Synaptic neuropeptide release by dynamin-dependent partial release from circulating vesicles

Wong, Man Yan; Cavolo, Samantha L.; Levitan, Edwin S.

doi:10.1091/mbc.e15-01-0002

Cited by 38 publications

(42 citation statements)

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“…by measuring the loss of Dilp2-GFP fluorescence). In contrast to distal type Ib boutons, which show no difference in release among boutons (Shakiryanova et al, 2006;Wong et al, 2015), the percentage of peptide released from type II boutons evoked by depolarization is ∼50% lower for distal boutons (Fig. 2C).…”

Section: Resultsmentioning

confidence: 91%

“…These results raised the possibility that accumulation of DCVs in type II boutons occurs differently than in type Ib boutons, where circulation to and from the most distal bouton with bidirectional capture along the way leads to equivalent delivery and neuropeptide release (Wong et al, 2012(Wong et al, , 2015. To test this hypothesis, we used approaches that previously revealed vesicle circulation in type Ib boutons.…”

Section: Transport and Capture In Type II Arborsmentioning

confidence: 99%

“…Recently, it was shown that glutamatergic type Ib en passant boutons at the Drosophila neuromuscular junction (NMJ) are supplied equivalently with functional DCVs by vesicle circulation and bidirectional capture (Wong et al, 2012(Wong et al, , 2015. Furthermore, synaptic capture of DCVs increases following activity and is constitutively elevated by a transcription factor in specialized neuroendocrine neurons (Shakiryanova et al, 2006;Bulgari et al, 2014;Cavolo et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Limited distal organelles and synaptic function in extensive monoaminergic innervation

Tao

Bulgari

Deitcher

et al. 2017

Journal of Cell Science

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Organelles such as neuropeptide-containing dense-core vesicles (DCVs) and mitochondria travel down axons to supply synaptic boutons. DCV distribution among en passant boutons in small axonal arbors is mediated by circulation with bidirectional capture. However, it is not known how organelles are distributed in extensive arbors associated with mammalian dopamine neuron vulnerability, and with volume transmission and neuromodulation by monoamines and neuropeptides. Therefore, we studied presynaptic organelle distribution in Drosophila octopamine neurons that innervate ∼20 muscles with ∼1500 boutons. Unlike in smaller arbors, distal boutons in these arbors contain fewer DCVs and mitochondria, although active zones are present. Absence of vesicle circulation is evident by proximal nascent DCV delivery, limited impact of retrograde transport and older distal DCVs. Traffic studies show that DCV axonal transport and synaptic capture are not scaled for extensive innervation, thus limiting distal delivery. Activity-induced synaptic endocytosis and synaptic neuropeptide release are also reduced distally. We propose that limits in organelle transport and synaptic capture compromise distal synapse maintenance and function in extensive axonal arbors, thereby affecting development, plasticity and vulnerability to neurodegenerative disease.

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Section: Resultsmentioning

confidence: 91%

Section: Transport and Capture In Type II Arborsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Limited distal organelles and synaptic function in extensive monoaminergic innervation

Tao

Bulgari

Deitcher

et al. 2017

Journal of Cell Science

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“…There may be a number of several reasons for this discrepancy. First, the LDCV exocytosis proceeds more slowly than the exocytosis of small synaptic vesicles with conventional neurotransmitter (Wong, Cavolo, & Levitan, 2015; Xia, Lessmann, & Martin, 2009). Secondly, as we have shown, the release (leakage) of calcium from calcium stores with the subsequent activation of CaMKII is required to trigger the exocytosis of LDCVs, which in total also requires a certain time.…”

Section: Discussionmentioning

confidence: 99%

Ryanodine‐ and CaMKII‐dependent release of endogenous CGRP induces an increase in acetylcholine quantal size in neuromuscular junctions of mice

