–2951.
   PubMed Web of Science ®Google Scholar
• Dines, J.S., Weber, L., Razzano, P., Prajapati, R., Timmer, M., Bowman, S., Bonasser, L., Dines, D.M., and Grande, D.P. (2007). The effect of growth differentiation factor-5-coated sutures on tendon repair in a rat model. J. Shoulder Elbow Surg. 16:S215–S221.
   PubMed Web of Science ®Google Scholar
• Yin, S., Cen, L., Wang, C., Zhao, G., Sun, J., Liu, W., Cao, Y., and Cui, L. (2010). Chondrogenic transdifferentiation of human dermal fibroblasts stimulated with cartilage-derived morphogenetic protein 1. Tissue Eng. A. 16:1633–1643.
   PubMed Web of Science ®Google Scholar
• Bring, D.K., Reno, C., Renstrom, P., Salo, P., Hart, D.A., and Ackermann, P.W. (2009). Joint immobilization reduces the expression of sensory neuropeptide receptors and impairs healing after tendon rupture in a rat model. J. Orthop. Res. 27:274–280.
   PubMed Web of Science ®Google Scholar
• Nakamura, M., Sone, S., Takahashi, I., Mizoguchi, I., Echigo, S., and Sasano, Y. (2005). Expression of versican and ADAMTS1, 4, and 5 during bone development in the rat mandible and hind limb. J. Histochem. Cytochem. 53:1553–1562.
   PubMed Web of Science ®Google Scholar
• Birch, H.L. (2007). Tendon matrix composition and turnover in relation to functional requirements. Int. J. Exp. Pathol. 88:241–248.
   PubMed Web of Science ®Google Scholar
• Oshin, A.O., and Stewart, M.C. (2007). The role of bone morphogenetic proteins in articular cartilage development, homeostasis and repair. Vet. Comp. Orthop. Traumatol. 20:151–158.
   Google Scholar
• Aspenberg, P. (2007). Stimulation of tendon repair: Mechanical loading, GDFs and platelets. A mini-review. Int. Orthop. 31:783–789.
   PubMed Web of Science ®Google Scholar
• Sakai, T., Yasuda, K., Tohyama, H., Azuma, H., Nagumo, A., Majima, T., and Frank, C.B. (2002). Effects of combined administration of transforming growth factor-beta1 and epidermal growth factor on properties of the in situ frozen anterior cruciate ligament in rabbits. J. Orthop. Res. 20:1345–1351.
   PubMed Web of Science ®Google Scholar
• Chang, J., Most, D., Stelnicki, E., Siebert, J.W., Longaker, M.T., Hui, K., and Lineaweaver, W.C. (1997). Gene expression of transforming growth factor beta-1 in rabbit zone II flexor tendon wound healing: Evidence for dual mechanisms of repair. Plast. Reconstr. Surg. 100:937–944.
   PubMed Web of Science ®Google Scholar
• Ferguson, M.W., and O'Kane, S. (2004). Scar-free healing: From embryonic mechanisms to adult therapeutic intervention. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359:839–850.
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Shirai, T., Morishita, S., Uchida, S., Saeki-Miura, K., and Makishima, F. (1999). p38- mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp. Cell Res. 250:351–363.
   PubMed Web of Science ®Google Scholar
• Gruber, R., Mayer, C., Bobacz, K., Krauth, M.T., Graninger, W., Luyten, F.P., and Erlacher, L. (2001). Effects of cartilage-derived morphogenetic proteins and osteogenic protein-1 on osteochondrogenic differentiation of periosteum-derived cells. Endocrinology 142:2087–2094.
   PubMed Web of Science ®Google Scholar
• Nakamura, T., Yamamoto, M., Tamura, M., and Izumi, Y. (2003). Effects of growth/differentiation factor-5 on human periodontal ligament cells. J. Periodontal Res. 38:597–605.
   PubMed Web of Science ®Google Scholar
• Birch, H.L., Bailey, J.V., Bailey, A.J., and Goodship, A.E. (1999). Age-related changes to the molecular and cellular components of equine flexor tendons. Equine Vet. J. 31: 391–396.
   PubMed Web of Science ®Google Scholar
• Scott, J.E. (1995). Extracellular matrix, supramolecular organisation and shape. J. Anatomica. 187(2):259–269.
   Google Scholar
• Schonherr, E., and Hausser, H.J. (2000). Extracellular matrix and cytokines: A functional unit. Dev. Immunol. 7:89–101.
   PubMedGoogle Scholar
• Rooney, P., Grant, M.E., and McClure, J. (1992). Endochondral ossification and de novo collagen synthesis during repair of the rat Achilles tendon. Matrix 12:274–281.
   PubMedGoogle Scholar
• Forslund, C., Rueger, D., and Aspenberg, P. (2003). A comparative dose-response study of cartilage-derived morphogenetic protein (CDMP)-1, -2 and -3 for tendon healing in rats. J. Orthop. Res. 21:617–621.
