Examination of intrafascicular muscle fiber terminations: Implications for tension delivery in series-fibered muscles

Young, Miriam; Paul, Angelika C.; Rodda, Judith; Duxson, Marilyn J.; Sheard, Philip W.

doi:10.1002/1097-4687(200008)245:2<130::aid-jmor4>3.0.co;2-r

Cited by 54 publications

(50 citation statements)

References 55 publications

(68 reference statements)

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“…Lateral transmission of force occurs from z-lines to extracellular matrix via costameres and catenincadherin complexes (Young et al, 2000;Paul et al, 2002). Lateral adhesion plaques with dense accumulations of transverse collagen fibrils can be visualized in guinea pig muscles stained for acetylcholinesterase (Young et al, 2000). Similar dense spots of intramuscular acetylcholinesterase, not associated with endplates or myotendinous junctions, are prominent in human muscles (our unpublished observations).…”

Section: Discussionmentioning

confidence: 60%

“…Fibers derived from secondary myotubes in guinea pig sternomastoid muscles terminate intrafascicularly, but fibers derived from primary myotubes run the full length of the muscle (Young et al, 2000). Cat limb muscles also include a small proportion of fibers (ϳ1%) grouped into one or a few slow motor units that run full length and presumably also are derived from primary myotubes (Eldred et al, 1993).…”

Section: Discussionmentioning

confidence: 99%

“…Some force can be transmitted laterally between fibers (Street, 1983;Patel and Lieber, 1997;Huijing, 1999;Huijing and Baan, 2001;Monti et al, 2001). Lateral transmission of force occurs from z-lines to extracellular matrix via costameres and catenincadherin complexes (Young et al, 2000;Paul et al, 2002). Lateral adhesion plaques with dense accumulations of transverse collagen fibrils can be visualized in guinea pig muscles stained for acetylcholinesterase (Young et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

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Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle

Harris¹,

Duxson²,

Butler³

et al. 2005

J. Neurosci.

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The sartorius muscle is the longest muscle in the human body. It is strap-like, up to 600 mm in length, and contains five to seven neurovascular compartments, each with a neuromuscular endplate zone. Some of its fibers terminate intrafascicularly, whereas others may run the full length of the muscle. To assess the location and timing of activation within motor units of this long muscle, we recorded electromyographic potentials from multiple intramuscular electrodes along sartorius muscle during steady voluntary contraction and analyzed their activity with spike-triggered averaging from a needle electrode inserted near the proximal end of the muscle. Approximately 30% of sartorius motor units included muscle fibers that ran the full length of the muscle, conducting action potentials at 3.9 Ϯ 0.1 m/s. Most motor units were innervated within a single muscle endplate zone that was not necessarily near the midpoint of the fiber. As a consequence, action potentials reached the distal end of a unit as late as 100 ms after initiation at an endplate zone. Thus, contractile activity is not synchronized along the length of single sartorius fibers. We postulate that lateral transmission of force from fiber to endomysium and a wide distribution of motor unit endplates along the muscle are critical for the efficient transmission of force from sarcomere to tendon and for the prevention of muscle injury caused by overextension of inactive regions of muscle fibers.

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Section: Discussionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle

Harris¹,

Duxson²,

Butler³

et al. 2005

J. Neurosci.

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“…Intrafascicular fiber terminations (IFTs) are characterized by elaborate folding of the sarcolemma and high expression levels of cell-matrix adhesion molecules, in particular the ␣7␤1 integrins and dystrophin (Young et al, 2000;Paul et al, 2002). From the terminal sarcolemma of the IFT, fibers of the extracellular matrix extend to contact other fibers terminating in a complementary manner to form myomyonal junctions.…”

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confidence: 99%

Development of a mammalian series‐fibered muscle

2004

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This study examines the processes by which multiply innervated, serially fibered mammalian muscles are constructed during development. We previously reported that primary myotubes of such a muscle, the guinea pig sternomastoid muscle, span from tendon to tendon and are innervated at each of the muscle's four innervation zones. Secondary myotubes form later, in association with each point of innervation (Duxson and Sheard, Dev. Dyn., 1995; 204:391-405). We now describe the further growth and development of the muscle. Secondary myotubes initially insert onto and grow along the primary myotube. However, as they reach a critical length, they encounter other secondary myotubes growing from serially adjacent innervation zones and may transfer their attachment(s) to these serially positioned secondary myotubes. Other secondary myotubes maintain attachment at one or both ends to their primary myotube. Thus, an interconnected network of primary and secondary myotubes is formed. Patterns of reactivity for cell adhesion molecules suggest that early attachment points between myotubes are the embryonic precursors of adult myomyonal junctions, characterized by the expression of ␣7B␤1 integrin. Finally, the results show that secondary myotubes positioned near a tendon are generally longer than those lying in the mid belly of the muscle, and we suggest that the environment surrounding the tendinous zone may somehow stimulate myotube growth. Anat Rec Part A 278A: 571-578, 2004.

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“…We have previously described the morphological form of various muscle-to-muscle and muscle-tomatrix junctions which are likely involved in tension transmission within one such muscle -the guinea pig sternomastoid muscle (Young et al 2000). Here, we use immunohistochemistry to investigate the cell adhesion molecules present at these junctions.…”

mentioning

confidence: 99%

Localization of α7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles

Paul

Sheard

Kaufman

et al. 2002

Cell and Tissue Research

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Non-primate mammalian muscles with fascicles above 35 mm in length are composed predominantly of arrays of short, non-spanning muscle fibres, which terminate within the belly of the muscle fascicle at one or both ends. We have previously described the morphological form of various muscle-to-muscle and muscle-to-matrix junctions which are likely involved in tension transmission within one such muscle - the guinea pig sternomastoid muscle (Young et al. 2000). Here, we use immunohistochemistry to investigate the cell adhesion molecules present at these junctions. We find strong immunoreactivity against the alpha 7B integrin subunit and dystrophin, and slight reactivity against the alpha 7A integrin at all intrafascicular fibre terminations (IFTs), as well as at the muscle-tendon junction (MTJ). Tenascin, the sole ligand for alpha 9 beta 1 integrin, was absent from IFTs but present at the MTJ, suggesting the two sites are molecularly distinct. In addition to their expression at junctional sites, alpha 7B integrin and dystrophin were also expressed ubiquitously along the non-junctional sarcolemma, suggesting potential involvement in diffuse lateral transmission of tension between adjacent fibres. We conclude that the distribution of alpha 7 beta 1 integrins and dystrophin in series-fibred muscles suggests they are involved in transmission of tension from intrafascicularly terminating fibres to neighbouring fibres lying both in-series and in-parallel, via the extracellular matrix (ECM).

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Examination of intrafascicular muscle fiber terminations: Implications for tension delivery in series-fibered muscles

Cited by 54 publications

References 55 publications

Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle

Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle

Development of a mammalian series‐fibered muscle

Localization of α7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles

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