Gaydukov

Балезина

2018

Brain and Behavior

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ObjectiveThe aim of this study was to identify the mechanism responsible for an increase in miniature endplate potentials (MEPPs) amplitude, induced by ryanodine as an agonist of ryanodine receptors in mouse motor nerve terminals.MethodsUsing intracellular microelectrode recordings of MEPPs and evoked endplate potentials (EPPs), the changes in spontaneous and evoked acetylcholine release in motor synapses of mouse diaphragm neuromuscular preparations were studied.ResultsRyanodine (0.1 μM) increased both the amplitudes of MEPPs and EPPs to a similar extent (up to 130% compared to control). The ryanodine effect was prevented by blockage of receptors of calcitonin gene‐related peptide (CGRP) by a truncated peptide CGRP 8‐37. Endogenous CGRP is stored in large dense‐core vesicles in motor nerve terminals and may be released as a co‐transmitter. The ryanodine‐induced increase in MEPPs amplitude may be fully prevented by inhibition of vesicular acetylcholine transporter by vesamicol or by blocking the activity of protein kinase A with H‐89, suggesting that endogenous CGRP is released in response to the activation of ryanodine receptors. Activation of CGRP receptors can, in turn, upregulate the loading of acetylcholine into synaptic vesicles, which will increase the quantal size. This new feature of endogenous CGRP activity looks similar to recently described action of exogenous CGRP in motor synapses of mice. The ryanodine effect was prevented by inhibitors of Ca/Calmodulin‐dependent kinase II (CaMKII) KN‐62 or KN‐93. Inhibition of CaMKII did not prevent the increase in MEPPs amplitude, which was caused by exogenous CGRP.ConclusionsWe propose that the activity of presynaptic CaMKII is necessary for the ryanodine‐stimulated release of endogenous CGRP from motor nerve terminals, but CaMKII does not participate in signaling downstream the activation of CGRP‐receptors followed by quantal size increase.

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“…Many of these mechanistic differences in DCV biology have been probed at Drosophila synapses using transgenic animals expressing an artificial neuropeptide-GFP-tagged rat atrial natriuretic factor peptide (ANF-GFP) (Rao et al 2001a). This transgenic line has proved highly valuable for DCV biology, revealing mechanisms of activity-dependent recruitment of DCVs (Shakiryanova et al 2005), DCV capture at active terminals (Wong et al 2012;Bulgari et al 2014), presynaptic ER-dependent Ca 2+ release driving DCV fusion (Shakiryanova et al 2007(Shakiryanova et al , 2011, and partial depletion of DCV contents upon release (Wong et al 2015). In addition to aspects of DCV release and trafficking, studies have revealed the role of the basic helix-loop-helix transcription factor Dimmed in driving neuroendocrine cell fate, including its role in regulating the expression of specific DCV proteins (Hewes et al 2006;Hamanaka et al 2010;Park et al 2011Park et al , 2014.…”

Section: Dense Core Vesicle Releasementioning

confidence: 99%

Transmission, Development, and Plasticity of Synapses

Harris¹,

2015

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Chemical synapses are sites of contact and information transfer between a neuron and its partner cell. Each synapse is a specialized junction, where the presynaptic cell assembles machinery for the release of neurotransmitter, and the postsynaptic cell assembles components to receive and integrate this signal. Synapses also exhibit plasticity, during which synaptic function and/or structure are modified in response to activity. With a robust panel of genetic, imaging, and electrophysiology approaches, and strong evolutionary conservation of molecular components, Drosophila has emerged as an essential model system for investigating the mechanisms underlying synaptic assembly, function, and plasticity. We will discuss techniques for studying synapses in Drosophila, with a focus on the larval neuromuscular junction (NMJ), a well-established model glutamatergic synapse. Vesicle fusion, which underlies synaptic release of neurotransmitters, has been well characterized at this synapse. In addition, studies of synaptic assembly and organization of active zones and postsynaptic densities have revealed pathways that coordinate those events across the synaptic cleft. We will also review modes of synaptic growth and plasticity at the fly NMJ, and discuss how pre-and postsynaptic cells communicate to regulate plasticity in response to activity. KEYWORDS FlyBook; Drosophila; synapse; neurotransmitter release; synaptic plasticity; active zone; synaptic vesicle TABLE OF CONTENTS Abstract 345Introduction 345

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Synaptic neuropeptide release by dynamin-dependent partial release from circulating vesicles

Cited by 38 publications

References 38 publications

Limited distal organelles and synaptic function in extensive monoaminergic innervation

Limited distal organelles and synaptic function in extensive monoaminergic innervation

Ryanodine‐ and CaMKII‐dependent release of endogenous CGRP induces an increase in acetylcholine quantal size in neuromuscular junctions of mice

Transmission, Development, and Plasticity of Synapses

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