   PubMed Web of Science ®Google Scholar
• Berglund, M., Reno, C., Hart, D.A., and Wiig, M. (2006). Patterns of mRNA expression for matrix molecules and growth factors in flexor tendon injury: Differences in the regulation between tendon and tendon sheath. J. Hand Surg. Am. 31:1279–1287.
   PubMed Web of Science ®Google Scholar
• Danielson, K.G., Baribault, H., Holmes, D.F., Graham, H., Kadler, K.E., and Iozzo, R.V. (1997). Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136:729–743.
   PubMed Web of Science ®Google Scholar
• Berglund, M., Wiig, M., Torstensson, M., Reno, C., and Hart, D.A. (2004). Assessment of mRNA levels for matrix molecules and TGF- beta1 in rabbit flexor and peroneus tendons reveals regional differences in steady-state expression. J. Hand Surg. Br. 29:165–169.
   PubMedGoogle Scholar
• Robbins, J.R., and Vogel, K.G. (1994). Regional expression of mRNA for proteoglycans and collagen in tendon. Eur. J. Cell Biol. 64:264–270.
   PubMed Web of Science ®Google Scholar
• Young, M.F., Bi, Y., Ameye, L., and Chen, X.D. (2002). Biglycan knockout mice: New models for musculoskeletal diseases. Glycoconj. J. 19:257–262.
   PubMed Web of Science ®Google Scholar
• Thomopoulos, S., Hattersley, G., Rosen, V., Mertens, M., Galatz, L., Williams, G.R., and Soslowsky, L.J. (2002). The localized expression of extracellular matrix components in healing tendon insertion sites: An in situ hybridization study. J. Orthop. Res. 20:454–463.
   PubMed Web of Science ®Google Scholar
• Stokes, M.B., Hudkins, K.L., Zaharia, V., Taneda, S., and Alpers, C.E. (2001). Up-regulation of extracellular matrix proteoglycans and collagen type I in human crescentic glomerulonephritis. Kidney Int. 59:532–542.
   PubMed Web of Science ®Google Scholar
• Funderburgh, J.L., Mann, M.M., and Funderburgh, M.L. (2003). Keratocyte phenotype mediates proteoglycan structure: A role for fibroblasts in corneal fibrosis. J. Biol. Chem. 278:45629–45637.
   PubMed Web of Science ®Google Scholar
• Yoon, J.H., and Halper, J. (2005). Tendon proteoglycans: Biochemistry and function. J. Musculoskelet. Neuronal Interact. 5:22–34.
   PubMedGoogle Scholar
• Bode-Lesniewska, B., Dours-Zimmermann, M.T., Odermatt, B.F., Briner, J., Heitz, P.U., and Zimmermann, D.R. (1996). Distribution of the large aggregating proteoglycan versican in adult human tissues. J. Histochem. Cytochem. 44:303–312.
   PubMed Web of Science ®Google Scholar
• Ritty, T.M., Roth, R., and Heuser, J.E. (2003). Tendon cell array isolation reveals a previously unknown fibrillin-2-containing macromolecular assembly. Structure 11:1179–1188.
   PubMed Web of Science ®Google Scholar
• Wight, T.N. (2002). Versican: A versatile extracellular matrix proteoglycan in cell biology. Curr. Opin. Cell Biol. 14:617–623.
   PubMed Web of Science ®Google Scholar
• Scott, A., Lian, O., Roberts, C.R., Cook, J.L., Handley, C.J., Bahr, R., Samiric, T., Ilic, M.Z., Parkinson, J., Hart, D.A., Duronio, V., and Khan, K.M. (2008). Increased versican content is associated with tendinosis pathology in the patellar tendon of athletes with jumper's knee. Scand. J. Med. Sci. Sports 18:427–435.
   PubMed Web of Science ®Google Scholar
• Corps, A.N., Robinson, A.H., Movin, T., Costa, M.L., Ireland, D.C., Hazleman, B.L., and Riley, G.P. (2004). Versican splice variant messenger RNA expression in normal human Achilles tendon and tendinopathies. Rheumatology (Oxford) 43:969–972.
   PubMed Web of Science ®Google Scholar
• Cawston, T.E., and Wilson, A.J. (2006). Understanding the role of tissue degrading enzymes and their inhibitors in development and disease. Best Pract. Res. Clin. Rheumatol. 20:983–1002.
   PubMed Web of Science ®Google Scholar
• Jones, G.C., Corps, A.N., Pennington, C.J., Clark, I.M., Edwards, D.R., Bradley, M.M., Hazleman, B.L., and Riley, G.P. (2006). Expression profiling of metalloproteinases and tissue inhibitors of metalloproteinases in normal and degenerate human Achilles tendon. Arthritis Rheum. 54:832–842.
