Muscle fascia and force transmission
2010, Journal of Bodywork and Movement Therapies
https://doi.org/10.1016/J.JBMT.2010.01.005Abstract
This paper reviews the major intramuscular extracellular matrix (IM-ECM) structures (endomysium, perimysium and epimysium) and their possible mechanical contributions to muscle functions. The endomysium appears to provide an efficient mechanism for transmission of contractile forces from adjacent muscle fibres within fascicles. This coordinates forces and deformations within the fascicle, protects damaged areas of fibres against over-extension, and provides a mechanism whereby myofibrils can be interrupted to add new sarcomeres during muscle growth without loss of contractile functionality of the whole column. Good experimental evidence shows that perimysium and epimysium are capable in some circumstances to act as pathways for myofascial force transmission. However, an alternative role for perimysium is reviewed, which involves the definition of slip planes between muscle fascicles which can slide past each other to allow large shear displacements due to shape changes in the whole muscle during contraction. As IM-ECM is continually remodelled so as to be mechanically adapted for its roles in developing and growing muscles, control of the processes governing IM-ECM turnover and repair may be an important avenue to explore in the reduction of fibrosis following muscle injury.
References (49)
- Avery, N.C., Bailey, A.J., 2008. Restraining cross-links responsible for the mechanical properties of collagen fibers; natural and artificial. In: Fratzl, P. (Ed.), Collagen: Structure and Mechanics. Springer, NY, pp. 81e110 (Chapter 4).
- Bailey, A.J., Paul, R.G., Knott, L., 1998. Mechanisms of maturation and ageing of collagen. Mechanisms of Ageing and Development 106, 1e56.
- Balcerzak, D., Querengesser, L., Dixon, W.T., Baracos, V.E., 2001. Coordinate expression of matrix-degrading proteinases and their activators and inhibitors in bovine skeletal muscle. Journal of Animal Science 79, 94e107.
- Banfi, C., Cavalca, V., Veglia, F., Brioschi, M., Barcella, S., Mussoni, L., Boccotti, L., Tremoli, E., Biglioli, P., Agostoni, P., 2005. Neurohormonal activation is associated with increased levels of plasma matrix metal loproteinase-2 in human heart failure. European Heart Journal 26, 481e488.
- Bendall, J.R., 1967. The elastin content of various muscles of beef animals. Journal of the. Science of Food & Agriculture 18, 553e558.
- Berk, B.C., Fujiwara, K., Lehoux, S., 2007. ECM remodelling in hypertensive heart disease. Journal of Clinical Investigation 117, 568e575.
- Brooks, J.C., Savell, J.W., 2004. Perimysium thickness as an indi- cator of beef tenderness. Meat Science 67, 329e334.
- Bruns, R.R., Gross, J., 1973. High-resolution analysis of the modi- fied quarter-stagger model of the collagen fibril. Biopolymers 13, 931e994.
- Chiquet, M., Gelman, L., Lutz, R., Maier, S., 2009. From mecha- notransduction to extracellular matrix gene expression in fibroblasts. Biochimica Biophysica Acta 1793, 911e920.
- Fang, S.H., Nishimura, T., Takahashi, K., 1999. Relationship between development of intramusclular connective tissue and toughness of pork during growth of pigs. Journal of Animal Science 77, 120e130.
- Gans, C., Gaunt, A.S., 1991. Muscle architecture in relation to function. Journal of Biomechanics 24, 53e65.
- Graham, H.K., Horn, M., Trafford, A.W., 2008. Extracellular matrix profiles in the progression to heart failure. Acta Physiologica 194, 3e23.
- Huijing, P.A., 2009. Epimuscular myofascial force transmission: a historical review and implications for new research. Interna- tional society of biomechanics Muybridge award lecture, Taipei, 2007. Journal of Biomechanics 42, 9e21.
- Johansson, N., Alaho, R., Uitto, V.J., Gre ´nman, R., Fusenig, N.E., Lo ´pez-Otin, C., Ka ¨ha ¨ri, V.M., 2000. Expression of collagenase-3 (MMP-13) and collagenase-1 (MMP-1) by transformed keratinocytes is dependent on the activity of p38 mitogen-activated protein kinase. Journal of Cell Science 113, 227e235.
- Kjaer, M., 2004. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiological Reviews 84, 649e698.
- Kjaer, M., Magnusson, S.P., 2008. Mechanical adaptation and tissue remodeling. In: Fratzl, P. (Ed.), Collagen: Structure and Mechanics. Springer, NY, pp. 249e267 (Chapter 9).
- Lawson, M.A., Purslow, P.P., 2001. Development of components of the extracellular matrix, basal lamina and sarcomere in chick quadriceps and pectoralis muscles. British Poultry Science 42, 315e320.
- Lewis, G.J., Purslow, P.P., 1989. The strength and stiffness of perimysial connective-tissue isolated from cooked beef muscle. Meat Science 26, 255e269.
- Listrat, A., Picard, B., Geay, Y., 1999. Age-related changes and location of type I, III, IV, V and VI collagens during development of four foetal skeletal muscles of double muscles and normal bovine muscles. Tissue and Cell 31, 17e27.
- Listrat, A., Lethias, C., Hocquette, J.F., Renand, G., Menissier, F., Geay, Y., Picard, B., 2000. Age related changes and location of types I, III, XII and XIV collagen during development of skeletal muscles from genetically different animals. Histochemical Journal 32, 349e356.
- Liu, A., Nishimura, T., Takahashi, K., 1995. Structural weakening of intramuscular connective tissue during post-mortem ageing of chicken semitendinosus muscle. Meat Science 39, 135e142.
