Drosophila larval neuromuscular junction: Molecular components and mechanisms underlying synaptic plasticity

Koh, Young Ho; Gramates, L. Sian; Budnik, Vivian

doi:10.1002/(sici)1097-0029(20000401)49:1<14::aid-jemt3>3.0.co;2-g

Cited by 89 publications

(22 citation statements)

References 165 publications

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“…Muscle fibres of the Drosophila larval body wall are stereotypically innervated by motor neurons that contain a characteristic complement of neurotransmitters, including glutamate, peptides and biogenic amines 56 . Throughout larval development, wild type motor neuron synapses are challenged by continuously growing target muscles.…”

Section: Wnts Induce Synaptic Differentiationmentioning

confidence: 99%

Wnts and TGFβ in synaptogenesis: old friends signalling at new places

Packard¹,

Mathew²,

Budnik³

2003

Nat Rev Neurosci

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116

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The formation of mature synaptic connections involves the targeted transport and aggregation of synaptic vesicles, the gathering of presynaptic release sites and the clustering of postsynaptic neurotransmitter receptors and ion channels. Positional cues are required to orient the cytoskeleton in the direction of neuronal outgrowth, and also to direct the juxtaposition of synaptic protein complexes at the pre-and postsynaptic membranes. Both anterograde and retrograde factors are thought to contribute positional information during synaptic differentiation, and recent studies in vertebrates and invertebrates have begun to uncover a new role in this process for proteins that are essential for pattern formation in the early embryo.Cells use distinct mechanisms for transmitting information to their neighbours, depending on their tissue type and environment. This intercellular communication is vital during the early stages of development, when nascent cells acquire their identities to organize the body plan, and later as mature cells work together to maintain function and lifestyle. Not surprisingly, disruption of intercellular communication leads to various diseases, ranging from cancer to mental retardation, so understanding the fundamental nature of cell-talk remains one of the most important areas of biology.In the nervous system, the elemental means of communication between cells is synaptic transmission. Chemical synapses are asymmetrical cellular junctions that are involved in the directional transmission of electrical signals. Essential to the high speed and efficiency at which neurons communicate is the exquisite molecular organization of the pre-and postsynaptic apparatus. In the presynaptic compartment, neurotransmitter-laden vesicles are poised at ACTIVE ZONES, ready for immediate release, and the calcium channels that are required to trigger exocytosis are spatially linked to the secretory machinery. At the postsynaptic membrane, neurotransmitter receptors form high-density clusters that are directly apposed to the active zones. The proper development and functioning of synaptic Correspondence to V.B. vbudnik@ bio.umass.edu. DATABASES The following terms in this article are linked online to: Entrez: http://www.ncbi.nlm.nih.gov/Entrez/Tbl1 FlyBase: http://flybase.bio.indiana.edu/ Arm | Arr Once synapses are formed, the strengthening and weakening of synaptic connections is believed to be central to the processes of learning and memory, and also to the regeneration of synaptic connectivity after a traumatic injury. This synaptic plasticity also depends on communication between pre-and postsynaptic compartments 1 , and it includes both anterograde and retrograde signals. The existence of a retrograde signal has been postulated to account for the adjustment of presynaptic outputs that result from changes in postsynaptic responses. For example, at the fly neuromuscular junction (NMJ), decreased muscle responses to neuronal stimuli can be brought about by manipulation of glutamate receptor (GluR) levels...

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Section: Wnts Induce Synaptic Differentiationmentioning

confidence: 99%

Wnts and TGFβ in synaptogenesis: old friends signalling at new places

Packard¹,

Mathew²,

Budnik³

2003

Nat Rev Neurosci

Self Cite

116

View full text Add to dashboard Cite

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“…This synapse is widely used for functional studies of synaptic transmission (Bellen, 1998;Gramates and Budnik, 1999;Featherstone and Broadie, 2000;Koh et al, 2000) and expresses postsynaptic glutamate receptors that are homologous to vertebrate non-NMDA glutamate receptors (Schuster et al, 1991;DiAntonio et al, 1999;. Subunit composition has been shown to both regulate biophysical properties of glutamate receptors and to control synapse formation and function in this model system (DiAntonio et al, 1999;Sigrist et al, 2000Sigrist et al, , 2002.…”