   PubMed Web of Science ®Google Scholar
• Ireland, D., Harrall, R., Curry, V., Holloway, G., Hackney, R., Hazleman, B., and Riley, G. (2001). Multiple changes in gene expression in chronic human Achilles tendinopathy. Matrix Biol. 20:159–169.
   PubMed Web of Science ®Google Scholar
• Oshiro, W., Lou, J., Xing, X., Tu, Y., and Manske, P.R. (2003). Flexor tendon healing in the rat: A histologic and gene expression study. J. Hand Surg. Am. 28:814–823.
   PubMedGoogle Scholar
• Tsuzaki, M., Guyton, G., Garrett, W., Archambault, J.M., Herzog, W., Almekinders, L., Bynum, D., Yang, X., and Banes, A.J. (2003). IL-1 beta induces COX2, MMP-1, -3 and -13, ADAMTS-4, IL-1 beta and IL-6 in human tendon cells. J. Orthop. Res. 21:256–264.
   PubMed Web of Science ®Google Scholar
• Clegg, P.D., Strassburg, S., and Smith, R.K. (2007). Cell phenotypic variation in normal and damaged tendons. Int. J. Exp. Pathol. 88:227–235.
   PubMed Web of Science ®Google Scholar
• Lo, I.K., Marchuk, L.L., Hollinshead, R., Hart, D.A., and Frank, C.B. (2004). Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am. J. Sports Med. 32:1223–1229.
   PubMed Web of Science ®Google Scholar
• Nomura, M., Hosaka, Y., Kasashima, Y., Ueda, H., Takehana, K., Kuwano, A., and Arai, K. (2007). Active expression of matrix metalloproteinase-13 mRNA in the granulation tissue of equine superficial digital flexor tendinitis. J. Vet. Med. Sci. 69:637–639.
   PubMed Web of Science ®Google Scholar
• Cunningham, B.A., Hemperly, J.J., Murray, B.A., Prediger, E.A., Brackenbury, R., and Edelman, G.M. (1987). Neural cell adhesion molecule: Structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236:799–806.
   PubMed Web of Science ®Google Scholar
• Oberlender, S.A., and Tuan, R.S. (1994). Spatiotemporal profile of N-cadherin expression in the developing limb mesenchyme. Cell Adhes. Commun. 2:521–537.
   PubMed Web of Science ®Google Scholar
• Derycke, L., De Wever, O., Stove, V., Vanhoecke, B., Delanghe, J., Depypere, H., and Bracke, M. (2006). Soluble N-cadherin in human biological fluids. Int. J. Cancer. 119:2895–2900.
   Google Scholar
• Simons, M., and Horowitz, A. (2001). Syndecan-4-mediated signalling. Cell. Signal. 13:855–862.
   PubMed Web of Science ®Google Scholar
• Jones, P.L., and Jones, F.S. (2000). Tenascin-C in development and disease: Gene regulation and cell function. Matrix Biol. 19:581–596.
   PubMed Web of Science ®Google Scholar
• Riley, G.P., Harrall, R.L., Cawston, T.E., Hazleman, B.L., and Mackie, E.J. (1996). Tenascin-C and human tendon degeneration. Am. J. Pathol. 149:933–943.
   PubMed Web of Science ®Google Scholar
• Jarvinen, T.A., Kannus, P., Jarvinen, T.L., Jozsa, L., Kalimo, H., and Jarvinen, M. (2000). Tenascin-C in the pathobiology and healing process of musculoskeletal tissue injury. Scand. J. Med. Sci. Sports 10:376–382.
   PubMed Web of Science ®Google Scholar
• Jinnin, M., Ihn, H., Asano, Y., Yamane, K., Trojanowska, M., and Tamaki, K. (2004). Tenascin-C upregulation by transforming growth factor-beta in human dermal fibroblasts involves Smad3, Sp1, and Ets1. Oncogene 23:1656–1667.
   PubMed Web of Science ®Google Scholar
• Smith, R.K., Zunino, L., Webbon, P.M., and Heinegard, D. (1997). The distribution of cartilage oligomeric matrix protein (COMP) in tendon and its variation with tendon site, age and load. Matrix Biol. 16:255–271.
   PubMed Web of Science ®Google Scholar
• Chiquet-Ehrismann, R., and Tucker, R.P. (2004). Connective tissues: Signalling by tenascins. Int. J. Biochem. Cell Biol. 36:1085–1089.
   PubMed Web of Science ®Google Scholar
• Halasz, K., Kassner, A., Morgelin, M., and Heinegard, D. (2007). COMP acts as a catalyst in collagen fibrillogenesis. J. Biol. Chem. 282:31166–31173.
   PubMed Web of Science ®Google Scholar
• Mehr, D., Pardubsky, P.D., Martin, J.A., and Buckwalter, J.A. (2000). Tenascin-C in tendon regions subjected to compression. J. Orthop. Res. 18:537–545.
   PubMed Web of Science ®Google Scholar