Synaptic target recognition at Drosophila neuromuscular junctions

Rose, Demian; Chibá, Akira

doi:10.1002/(sici)1097-0029(20000401)49:1<3::aid-jemt2>3.3.co;2-5

Cited by 5 publications

(5 citation statements)

References 51 publications

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“…Much of this work has been carried out at neuromuscular synapses of identified body wall muscles in the embryo and third instar larva as well as neuromuscular synapses of the adult. The embryonic and larval preparations have been characterized extensively and serve as important models for analysis of synaptic development, plasticity, and function (Keshishian et al 1996;Koh et al 2000;Matthies and Broadie 2003;Richmond and Broadie 2002;Rose and Chiba 2000;Stimson and Ramaswami 1999;Wu and Bellen 1997). Adult neuromuscular preparations have been utilized for investigating mechanisms of synaptic function, for example in defining the roles of dynamin (Ikeda et al 1976; Koenig and Ikeda 1996;Kosaka and Ikeda 1983;Poodry and Edgar 1979;Salkoff and Kelly 1978), NSF (Kawasaki et al 1998), and presynaptic calcium channels (Brooks et al 2003;Kawasaki et al , 2002Kawasaki et al , 2004, and important developmental studies have been carried out as well Keshishian 1999, 1998;Ikeda and Koenig 1988;Rivlin et al 2004;Sun and Wyman 1997;Trimarchi et al 1999).…”

Section: Introductionmentioning

confidence: 99%

Properties of Short-Term Synaptic Depression at Larval Neuromuscular Synapses in Wild-Type and Temperature-Sensitive Paralytic Mutants ofDrosophila

Kawasaki

Ordway

2005

Journal of Neurophysiology

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The larval neuromuscular synapse of Drosophila serves as an important model for genetic and molecular analysis of synaptic development and function. Further functional characterization of this synapse, as well as adult neuromuscular synapses, will greatly enhance the impact of this model system on our understanding of synaptic transmission. Here we describe a form of short-term synaptic depression observed at larval, but not adult, neuromuscular synapses and explore the underlying mechanisms. Larval neuromuscular synapses exhibited a form of short-term depression that was strongly dependent on stimulation frequency over a narrow range of low frequencies (0.1-1 Hz). This form of synaptic depression, referred to here as low-frequency short-term depression (LF-STD), results from an activity-dependent reduction in neurotransmitter release. However, in contrast to the predictions of depletion models, the degree of depression was independent of the initial level of neurotransmitter release over a range of extracellular calcium concentrations. This conclusion was confirmed in two temperature-sensitive (TS) paralytic mutants, cacophony and shibire, which exhibit reduced neurotransmitter release resulting from conditional disruption of presynaptic calcium channels and dynamin, respectively. Higher stimulation frequencies (40 or 60 Hz) produced two components of depression that appeared to include LF-STD as well as a more conventional component of short-term depression. These findings reveal novel properties of short-term synaptic depression and suggest that complementary genetic analysis of larval and adult neuromuscular synapses will further define the in vivo mechanisms of neurotransmitter release and short-term synaptic plasticity.

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Section: Introductionmentioning

confidence: 99%

Properties of Short-Term Synaptic Depression at Larval Neuromuscular Synapses in Wild-Type and Temperature-Sensitive Paralytic Mutants ofDrosophila

Kawasaki

Ordway

2005

Journal of Neurophysiology

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“…The creation of every functional synapse begins with synaptic target recognition, the series of events in which a pre-and a postsynaptic cell identify one another as partners. In recent years, a fairly solid understanding of the molecular components underlying this process has developed (Sanes and Lichtman, 1999;Rose and Chiba, 2000;Garner et al, 2002;Jin, 2002). Remaining to be examined more closely are the cellular dynamics that accompany synaptic targeting and allow partner cells to physically interact in a meaningful way.…”

