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Mechanical Adaptation and Tissue Remodeling

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Collagen

Abstract

The adaptive response of connective tissue to mechanical loading includes an increased synthesis and turnover of matrix proteins, including the collagen. Collagen formation and degradation increases with acute loading of tendon and skeletal muscle, in vivo. This increased activity is associated with local and systemic release of growth factors (e.g., IGF-1, TGF-beta, IL-6) that is temporally coupled with a rise in procollagen expression. Chronic loading of tissue, such as with physical training, will lead to increased collagen turnover and a net collagen synthesis which are together associated with a modification of the mechanical properties, including a reduction in tendon stress. Altogether this likely yields a more load-resistant tissue. The adaptation time to chronic loading is longer in tendon tissue compared to contractile elements of skeletal muscle or heart, and it is only with very prolonged loading that significant changes in gross dimensions of the tendon can be observed. Current observations support the notion that mechanical loading leads to collagen-rich tissue adaptation, and that this requires an intimate interplay between mechanical signaling and biochemical changes in the matrix, such that chemical changes can be converted into adaptations in morphology, structure and material properties.

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References

  • Abrahamsson SO (1997). Similar effect of recombinant human insulin-like growth factor-I and II in cellular activities in flexor tendons of young rabbits: experimental studies in vitro. J Orthop Res 15: 256–262.

    Article  Google Scholar 

  • Alexander RM & Bennet-Clark HC (1977). Storage of elastic strain energy in muscle and other tissues. Nature 265: 114–117.

    Article  Google Scholar 

  • Almekinders LC, Vellema JH, & Weinhold PS (2002). Strain patterns in the patellar tendon and the implications for patellar tendinopathy. Knee Surg Sports Traumatol Arthrosc 10: 2–5.

    Article  Google Scholar 

  • Arndt AN, Bruggemann GP, Koebke J, & Segesser B (1999). Asymmetrical loading of the human triceps surae: I. Mediolateral force difference in the Achilles tendon. Foot Ankle Int 20:445–449.

    Google Scholar 

  • Arnoczky SP, Lavagnino M, Whallon JH, & Hoonjan A (2002). In situ cell nucleus deformation in tendons under tensile load; a morphological analysis using confocal laser microscopy. J Orthop Res 20: 29–35.

    Article  Google Scholar 

  • Babraj J, Cuthbertson D, Smith J, Langberg H, Miller BF, Krogsgaard M, Kjær M, & Rennie MJ (2005). Collagen synthesis in human musculoskeletal tissues and skin. Am J Physiol 99: 986–994.

    Article  Google Scholar 

  • Basso O, Amis AA, Race A, & Johnson DP (2002). Patellar tendon fiber strains: their differential responses to quadriceps tension. Clin Orthop 400: 246–253.

    Article  Google Scholar 

  • Biewener AA & Roberts TJ (2000). Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc Sport Sci Rev 28: 99–107.

    Google Scholar 

  • Birch HL, McLaughlin L, Smith RK, & Goodship AE (1999). Treadmill exercise-induced tendon hypertrophy: assessment of tendons with different mechanical functions. Equine Vet J Suppl 30: 222–226.

    Google Scholar 

  • Bojsen-Moller J, Hansen P, Aagaard P, Svantesson U, Kjær M, & Magnusson SP (2004). Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. J Appl Physiol 97: 1908–1914.

    Article  Google Scholar 

  • Bojsen-Moller J, Kalliokoski KK, Seppanen M, Kjær M, & Magnusson SP (2006). Low-intensity tensile loading increases intratendinous glucose uptake in the Achilles tendon. J Appl Physiol 101: 196–201.

    Article  Google Scholar 

  • Buchanan CI & Marsh RL (2001). Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J Appl Physiol 90: 164–171.

    Google Scholar 

  • Chong, AK, et al. (2007). Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit Achilles tendon model. J Bone Joint Surg Am, 89: 74–81.

    Article  Google Scholar 

  • Crameri R, Langberg H, Jensen CH, Teisner B, Schrøder HD, & Kjær M (2004a). Activation of satellite cells in human skeletal muscle after a single bout of exercise. J Physiol 558:333–340.

