Release of acetylcholine from embryonic neurons upon contact with muscle cell

Chow, Ida; Poo, MM

doi:10.1523/jneurosci.05-04-01076.1985

Cited by 101 publications

(76 citation statements)

References 11 publications

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“…Our observation that presynaptic exocytotic machinery can develop in the absence of postsynaptic receptors agrees with previously published studies showing that nerve-muscle synapses form in the presence of antagonists that block receptor function (Cohen, 1972;Ding et al, 1983;Landmesser and Szente, 1986). Our results are also consistent with the findings that dissociated spinal neuron somas and associated growth cones are capable of both spontaneous (Kidokoro and Yeh, 1982;Hume et al, 1983;Young and Poo, 1983;Chow and Poo, 1985) and evoked (Sun and Poo, 1987) transmitter release. However, studies using Xenopus have further indicated that responses to both spontaneous and stimulusevoked release of ACh from spinal neurons are potentiated on contact with muscle.…”

Section: Discussionsupporting

confidence: 93%

“…Postsynaptic modulation of transmitter release machinery has been provided from studies that use Xenopus nerve and muscle wherein the formation of synaptic contacts can be strictly controlled. Measurement of synaptic responses from myocytes shows that both motor neuron somas and growth cones can spontaneously release ACh before contact with muscle (Kidokoro and Yeh, 1982;Hume et al, 1983;Young and Poo, 1983;Chow and Poo, 1985). However, contact with muscle potentiates transmitter release, as reflected in the increased size (Evers et al, 1989;Liou et al, , 1999 and frequency of spontaneous events (Xie and Poo, 1986;Evers et al, 1989).…”

Section: Introductionmentioning

confidence: 99%

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Optical Measurements of Presynaptic Release in Mutant Zebrafish Lacking Postsynaptic Receptors

Ono

Brehm

2003

J. Neurosci.

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Differentiation of presynaptic nerve terminals is mediated, in part, through contact with the appropriate postsynaptic target cell. In particular, studies using dissociated nerve and muscle derived from Xenopus embryos have indicated that the properties of transmitter release from motor neurons are altered after contact with skeletal muscle. This maturation of presynaptic function has further been linked to retrograde signaling from muscle that involves activation of postsynaptic ACh receptors. Using FM1-43 optical determinants of exocytosis, we now compare calcium-mediated exocytosis at neuromuscular junctions of wild-type zebrafish to mutant fish lacking postsynaptic ACh receptors. In response to either high-potassium depolarization or direct electrical stimulation, we observed no differences in the rate or extent of FM1-43 destaining. These data indicate that the acquisition of stimulus-evoked exocytosis at early developmental stages occurs independent of both postsynaptic receptor and synaptic responses in zebrafish.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Optical Measurements of Presynaptic Release in Mutant Zebrafish Lacking Postsynaptic Receptors

Ono

Brehm

2003

J. Neurosci.

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“…However, the influence of muscle on competent neurons was considerably greater: the percentage of neuritic length occupied by SVAPs was about 5-fold greater for portions of neurites on muscle than for portions off muscle. This result is in agreement with recent elegant studies indicating that contact with muscle regulates the distribution of ACh release sites in these neurons and causes an immediate (within seconds) local increase in ACh release (Chow and Poo, 1985;Xie and Poo, 1986). In addition, we found that about 50% of the SVAP length on muscle was located at NARPs.…”

Section: Discussionsupporting

confidence: 93%

Distribution of synaptic specializations along isolated motor units formed in Xenopus nerve-muscle cultures

Cohen¹,

Rodriguez-Marin²,

Wilson³

1987

J. Neurosci.

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The capacity of individual muscle cells and neurons to establish synaptic specializations along the entire extent of their neurite- muscle contacts was assessed in culture. Spinal cord neurons derived from embryos of Xenopus laevis were plated at low density in cultures of Xenopus myotomal muscle cells in order to obtain isolated motor units whose neuron and muscle cells were not contacted by any other neuron. These isolated motor units were examined for localization of acetylcholine receptors (AChRs) after staining with fluorescent alpha- bungarotoxin and, in some cases, for localization of a synaptic vesicle antigen by immunofluorescence. The neurite-muscle contacts formed by competent neurons exhibited discontinuous sites of AChR localization occupying about 25% of the contact length as compared with 2% for incompetent neurons. Competent neurons, unlike incompetent ones, established these neurite-associated receptor patches (NARPs) on virtually all the muscle cells they contacted and functionally innervated them. These and other observations on the distribution of NARPs throughout the isolated motor units indicate that the capacity of competent neurons to establish NARPs extends to the limits of growth of most if not all of their neurites, that this capacity is least in the most proximal portions of initial neuritic segments, and that the overall capacity of muscle cells to generate NARPs can be saturated by long lengths of neurite-muscle contact. The results also suggest that even in the absence of competitive interactions between neurons there are spatial discontinuities in neuritic action and/or muscle response during the establishment of NARPs. Synaptic vesicle antigen patches (SVAPs) occurred along the neuritic arbor of all neurons, but their distribution in competent neurons (those which established NARPs) and in incompetent ones differed. For competent neurons the percentage of neurite length occupied by SVAPs was 4.8-fold greater on muscle cells than off, whereas the corresponding value for incompetent neurons was only 1.5-fold. This large preferential localization of SVAPs along neurite-muscle contacts of competent neurons was further associated with a colocalization of SVAPs and NARPs that was greater than predicted by chance. These results suggest that muscle cells are much more effective in influencing the distribution of synaptic vesicles along the neuritic arbor of competent neurons than along the arbor of incompetent neurons and that this influence is greatest at sites of postsynaptic differentiation.(ABSTRACT TRUNCATED AT 400 WORDS)

