The growth of segmental nerves from the brachial myotomes into the proximal muscles of the chick forelimb during development

Bennett, Max R.; Davey, D. F.; Uebel, K. E.

doi:10.1002/cne.901890209

Cited by 61 publications

(20 citation statements)

References 36 publications

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“…The (34). In the limb of the chicken embryo, primary myotubes first appear at ED4.5 (35) and secondary myotubes are clearly delineated by ED11-ED12 (14,16). Fibers of diverse types appear to form during both phases of myogenesis (11,(14)(15)(16).…”

Section: Discussionmentioning

confidence: 99%

Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains.

Miller¹,

Stockdale²

1986

Proc. Natl. Acad. Sci. U.S.A.

148

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A clonal analysis was used to show that skeletal muscle myoblasts are committed to distinct cell lineages during development. Myoblasts taken from embryonic chicken hindlimb muscles of different ages were cultured at clonal density. The content offast and slow classes of the myosin heavy chain isoforms in the myotubes of the resulting muscle colonies was determined immunocytochemically with specific monoclonal antibodies that served as markers for the different fiber types. The muscle colonies formed by cloning myoblasts from early hindlimbs (days 4-6 in ovo) were of three types: the most numerous type, in which all myotubes in a colony contained only the fast class of myosin heavy chain; a less numerous type, in which all myotubes in a colony contained both the fast and slow classes of myosin heavy chain isoforms; and a rare type, in which all myotubes in a colony contained only the slow class of myosin heavy chain. The muscle colonies formed by cloning myoblasts from later hindlimbs (days 10-12 in ovo) were, however, all of one type, in which every myotube in a colony contained only fast myosin heavy chain. Thus, myoblasts in the early embryo (days 4-6 in ovo) were a heterogeneous population committed to three myogenic lineages: fast, mixed fast/slow, and slow, whereas myoblasts from the later embryo (days 10-12 in ovo) were only in the fast myogenic lineage. These results suggest that muscle fiber formation is rooted in two developmental phases-an early phase in which diverse fiber types are formed from intrinsically diverse populations of myoblasts and a later phase in which fibers are formed from a single population of myoblasts.The analysis of cell lineage is a central problem in developmental biology. To understand the molecular and cellular mechanisms underlying differentiation of a particular cell type, it is necessary to identify and isolate the immediate precursors ofthe differentiated cell of interest. One system in which the analysis of cell lineage has presented a long-standing problem is the formation of the three muscle cell types of skeletal muscle: the fast, mixed fast/slow, and slow muscle fibers which are described below. Two models-one requiring a single myogenic lineage and a second requiring multiple myogenic lineages-could explain muscle fiber diversification (1). It has usually been assumed that all muscle fibers arise from a single myoblast population, with diversification specified later by the type of innervation the fibers received. The experimental justification for this assumption has not, however, been compelling, and the alternative model, that fast, mixed fast/slow, and slow fibers form from separate myoblast populations, has remained an open possibility (1). Recent results led us to reexamine myogenic lineages in muscle fiber diversification.Adult muscles in birds and mammals contain a heterogeneous population of muscle fibers with fast, mixed, and slow properties. Although first defined physiologically, these fiber types can now be defined biochemically by the presence...

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Section: Discussionmentioning

confidence: 99%

Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains.

Miller¹,

Stockdale²

1986

Proc. Natl. Acad. Sci. U.S.A.

148

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“…In developing chick limb muscle the interval is apparently short. Nerve fibres have been detected by embryonic day 4 (Oppenheim & Heaton, 1975;Bennett et al 1980) and ACh receptor patches have been observed as early as embryonic days 4-5 (Betz et al 1980), but the sequence has not yet been established.…”

Section: Development Of Sites Of High Ach Receptor Densitymentioning

confidence: 99%

Developmental changes in the distribution of acetylcholine receptors in the myotomes of Xenopus laevis.