    Article  Google Scholar 

  • Crameri R, Langberg H, Teisner B, Magnusson P, Olesen JL, Koskinen S, Suetta C, & Kjær M (2004b). Synchronous disruption of the extracellular matrix and mechanical tenderness in skeletal muscle after a single bout of eccentric loading in humans. Matrix Biol 23:259–264.

    Article  Google Scholar 

  • Crameri R, Aaagaard P, Qvortrup K, Langberg H, Olesen JL, & Kjær M (2007). Myofibre damage in human skeletal muscle: Effects of electrical stimulation vs voluntary contraction. J Physiol 583: 365–380.

    Article  Google Scholar 

  • Cresswell AG, Loscher WN, & Thorstensson A (1995). Influence of gastrocnemius muscle length on triceps surae torque development and electromyographic activity in man. Exp Brain Res 105: 283–290.

    Article  Google Scholar 

  • DeBoer J, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, & Rennie MJ (2007). The temporal response of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585: 241–251.

    Article  Google Scholar 

  • DeMos, M et al. (2007). Intrinsic differentiation potential of adolescent human tendon tissue: an in-vitro cell differentiation study. BMC Musculoskelet Disord, 8: 16–22.

    Article  Google Scholar 

  • Døssing S & Kjær M (2005). Growth hormone and connective tissue in exercise. Scand. J Med Sci Sports 15: 202–210.

    Article  Google Scholar 

  • Finni T, Hodgson JA, Lai AM, Edgerton VR, & Sinha S (2003). Nonuniform strain of human soleus aponeurosis-tendon complex during submaximal voluntary contractions in vivo. J Appl Physiol 95: 829–837.

    Google Scholar 

  • Fukashiro S, Itoh M, Ichinose Y, Kawakami Y, & Fukunaga T (1995). Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo. Eur J Appl Physiol 71: 555–557.

    Article  Google Scholar 

  • Goldspink G (2006). Impairment of IGF-I gene splicing and MGF expression associated with muscle wasting. Int J Biochem Cell Biol 38: 481–489.

    Article  Google Scholar 

  • Hansen P, Aagaard P, Kjær M, Larsson B, & Magnusson SP (2003). The effect of habitual running on human Achilles tendon load-deformation properties and cross-sectional area. J Appl Physiol 95: 2375–2380.

    Google Scholar 

  • Hansen P, Bojsen-Moller J, Aagaard P, Kjær M, & Magnusson SP (2006). Mechanical properties of the human patellar tendon, in vivo. Clin Biomech 21: 54–58.

    Article  Google Scholar 

  • Haraldsson BT, Aagaard P, Krogsgaard M, Alkjaer T, Kjær M, & Magnusson SP (2005). Region-specific mechanical properties of the human patella tendon. J Appl Physiol 98: 1006–1012.

    Article  Google Scholar 

  • Haraldsson BT, Aagard P, Qvortrup K, Bojsen-Moller J, Krogsgaard M, Koskinen S, Kjaer M, Magnusson SP (2008). Lateral force transmission between human tendon fascicles. Matrix Biol. 27:86–95.

    Article  Google Scholar 

  • Heinemeier K, Langberg H, Olesen JL, & Kjær M (2003) Role of transforming growth factor beta in relation to exercise induced type I collagen synthesis in human tendinous tissue. J Appl Physiol 95: 2390–2397.

    Google Scholar 

  • Heinemeier KM, Olesen JL, Schjerling P, Haddad F, Langberg H, Baldwin KM, & Kjær M (2007a). Short term strength training and the expression of myostatin- and IGF-I isoforms in rat muscle and tendon: Differential effects of specific contraction types. J Appl Physiol 102: 573–581.

    Article  Google Scholar 

  • Heinemeier KM, Olesen JL, Haddad F, Langberg H, Kjær M, Baldwin KM, & Schjerling P (2007b). Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J Physiol 582: 1303–1316.

    Article  Google Scholar 

  • Huijing PA & Jaspers RT (2005). Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand J Med Sci Sports 15: 349–380.

    Article  Google Scholar 

  • Johnson DP, Wakeley CJ, & Watt I (1996). Magnetic resonance imaging of patellar tendonitis. J Bone Joint Surg – Br 78: 452–457.

