Muscle fascia and force transmission

doi:10.1016/j.jbmt.2010.01.005

Journal of Bodywork and Movement Therapies

Volume 14, Issue 4, October 2010, Pages 411-417

https://doi.org/10.1016/j.jbmt.2010.01.005 Get rights and content

Summary

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.

Introduction

The soft connective tissues associated with muscle tissue have been referred to as the intramuscular extracellular matrix (IM-ECM), intramuscular connective tissue (IMCT) and muscle fasciae (MF). Although these general names can be used interchangeably, the term IM-ECM will be used here. Substantial reviews of the structure, development, composition and function of IM-ECM exist (Purslow and Duance, 1990, Purslow, 2002, Purslow, 2008). The mechanisms and pathways by which IM-ECM is remodelled and adapted due to changing functional demands during muscle growth and repair, and in response to exercise training or disuse, are addressed by Kjær and Magnusson (2008). Like most other soft connective tissue structures, the amount and composition of IM-ECM structures are not simply programmed during embryogenesis and subsequent post-natal maturation processes. The amounts and composition of the various IM-ECM structures in living tissue represent a dynamic balance between deposition, growth, remodelling and degradation, which is affected by the interplay between functional demands on the tissue and the mechanical environment. The cellular mechanisms of mechanotransduction in fibroblasts are reviewed by Chiquet et al. (2009). The purpose of the current review is to highlight information pointing to the crucial roles of IM-ECM in force transmission and accommodation of shape changes in functioning muscle.

Section snippets

General structure and biochemical composition of IM-ECM

As schematically shown in Fig. 1, each muscle is surrounded by epimysium, a connective tissue layer that is continuous with the tendons that attach the muscles to the bones. In some long strap-like muscles the epimysium is composed of two parallel sets of wavy collagen fibres in a crossed-ply arrangement, embedded in a proteoglycan matrix (see Fig. 2). When the muscle is at its resting length, the two sets of collagen fibres are arranged at angles of approximately 55° to the long axis of the

IM-ECM changes during muscle development

During embryonic development of intramuscular connective tissue, the amounts of the various collagens and PGs changes (Velleman et al., 1999, Listrat et al., 1999, Lawson and Purslow, 2001). Spatial variations between the endomysium and perimysium within one muscle (Nishimura et al., 1997) and differences in expression of both collagen type I and PG components such as laminin between muscles (Lawson and Purslow, 2001) are both determined early in prenatal development. In bovine muscles, type I

The amounts and composition of endomysium and perimysium vary between functionally different muscles

In fully developed adult animals, there are large differences in the amounts and composition of IM-ECM between different muscles in the body. Histological comparison (see Fig. 4 in Purslow, 2005) illustrates that the continuous perimysial network surrounds or separates fascicles of radically different sizes and shapes in different muscles from the same animal. This difference also results in different thicknesses of perimysial connective tissue. A comparison of the connective tissue content of

Structure and functional roles of the endomysium

As reviewed by Purslow and Duance (1990), each muscle cell is surrounded by its own plasmalemma and basement membrane. Filling the intervening region between the basement membranes of two adjacent muscle cells is the much more substantial reticular layer, which is comprised of a network of collagen fibrils and fibres in a proteoglycan matrix.

The thickness of the endomysium as a whole varies with muscle length, becoming thicker at short muscle lengths and thinner as the muscle is extended (see

Functional anatomy of the perimysium

Two sizes of fascicles and, therefore, two levels of perimysial structure can be distinguished in cross-sections of muscle. Small (primary) fascicles or muscle fibre bundles are delineated by primary perimysium. Groups of primary fascicles are then organised into larger, secondary fascicles by secondary perimysium, which tends to be thicker than primary perimysium. In porcine semitendinosus muscle, the thicker secondary perimysium is in the order of 10 μm thick at birth and increases to approach

Control of turnover of IM-ECM as a possible treatment in muscle injury and repair of fibrosis

Muscle growth, turnover, and repair necessitate remodelling of IM-ECM, principally under the control of matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs (TIMPs). MMPs are expressed by muscle cells as well as by fibroblasts in the IM-ECM (Balcerzak et al., 2001). Adaptation of muscle, including muscle hypertrophy following exercise training is known to involve increased expression of a range of MMPs (Kjaer, 2004). Expression of MMPs is stimulated by mechanical forces, hormones, and

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Fascia PhysiologyMuscle fascia and force transmission

Summary

Introduction

Section snippets

General structure and biochemical composition of IM-ECM

IM-ECM changes during muscle development

The amounts and composition of endomysium and perimysium vary between functionally different muscles

Structure and functional roles of the endomysium

Functional anatomy of the perimysium

Control of turnover of IM-ECM as a possible treatment in muscle injury and repair of fibrosis

Mechanisms of Ageing and Development

Meat Science

Biochimica Biophysica Acta

Journal of Biomechanics

Journal of Biomechanics

Meat Science

Tissue and Cell

Meat Science

International Journal of Biochemistry and Cell Biology

Comparative Biochemistry and Physiology. A Molecular And Integrative Physiology

Meat Science

Tissue and Cell

Poultry Science

Restraining cross-links responsible for the mechanical properties of collagen fibers; natural and artificial

Coordinate expression of matrix-degrading proteinases and their activators and inhibitors in bovine skeletal muscle

Journal of Animal Science

Neurohormonal activation is associated with increased levels of plasma matrix metal loproteinase-2 in human heart failure

European Heart Journal

The elastin content of various muscles of beef animals

Journal of the. Science of Food & Agriculture

ECM remodelling in hypertensive heart disease

Journal of Clinical Investigation

High-resolution analysis of the modified quarter-stagger model of the collagen fibril

Biopolymers

Relationship between development of intramusclular connective tissue and toughness of pork during growth of pigs

Journal of Animal Science

Extracellular matrix profiles in the progression to heart failure

Acta Physiologica

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

Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading

Physiological Reviews

Mechanical adaptation and tissue remodeling

Fascia Physiology
Muscle fascia and force transmission