- Magid, A., Law, D.J., 1985. Myofibrils bear most of the resting tension in frog skeletal muscle. Science 230, 1280e1282.
- Navegantes, L.C.C., Migliorini, R.H., Kettelhut, I.C., 2002. Adren- ergic control of protein metabolism in skeletal muscle. Current Opinion in Clinical Nutrition and Metabolic Care 5, 281e286.
- Navegantes, L.C.C., Baviera, A.M., Kettelhut, I.C., 2009. The inhibitory role of sympathetic nervous system in the Ca 2þ - dependent proteolysis of skeletal muscle. Brazilian Journal of Medical and Biological Research 42, 21e28.
- Nishimura, T., Hattori, A., Takahashi, K., 1994. Ultrastructure of the intramuscular connective tissue in bovine skeletal muscle. Acta Anatomica 151, 250e257.
- Nishimura, T., Hattori, A., Takahashi, K., 1995. Structural weak- ening of intramuscular connective tissue during post mortem ageing of beef. Journal of Animal Science 76, 528e532.
- Nishimura, T., Ojima, K., Hattori, A., Takahashi, K., 1997. Devel- opmental expression of extracellular matrix components in intramuscular connective tissue of bovine semitendinosus muscle. Histochemistry and Cell Biology 107, 215e221.
- Ohtani, O., Ushiki, T., Taguchi, T., Kikuta, A., 1988. Collagen fibrillar networks as skeletal frameworks e a demonstration by cell-maceration scanning electron-microscope method. Archives Of Histology and Cytology 51, 249e261.
- Paul, R.G., Bailey, A.J., 1996. Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. International Journal of Biochemistry and Cell Biology 28, 1297e1310.
- Podolsky, R.J., 1964. The maximum sarcomere length for contraction of isolated myofibrils. Journal of Physiology 170, 110e123.
- Purslow, P.P., 1989. Strain-induced reorientation of an intramus- cular connective tissue network: implications for passive muscle elasticity. Journal of Biomechanics 22, 21e23.
- Purslow P.P., 1999. The intramuscular connective tissue matrix and cell-matrix interactions in relation to meat toughness. Proceedings of the 45th Interantional Congress of Meat Science and Technology, Yokohama, Japan, pp. 210e219.
- Purslow, P.P., 2002. The structure and functional significance of variations in the connective tissue within muscle. Comparative Biochemistry and Physiology. A Molecular And Integrative Physiology 133, 947e966.
- Purslow, P.P., 2005. Intramuscular connective tissue and its role in meat quality. Meat Science 70, 435e447.
- Purslow, P.P., 2008. The extracellular matrix of skeletal and cardiac muscle. In: Fratzl, P. (Ed.), Collagen: Structure and Mechanics. Springer, NY, pp. 325e358 (Chapter 12).
- Purslow, P.P., Duance, V.C., 1990. The structure and function of intramuscular connective tissue. In: Hukins, D.W.L. (Ed.), Connective Tissue Matrix, vol. 2. MacMillan, pp. 127e166.
- Purslow, P.P., Trotter, J.A., 1994. The morphology and mechanical properties of endomysium in series-fibred muscles; variations with muscle length. Journal of Muscle Research and Cell Motility 15, 299e304.
- Rowe, R.W.D., 1981. Morphology of perimysial and endomysial connective tissue in skeletal muscle. Tissue and Cell 13, 681e690.
- Schmalbruch, H., 1985. Skeletal Muscle. Springer, Berlin.
- Scott, J.E., 1990. Proteoglycan: collagen interactions and subfibrillar structure in collagen fibrils. Implications in the development and ageing of connective tissues. Journal of Anatomy 169, 23e35.
- Shen, Q.W., Du, M., 2005. Role of AMP-activated protein kinase in the glycolysis of postmortem muscle. Journal of the Science of Food and Agriculture 85, 2401e2406.
- Swatland, H.J., 1975. Morphology and development of connective tissue in porcine and bovine muscle. Journal of Animal Science 41, 78e86.
- Trotter, J.A., 1993. Functional morphology of force transmission in skeletal muscle. Acta Anatomica 146, 205e222.
- Trotter, J.A., Purslow, P.P., 1992. Functional morphology of the endomysium in series fibered muscles. Journal of Morphology 212, 109e122.
- Trotter, J.A., Richmond, F.J.R., Purslow, P.P., 1995. Functional morphology and motor control of series fibred muscles. In: Holloszy, J.O. (Ed.), Exercise and Sports Sciences Reviews, vol. 23. Williams and Watkins, Baltimore, pp. 167e213.
- Tsang, M.Y.C., Rabkin, E.W., 2009. p38 Mitogen-activated protein kinase (MAPK) is activated by noradrenaline and serves a car- dioprotective role, whereas adrenaline induces p38 MAPK dephosphorylation. Clinical and Experimental Pharmacology and Physiology 36, e12ee19.
- Velleman, S.G., Liu, X.S., Eggen, K.H., Nestor, K.E., 1999. Devel- opmental downregulation of proteoglycan synthesis and decorin expression during turkey embryonic skeletal muscle formation. Poultry Science 78, 1619e1626.
- Villareal, F.J., Kim, N.N., 1997. Regulation of myocardial extra- cellular matrix components by mechanical and chemical growth factors. Cardiovascular Pathology 7, 145e151.
- Yamaguchi, J., Nagao, M., Kasziro, Y., Itoh, H., 1997. Activation of p38 mitogen-activated protein kinase by signalling through G protein-coupled receptors. Journal of Biological Chemistry 272, 27771e27777.