    Google Scholar 

  • Kadi F, Charifi N, Denis C, Lexell J, Andersern JL, Schjerling P, Olsen S, & Kjær M (2005). The behaviour of satellite cells in response to exercise: What have we learned from human studies? Pfügers Arch 451: 319–327.

    Article  Google Scholar 

  • Kajikawa, Y et al. (2007). GFP chimeric models exhibited a biphasic pattern of mesenchymal cell invasion in tendon healing. J Cell Physiol 210: 684–691.

    Article  Google Scholar 

  • Kannus P & Jozsa L (1991). Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg [Am] 73: 1507–1525.

    Google Scholar 

  • Kastelic J, Galeski A, & Baer E (1978). The multicomposite structure of tendon. Connect Tissue Res 6: 11–23.

    Article  Google Scholar 

  • Kjær M (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84: 649–698.

    Article  Google Scholar 

  • Kongsgaard M, Aagaard P, Kjær M, & Magnusson SP (2005). Structural Achilles tendon properties in athletes subjected to different exercise modes and in Achilles tendon rupture patients. J Appl Physiol 99: 1965–1971.

    Article  Google Scholar 

  • Kongsgaard M, Reitelseder S, Pedersen TG, Holm L, Aagaard P, Kjær M, & Magnusson SP (2007). Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol 191: 111–112.

    Article  Google Scholar 

  • Koskinen SO, Heinemeier KM, Olesen JL, Langberg H, & Kjær M (2004). Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon related connective tissue. J Appl Physiol 96: 861–864.

    Article  Google Scholar 

  • Kovanen V (1989). Effects of ageing and physical training on rat skeletal muscle. Acta Physiol Scand 135 suppl 577: 1–56.

    Google Scholar 

  • Kurtz CA, Loebig TG, Anderson DD, Demeo PJ & Cambell PG (1999). Insulin-like growth factor I accelerates functional recovery from Achilles tendon injury in a rat model. Am J Sports Med 27: 363–369.

    Google Scholar 

  • Langberg H, Skovgaard D, Bülow J, & Kjær M (2000). Time pattern of exercise-induced changes in type-I collagen turnover after prolonged endurance exercise in humans. Calcif Tissue Int 67: 41–44.

    Article  Google Scholar 

  • Langberg, H., Rosendal L, & Kjær M (2001). Training induced changes in peritendinous type I collagen turnover determined by microdialysis in humans. J Physiol 534:297–302.

    Article  Google Scholar 

  • Langberg H, Ellingsgaard H, Madsen T, Jansson J, Magnusson SP, Aagaard P, & Kjær M (2007). Eccentric rehabilitation exercise increases peritendinous type I collagen synthesis in humans with Achilles tendinosis. Scand J Med Sci Sports 17: 61–66.

    Google Scholar 

  • Langberg H, Skovgaard D, Petersen LJ, Bulow J, & Kjær M (1999). Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans. J Physiol 521 Pt 1: 299–306.

    Google Scholar 

  • Lange, KH, Andersen JL, Beyer N, Isaksson F, Larsson B, Rasmussen MH, Juul A, Bülow J, & Kjær M (2002). GH administration changes myosin heavy chain isoforms in skeletal muscle but does not augment muscle strength or hypertrophy, either alone or combined with resistance exercise training in healthy elderly men. J Clin Endocrinol Metab 87: 513–523.

    Article  Google Scholar 

  • Laurent GJ (1987). Dynamic state of collagen pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am J Physiol 252: C1–C9.

    Google Scholar 

  • Leask A, Holmes A, & Abraham DJ (2002). Connective tissue growth factor: a new and important player in the pathogenesis of fibrosis. Curr Rheumatol Rep 4: 136–142.

    Article  Google Scholar 

  • Lindahl GE, Chambers RC, Papakrivopoulou J, Dawson SJ, Jacobsen MC, Bishop JE, & Laurent GJ (2002). Activation of fibroblast procollagen alpha I(I) transcription by mechanical strain is transforming growth factor beta dependent and involves increased binding of CCAAT-binding factor (CBF/NF-y) at the proximal promotor. J Biol Chem 277: 6153–6161.

