Development of neuromuscular junctions in rat embryos

Dennis, Michael; Ziskind-Conhaim, Lea; Harris, AJ

doi:10.1016/0012-1606(81)90290-6

Cited by 295 publications

(149 citation statements)

References 36 publications

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“…The early strikingly different expressions of slow MHC in primary myotubes between both portions could be neurally regulated since primary myotubes have been shown to be functionally innervated within hours of their formation (Dennis et al, 1981). This is consistent with the fact that primary myotubes are innervated before 45 dg in the pig ST muscle (Beermann et al, 1978).…”

Section: Discussion Primary Myotubes Expressed Slow Mhc In the Deep Msupporting

confidence: 67%

Pattern of muscle fiber type formation in the pig

Lefaucheur¹,

Edom

Ecolan³

et al. 1995

Developmental Dynamics

141

120

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The aim of this study was to analyze the temporal sequence of expression of the myosin isoforms in the populations of muscle fibers in the pig and to bring more information on the origin of the strikingly different pattern of fiber composition and distribution between the deep medial red (oxido-glycolytic) and superficial white (glycolytic) portions of semitendinosus (ST) muscle. Muscle samples were taken from 49-, 55-, 75-, 90-, 103-, and 113-(birth) day-old fetuses, from 6-, 11-, 21-, 35-, 50-, and 80-day-old piglets, and from a 3-year-old pig. Our results confirm the sequential formation of primary and secondary generation fibers. The use of immunohistochemistry and heterologous monoclonal antibodies (mAb) directed against specific myosin heavy chain (MHC) isoforms revealed a different pattern of gene expression between the two portions of the ST muscle for both generations of fibers. By 75 days of gestation (dg), primary myotubes from the deep medial portion stained positively for the anti-slow MHC mAb and negatively for the adult anti-fast MHC, whereas the opposite was observed in the superficial portion. Secondary fibers never expressed slow MHC until late gestation. Instead, they expressed an adult fast MHC isoform as soon as they formed in the deep medial portion and later on in the superficial portion. From late gestation to the first 3 postnatal weeks, slow MHC began to be expressed in a subpopulation of secondary fibers. These fibers were in the direct vicinity of primary myotubes in the deep medial portion, whereas their location could not be established in the superficial portion. The remaining secondary fibers matured to type IIA in the direct vicinity of these type I fibers and to type IIB at the periphery of the islets. In both portions of the muscle, a subpopulation of secondary fibers, the first ones to express slow MHC, also transitorily expressed a MHC that was identical or closely related to the a-cardiac MHC during the early postnatal period. A third generation of small diameter fibers was observed shortly after birth and reacted with the anti-fetal MHC mAb; their destiny remains to be established. The present work reveals a remarkable pattern of MHC gene expression in the pig and raises many questions on the real nature of these isoforms. In order to answer these questions, we have undertaken to make a cDNA library of pig skeletal muscle and to screen 0 1995 WILEY-LISS, INC.this library with the same mAbs used in the present study. o 1995 Wiley-Liss, Inc.

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Section: Discussion Primary Myotubes Expressed Slow Mhc In the Deep Msupporting

confidence: 67%

Pattern of muscle fiber type formation in the pig

Lefaucheur¹,

Edom

Ecolan³

et al. 1995

Developmental Dynamics

141

120

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“…If the key to myoblast fusion or to induction of the preconditions for fusion is calcium ion influx, this can be induced in a number of ways other than by neural activation of AChR. Embryonic muscles are highly susceptible to stretch-induced depolarization (Dennis et al, 1981), and denervated muscles to fasciculation resulting from spontaneous depolarization, both of which result in calcium influx into the affected cells. Such spontaneous depolarizations of aneural embryonic muscles would be expected to affect the primary myotubes, and also myoblasts which were postmitotic, extended along the longitudinal muscle axis, and in the early stages of differentiation.…”

Section: Discussion Secondary Myotubes Form Only At Sites Of Innervationmentioning

confidence: 99%

Formation of new myotubes occurs exclusively at the multiple innervation zones of an embryonic large muscle