Section: Introductionmentioning

confidence: 99%

Four Different Subunits Are Essential for Expressing the Synaptic Glutamate Receptor at Neuromuscular Junctions ofDrosophila

Qin

Schwarz²,

Kittel³

et al. 2005

J. Neurosci.

208

234

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Three ionotropic glutamate receptor subunits, designated GluRIIA, GluRIIB, and GluRIII, have been identified at neuromuscular junctions of Drosophila. Whereas GluRIIA and GluRIIB are redundant for viability, it was shown recently that GluRIII is essential for both the synaptic localization of GluRIIA and GluRIIB and the viability of Drosophila. Here we identify a fourth and a fifth subunit expressed in the neuromuscular system, which we name GluRIID and GluRIIE. Both new subunits we show to be necessary for survival. Moreover, both GluRIID and GluRIIE are required for the synaptic expression of all other glutamate receptor subunits. All five subunits are interdependent for receptor function, synaptic receptor expression, and viability. This indicates that synaptic glutamate receptors incorporate the GluRIII, GluRIID, and GluRIIE subunit together with either GluRIIA or GluRIIB at the Drosophila neuromuscular junction. At this widely used model synapse, the assembly of four different subunits to form an individual glutamate receptor channel may thus be obligatory. This study opens the way for a further characterization of in vivo glutamate receptor assembly and trafficking using the efficient genetics of Drosophila.

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“…The neuromuscular junction of Drosophila (NMJ) allows for the efficient genetic analysis of development, plasticity, and function of glutamatergic synapses (Jan and Jan, 1976;Keshishian et al, 1996;Prokop, 1999;Koh et al, 2000;Richmond and Broadie, 2002). The glutamate receptor subunits expressed at the NMJ are related to mammalian non-NMDA-type glutamate receptors, and glutamate receptor levels can control the number of synapses forming at the NMJ (Petersen et al, 1997;Sigrist et al, 2000Sigrist et al, , 2002Sigrist et al, , 2003.…”

Section: Introductionmentioning

confidence: 99%

Non-NMDA-Type Glutamate Receptors Are Essential for Maturation But Not for Initial Assembly of Synapses atDrosophilaNeuromuscular Junctions

Schmid

Qin²,

Wichmann³

et al. 2006

J. Neurosci.

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The assembly of glutamatergic postsynaptic densities (PSDs) seems to involve the gradual recruitment of molecular components from diffuse cellular pools. Whether the glutamate receptors themselves are needed to instruct the structural and molecular assembly of the PSD has hardly been addressed. Here, we engineered Drosophila neuromuscular junctions (NMJs) to express none or only drastically reduced amounts of their postsynaptic non-NMDA-type glutamate receptors. At such NMJs, principal synapse formation proceeded and presynaptic active zones showed normal composition and ultrastructure as well as proper glutamate release. At the postsynaptic site, initial steps of molecular and structural assembly took place as well. However, growth of the nascent PSDs to mature size was inhibited, and proteins normally excluded from PSD membranes remained at these apparently immature sites. Intriguingly, synaptic transmission as well as glutamate binding to glutamate receptors appeared dispensable for synapse maturation. Thus, our data suggest that incorporation of non-NMDA-type glutamate receptors and likely their protein-protein interactions with additional PSD components triggers a conversion from an initial to a mature stage of PSD assembly.

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Drosophila larval neuromuscular junction: Molecular components and mechanisms underlying synaptic plasticity

Cited by 89 publications

References 165 publications

Wnts and TGFβ in synaptogenesis: old friends signalling at new places

Wnts and TGFβ in synaptogenesis: old friends signalling at new places

Four Different Subunits Are Essential for Expressing the Synaptic Glutamate Receptor at Neuromuscular Junctions ofDrosophila

Non-NMDA-Type Glutamate Receptors Are Essential for Maturation But Not for Initial Assembly of Synapses atDrosophilaNeuromuscular Junctions

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