Section: Introductionmentioning

confidence: 99%

Myopodia (postsynaptic filopodia) participate in synaptic target recognition

Ritzenthaler

Chiba

2003

J. Neurobiol.

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Synaptic partner cells recognize one another by utilizing a variety of molecular cues. Prior to neuromuscular synapse formation, Drosophila embryonic muscles extend dynamic actin-based filopodia called "myopodia." In wild-type animals, myopodia are initially extended randomly from the muscle surface but become gradually restricted to the site of motoneuron innervation, a spatial redistribution we call "clustering." Previous experiments with prospero mutant embryos demonstrated that myopodia clustering does not occur in the absence of motoneuron outgrowth into the muscle field. However, whether myopodia clustering is due to a general signal from passing axons or is a result of the specific interactions between synaptic partners remained to be investigated. Here, we have examined the relationship of myopodia to the specific events of synaptic target recognition, the stable adhesion of synaptic partners. We manipulated the embryonic expression of alphaPS2 integrin and Toll, molecules known to affect synaptic development, to specifically alter synaptic targeting on identified muscles. Then, we used a vital single-cell labeling approach to visualize the behavior of myopodia in these animals. We demonstrate a strong positive correlation between myopodia activity and synaptic target recognition. The frequency of myopodia clustering is lowered in cases where synaptic targeting is disrupted. Myopodia clustering seems to result from the adherence of a subset of myopodia to the innervating growth cone while the rest are eliminated. The data suggest that postsynaptic cells play a dynamic role in the process of synaptic target recognition.

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“…In Drosophila, each body wall hemisegment contains a well-defined set of 30 muscles, arranged along the ventral-dorsal axis, that are innervated by about 40 motoneurons in a stereotypic, timed manner (25,38,42). All muscles of Drosophila embryos express Comm during the period of motoneuron-muscle interactions.…”

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confidence: 99%

Regulation of Commissureless by the Ubiquitin Ligase DNedd4 Is Required for Neuromuscular Synaptogenesis in Drosophila melanogaster

Ing

Shteiman-Kotler²,

Castelli³

et al. 2007

Molecular and Cellular Biology

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Muscle synaptogenesis in Drosophila melanogaster requires endocytosis of Commissureless (Comm), a binding partner for the ubiquitin ligase dNedd4. We investigated whether dNedd4 and ubiquitination mediate this process. Here we show that Comm is expressed in intracellular vesicles in the muscle, whereas Comm bearing mutations in the two PY motifs (L/PPXY) responsible for dNedd4 binding [Comm(2PY3AY)], or bearing Lys3Arg mutations in all Lys residues that serve as ubiquitin acceptor sites [Comm(10K3R)], localize to the muscle surface, suggesting they cannot endocytose. Accordingly, aberrant muscle innervation is observed in the Comm(2PY3AY) and Comm(10K3R) mutants expressed early in muscle development. Similar muscle surface accumulation of Comm and innervation defects are observed when dNedd4 is knocked down by double-stranded RNA interference in the muscle, in dNedd4 heterozygote larvae, or in muscles overexpressing catalytically inactive dNedd4. Expression of the Comm mutants fused to a single ubiquitin that cannot be polyubiquitinated and mimics monoubiquitination [Comm(2PY3AY)-monoUb or Comm(10K3R)-monoUb] prevents the defects in both Comm endocytosis and synaptogenesis, suggesting that monoubiquitination is sufficient for Comm endocytosis in muscles. Expression of the Comm mutants later in muscle development, after synaptic innervation, has no effect. These results demonstrate that dNedd4 and ubiquitination are required for Commissureless endocytosis and proper neuromuscular synaptogenesis.

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Synaptic target recognition at Drosophila neuromuscular junctions

Cited by 5 publications

References 51 publications

Properties of Short-Term Synaptic Depression at Larval Neuromuscular Synapses in Wild-Type and Temperature-Sensitive Paralytic Mutants ofDrosophila

Properties of Short-Term Synaptic Depression at Larval Neuromuscular Synapses in Wild-Type and Temperature-Sensitive Paralytic Mutants ofDrosophila

Myopodia (postsynaptic filopodia) participate in synaptic target recognition

Regulation of Commissureless by the Ubiquitin Ligase DNedd4 Is Required for Neuromuscular Synaptogenesis in Drosophila melanogaster

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