    Article  Google Scholar 

  • Liu SH, Shaikh R, Panossian V, Yang RS, Nelson SD, Soleiman N, Finerman GA, & Lane JM (1996). Primary immunolocalization of estrogen and progesterone target cells in the human anterior cruciate ligament. J Orthop Res 14: 526–533.

    Article  Google Scholar 

  • Longobardi S, Keay N, Ehrnborg C, Cittadini A, Rosen T, Dall R, Boroujerdi MA, Bassett EE, Healy ML, Pentecost C, Wallace JD, Powrie J, Jorgensen JO, & Sacca L (2000). Growth hormone (GH) effects on bone and collagen turnover in healthy adults and its potential as a marker of GH abuse in sports: a double blind, placebo-controlled study. The GH-2000 Study Group. J Clin Endocrinol Metab 85: 1505–1512.

    Article  Google Scholar 

  • Maffulli N, Waterston SW, Squair J, Reaper J, & Douglas AS (1999). Changing incidence of Achilles tendon rupture in Scotland: a 15-year study. Clin J Sport Med 9: 157–160.

    Article  Google Scholar 

  • Maganaris CN & Paul JP (1999). In vivo human tendon mechanical properties. J Physiol (Lond) 521: 307–313.

    Article  Google Scholar 

  • Magnusson SP, Hansen P, Aagaard P, Brond J, Dyhre-Poulsen P, Bojsen-Moller J, & Kjær M (2003). Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol Scand 177: 185–195.

    Article  Google Scholar 

  • Magnusson SP & Kjær M (2003). Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. Eur J Appl Physiol 90: 549–553.

    Article  Google Scholar 

  • Magnusson SP, Qvortrup K, Larsen JO, Rosager S, Hanson P, Aagaard P, Krogsgaard M, & Kjær M (2002). Collagen fibril size and crimp morphology in ruptured and intact Achilles tendons. Matrix Biol 21: 369–377.

    Article  Google Scholar 

  • Miller B, Olesen JL, Hansen M, Døssing S, Crameri R, Welling RJ, Langberg H, Flyvbjerg A, Kjær M, Babraj J, Smith K, & Rennie MJ (2005). Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567:1021–1033.

    Article  Google Scholar 

  • Miller B, Hansen M, Olesen JL, Flyvbjerg A, Schwarz P, Babraj JA, Smith K, Rennie MJ, & Kjær M (2006a). No effect of menstrual cycle on myofibrillar and connective tissue synthesis in contracting skeletal muscle. Am J Physiol 290: E163–E168.

    Google Scholar 

  • Miller BF, Hansen M, Olesen JL, Schwarz P, Babraj JA, Smith K, Rennie MJ, & Kjær M (2006b). Tendon collagen synthesis at rest and after exercise in women. J Appl Physiol 102:541–546.

    Article  Google Scholar 

  • Mosler E, Folkhard W, Knorzer E, Nemetschek-Gansler H, Nemetschek T, & Koch MH (1985). Stress-induced molecular rearrangement in tendon collagen. J Mol Biol 182: 589–596.

    Article  Google Scholar 

  • Olesen JL, Heinemeier KM, Langberg H, Magnusson SP, Kjær M, & Flyvbjerg A (2006). Expression, content and localization of IGF-1 in human Achilles tendon. Conn Tissue Res 47:200–206.

    Article  Google Scholar 

  • Olesen, JL, Langberg H, Heinemeier K, Flyvbjerg A, & Kjær M (2007a). Exercise-dependent IGF-I, IGFBPs, and type I collagen changes in human peritendinous connective tissue determined by microdialysis. J Appl Physiol 102:. 214–220.

    Article  Google Scholar 

  • Olesen JL, Heinemeier KM, Haddad F, Langberg H, Flyvbjerg A, Kjær M, & Baldwin KM (2007b). Expression of insulin-like growth factor I, insulin-like growth factor binding proteins, and collagen mRNA in mechanically loaded plantaris tendon. J Appl Physiol 101:183–188.

    Article  Google Scholar 

  • Parry DA, Barnes GR, & Craig AS (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.

    Article  Google Scholar 

  • Patterson-Kane JC, Wilson AM, Firth EC, Parry DA, & Goodship AE (1997). Comparison of collagen fibril populations in the superficial digital flexor tendons of exercised and nonexercised thoroughbreds. Equine Vet J 29: 121–125 [published erratum appears in Equine Vet J 1998 Mar; 30(2):176].