Duxson

Sheard

1995

Developmental Dynamics

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This work examines the general principle of whether production of embryonic muscle fibres is invariably linked to sites of innervation, as we have previously reported in small rodent muscles (Duxson et al. 119891 Development 1OE74.3-750). The experimental strategy has been to make a detailed electron microscopic analysis of the formation of new myotubes in a large muscle having multiple, discrete innervation zones. The particular model system is the guinea pig sternomastoid muscle, a strap-like, parallel-fibred muscle with four distinct endplate bands, both in the embryo and the adult. Primary myotubes in the developing muscle extended from tendon to tendon of the muscle and were innervated at each of the multiple endplate zones. Each point of innervation of the primary myotubes was a focus around which many new secondary myotubes formed, and each secondary myotube was approximately centred on one of the innervation sites of its supporting primary myotube. This confirms our previous report, in rat IVth lumbrical muscle, of an invariable association between sites of formation of new secondary myotubes and sites of innervation. We suggest that, in vivo, nerve terminals either directly induce the initial myoblast fusions which give rise to new secondary myotubes, or induce some precondition for fusion. An alternative hypothesis is that a common patterning influence in the muscle localizes both innervation and secondary myotube formation to the same zone. The pattern of secondary myotube production in the embryo has important implications for the size and final architecture of muscles in larger animals, and some of these are discussed. o 1995 Wiley-Liss, Inc.

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“…Thus, our measurements at P7 might reflect a stage of synapse elimination that normally occurs prenatally in other muscles. However, it is also possible that some of this apparent overlap at P7 could be due to electrical coupling among developing muscle fibers (Dennis et al, 1981), which would cause our estimates of motor unit size to be spuriously large. Nonetheless, the finding that motor unit size but not number decreases during the period when multiaxonal innervation is eliminated in the LA muscle (Jordan et al, 1988) indicates that synapse elimination in the LA involves an elimination of axon terminals from d@rent motoneurons, as has been described in numerous other rat muscles (Redfern, 1970;Brown et al, 1976;Rosenthal and Taraskevich, 1977;Betz et al, 1979;Dennis et al, 198 1;Lavidis, 1984b, Balice-Gordon andThompson, 1988).…”

Section: Control Of Motor Unit Size During Developmentmentioning

confidence: 99%

Hormonal regulation of motor unit size and synaptic strength during synapse elimination in the rat levator ani muscle

et al. 1992

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Previous anatomical studies suggest that androgen regulates synapse elimination in the androgen-sensitive levator ani(LA) muscle of the rat. Androgen treatment beginning on postnatal day 7 (P7) prevents some of the normal loss of multiaxonal innervation in this muscle. The present study used physiological techniques to measure the number and size of LA motor units during the synapse elimination period in muscles from normals, and castrates treated with either testosterone propionate or oil. The number of increments in LA twitch tension as nerve stimulation intensity increased, a measure of the number of motor units, was the same at the end (P28) of synapse elimination as near the beginning (P7) of this process. This result indicates that motoneuronal cell death does not contribute to synapse elimination in the LA. Moreover, androgen during this period did not influence the number of LA motor units. In contrast, between P7 and P28, there was a dramatic decline in the size of LA motor units, as indicated by a decrease in the percentage of twitch or tetanus tension of individual motor units relative to the maximal twitch or tetanus tension of the whole muscle. In addition, androgen treatment of castrated males during this period prevented some of the normal decline in the size of LA motor units. Estimates of the number of inputs per LA muscle fiber derived from the number of LA motor units and their average size indicate that androgen maintains polyneuronal innervation in the LA muscle. This finding supports previous anatomical studies suggesting that androgen can prevent synapse elimination in this muscle. The strength of LA synapses was also examined by measuring the tetanus: twitch ratio of individual motor units and by measuring the safety margin of LA synapses. Both measurements indicated that the average strength of LA synapses increases during synapse elimination. Moreover, androgen appeared to spare synapses from elimination without increasing their strength, since androgen-treated muscles generally had larger motor units but the same mean tetanus:twitch ratio and safety margins as untreated LA muscles except at P28, when synapses in androgen-treated LA muscles had appreciably lower safety margins than normal. These results suggest that androgen regulates synapse elimination through a mechanism(s) independent of synaptic strength.

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Development of neuromuscular junctions in rat embryos

Cited by 295 publications

References 36 publications

Pattern of muscle fiber type formation in the pig

Pattern of muscle fiber type formation in the pig

Formation of new myotubes occurs exclusively at the multiple innervation zones of an embryonic large muscle

Hormonal regulation of motor unit size and synaptic strength during synapse elimination in the rat levator ani muscle

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