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“…Because muscle pioneers are the first cells to assemble contractile elements, to cluster acetylcholine receptors (Liu and Westerfield, 1992), and to contract, and because these contractions can be blocked with cholinergic antagonists, these regions of apposition probably represent sites of neuromuscular transmission. These observations suggest that the early functional interactions between zebrafish primary motoneurons and muscle pioneers are attributable to release of transmitter from the growth cone, as described previously for cultured Xenopus laevis spinal neurons (Young and Poo, 1983;Chow and Poo, 1985;Sun and Poo, 1985) and cultured chick ciliary ganglion neurons (Hume et al, 1983). Transmitter release may provide a mechanism for growth cones to interact with or modify their immediate environment (Bentley and O'Connor, 1994;Kater and Rehder, 1995).…”

Section: Muscle Pioneers Are Intermediate Targets For Primary Motoneusupporting

confidence: 70%

Pathfinding by Identified Zebrafish Motoneurons in the Absence of Muscle Pioneers

et al. 1997

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To identify the cellular cues that guide zebrafish neuronal growth cones to their targets, we examined interactions between identified motor growth cones and identified muscle fibers and tested whether these fibers were required for growth cone navigation. Caudal primary motoneurons (CaPs) and middle primary motoneurons (MiPs) are identified motoneurons that innervate cell-specific regions of the myotome. Growth cones of both cells initially extend along a common pathway and then pause at a set of identified muscle fibers, called muscle pioneers, before diverging along cell-specific pathways. Muscle pioneers are intermediate targets of both CaP and MiP Liu and Westerfield, 1990); both motoneurons extend their growth cones directly to the muscle pioneers on which the first functional neuromuscular contacts form, suggesting that muscle pioneers may provide guidance information to these growth cones. We tested this idea by ablating muscle pioneers and observing the resulting motor axonal trajectories. Both CaP and MiP ultimately formed normal axonal arbors after muscle pioneer ablation, showing that muscle pioneers are unnecessary for formation of correct axonal trajectories; however, although final cellular morphology was correct in the absence of muscle pioneers, MiP growth cones branched abnormally or extended ventrally beyond the common pathway. Ablation of CaP and the muscle pioneers together increased the aberrant behavior of the MiP growth cone. Our results provide evidence that an intermediate target, the muscle pioneers, affects motor axonal extension without altering target choice, suggesting that other cues also contribute to proper pathway navigation. Key words: acetylcholine receptors; neuromuscular junctions; axogenesis; zebrafish motoneurons; muscle pioneers; pathway navigationThe environment through which growth cones navigate contains cues that regulate neuronal pathfinding (Frank and Wenner, 1993;Goodman and Shatz, 1993;Keynes and Cook, 1995). En route to their synaptic targets, neurons may project axons to intermediate targets that influence subsequent pathway choice . For example, some grasshopper pioneer neurons project to guidepost cells (Bentley and Keshishian, 1982) that are required for normal pathfinding (Bentley and Caudy, 1983). Chick hindlimb motoneurons (Lance-Jones and Landmesser, 1981; Tosney and Landmesser, 1985a,b;Landmesser, 1992) and spinal commissural neurons (Bovolenta and Dodd, 1991) also project to specific intermediate targets, which appear to influence extension. These results suggest that intermediate targets serve as choice points for pathway selection.We examined the role of potential intermediate targets in the pathway choices of zebrafish primary motoneurons. We focused on the first two primary motoneurons to extend growth cones out of the spinal cord: C aP and MiP (see Fig. 1) Myers et al., 1986). The C aP growth cone pioneers a common pathway to the nascent horizontal myoseptum, where it pauses before selecting its cell-specific pathway along ventral myotome Myers e...

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Release of acetylcholine from embryonic neurons upon contact with muscle cell

Cited by 101 publications

References 11 publications

Optical Measurements of Presynaptic Release in Mutant Zebrafish Lacking Postsynaptic Receptors

Optical Measurements of Presynaptic Release in Mutant Zebrafish Lacking Postsynaptic Receptors

Distribution of synaptic specializations along isolated motor units formed in Xenopus nerve-muscle cultures

Pathfinding by Identified Zebrafish Motoneurons in the Absence of Muscle Pioneers

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