Chow¹,

Cohen²

1983

The Journal of Physiology

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SUMMARY1. The acquisition and distribution of nerve fibres and of acetylcholine (ACh) receptors were examined in the myotomes of Xenopus laevis during normal development. This muscle is well-suited for investigating temporal relationships during neuromuscular synaptogenesis because the age of the Xenopus embryo at the onset of innervation can be assessed with an accuracy of about one hour. Myotomal nerve fibres were visualized after staining them with nitroblue tetrazolium and ACh receptors were examined after exposure to x-bungarotoxin labelled with 1251 or fluorescent dye.2. Nerve fibres were seen in the myotomes of some embryos as early as stage 19(20'75 hr) and in virtually all embryos by stage 24 (26-25 hr). From the outset they were located mainly at the ends of the myotomes, but some myotomes also exhibited nerve fibres in more central regions.3. ACh receptors were already present in myotomes by stage 19 (20-75 hr) and initially had a widespread, uniform distribution. The density of extrajunctional ACh receptors increased until stage 36 (50 hr) and then declined less than 3-fold over the next 10 days of development.4. Discrete patches of high ACh receptor density began to appear at the ends of the myotomes at stage 22 (24 hr) and were seen in almost all embryos by stage 26 (29-5 hr). ACh receptor patches were also seen in central regions of some myotomes and these were usually aligned in patterns which resembled the course of nerve fibres.5. The present findings suggest that myotomal muscle cells in Xenopus embryos begin to acquire ACh receptors shortly before the arrival of nerve fibres and that discrete patches of ACh receptors begin to form at presumptive synaptic sites on the average about 3 hr after the arrival of the nerve fibres. The latter delay is considerably shorter than that in developing rat muscle.6. The temporal and spatial relationships between nerve fibres and the development of ACh receptor patches in Xenopus myotomes in vivo are consistent with findings in Xenopus cell cultures which indicate that nerve fibres can rapidly induce ACh receptor localization at sites of nerve-muscle contact.

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“…Indirect measurements indicate that DRG neurons grow processes toward more distant targets at greater rates than toward closer targets (Honig, 1982;Scott, 1982;Swanson and Lewis, 1982). The main objective ofthi: present study was therefore to determine whether growth rate is determined more by an intrinsic, segmentally based program, as has been suggested for cranial sensory neurons by Davies ( 1989), or whether it is determined more by the environment of the limbs, which regulates neurite outgrowth, as suggested indirectly by earlier work (Hamburger, 1939;Bennett et al, 1980;Swanson and Lewis, 1982). We investigated this problem by culturing isolated cells and explants from DRG taken from chick embryos during the stages over which DRG neurons normally grow axons into the periphery.…”

Section: Discussionmentioning

confidence: 90%

Segmental independence and age dependence of neurite outgrowth from embryonic chick sensory neurons

Parson

Ribchester

1995

J. Neurobiol.

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SUMMARYTargets in limb regions of the chick embryo are further removed from the dorsal root ganglia that innervate them compared with thoracic ganglion-to-target distances. It has been inferred that axons grow into the limb regions two to three times faster than into nonlimb regions. We tested whether the differences were due to intrinsic properties of the neurons located at different segmental levels. Dorsal root ganglia (DRG) were isolated from the forelimb, trunk, and hind limb regions of stage 25-30 embryos. Neurite outgrowth was measured in dissociated cell culture and in cultures of DRG explants. Although there was considerable variability in the amount of neurite outgrowth, there were no substantive differences in the amount or the rate of outgrowth comparing brachial, thoracic, or lumbosacral neurons. The amount of neurite outgrowth in dissociated cell cultures increased with the stage of development. Overall, our data suggest that DRG neurons express a basal amount of outgrowth, which is initially independent of target-derived neurotrophic influences; the magnitude of this intrinsic growth potential increases with stage of development; and the neurons of the DRG are not intrinsically specified to grow neurites at rates that are matched to the distance they are required to grow to make contact with their peripheral targets in vivo. We present a speculative model based on Poisson statistics, which attempts to account for the variability in the amount of neurite outgrowth from dissociated neurons.

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The growth of segmental nerves from the brachial myotomes into the proximal muscles of the chick forelimb during development

Cited by 61 publications

References 36 publications

Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains.

Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains.

Developmental changes in the distribution of acetylcholine receptors in the myotomes of Xenopus laevis.

Segmental independence and age dependence of neurite outgrowth from embryonic chick sensory neurons

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