    Article  Google Scholar 

  • Puxkandl R, Zizak I, Paris O, Keckes J, Tesch W, Bernstorff S, Purslow P, & Fratzl P (2002). Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc Lond B Biol Sci 357: 191–197.

    Article  Google Scholar 

  • Redaelli A, Vesentini S, Soncini M, Vena P, Mantero S, & Montevecchi FM (2003). Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons – a computational study from molecular to microstructural level. J Biomech 36: 1555–1569.

    Article  Google Scholar 

  • Reeves ND, Maganaris CN, & Narici MV (2003). Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol 548: 971–981.

    Article  Google Scholar 

  • Riley, GP et al. (2002) Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol 21: 185–195.

    Article  Google Scholar 

  • Rosager S, Aagaard P, Dyhre-Poulsen P, Neergaard K, Kjær M, & Magnusson SP (2002). Load-displacement properties of the human triceps surae aponeurosis and tendon in runners and non-runners. Scand J Med Sci Sports 12: 90–98.

    Article  Google Scholar 

  • Sasaki N & Odajima S (1996). Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. J Biomech 29: 1131–1136.

    Article  Google Scholar 

  • Sciore P, Frank CB, & Hart DA (1998). Identification of sex hormone receptors in human and rabbit ligaments of the knee by reverse transcription-polymerase chain reaction: evidence that receptors are present in tissue from both male and female subjects. J Orthop Res 16: 604–610.

    Article  Google Scholar 

  • Scott JE (2003). Elasticity in extracellular matrix ’shape modules’ of tendon, cartilage, etc. A sliding proteoglycan-filament model. J Physiol 553: 335–343.

    Article  Google Scholar 

  • Skutek M, Van Griensven M, Zeichen J, Brauer N, & Bosch U (2001). Cyclic mechanical stretching modulates secretion pattern of growth factors in human fibroblasts. Eur J Appl Physiol 86: 48–52.

    Article  Google Scholar 

  • Smith, RK & Webbon PM (2005). Harnessing the stem cell for the treatment of tendon injuries: heralding a new dawn? Br J Sports Med 39: 582–584.

    Article  Google Scholar 

  • Street SF (1983). Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114: 346–364.

    Article  Google Scholar 

  • Sykova, E. & Jendelova P (2007). Migration, fate and in vivo imaging of adult stem cells in the CNS. Cell Death Differ 14: 1336–1342.

    Article  Google Scholar 

  • Thompson JI & Czernuszka JT (1995). The effect of two types of cross-linking on some mechanical properties of collagen. Biomed Mater Eng 5: 37–48.

    Google Scholar 

  • Vesentini S, Redaelli A, & Montevecchi FM (2005). Estimation of the binding force of the collagen molecule-decorin core protein complex in collagen fibril. J Biomech 38: 433–443.

    Article  Google Scholar 

  • Westh E, Kongsgaard M, Bojsen-Moller J, Aagaard P, Hansen M, Kjær M, & Magnusson SP (2007). Effect of habitual exercise on the structural and mechanical properties of human tendon, in vivo, in men and women. Scand J Med Sci Sports.

    Google Scholar 

  • Wilson VJ, Rattray M, Tomas CR, Moreland BH, & Schulster D (1995). Growth hormone increases IGF-I, collagen type I and collagen II gene expression in dwarf rat skeletal muscle. Mol Cell Endocrinol 115: 187–197.

    Article  Google Scholar 

  • Woo SL, Gomez MA, Woo YK, & Akeson WH (1982). Mechanical properties of tendon and ligaments. The relationship of immobilization and exercise on tissue remodeling. Biorheology 19: 397–408.

    Google Scholar 

  • Yu WD, Panossian V, Hatch JD, Liu SH & Finerman GA (2001). Combined effects of estrogen and progesterone on the anterior cruciate ligament. Clin Orthop 21: 268–281.

    Google Scholar 

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Kjær, M., Magnusson, S. (2008). Mechanical Adaptation and Tissue Remodeling. In: Fratzl, P. (eds) Collagen. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-73906-9_9

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