Mechanisms of Dendritic Elaboration of Sensory Neurons in<i>Drosophila</i>: Insights from<i>In Vivo</i>Time Lapse

Williams, Darren W.; Truman, James W.

doi:10.1523/jneurosci.4521-03.2004

Cited by 70 publications

(70 citation statements)

References 39 publications

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“…The abdominal sensory system of the adult fly is a mosaic consisting of postembryonic neurons derived from the imaginal histoblast nests and genital disk (Hartenstein and Posakony, 1989;Taylor, 1989), and a subset of larval sensory neurons of embryonic origin (Williams and Shepherd, 1999;Williams and Truman, 2004). At the onset of metamorphosis, larval sensory neurons either die or survive and remodel.…”

Section: Discussionmentioning

confidence: 99%

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Cellular mechanisms of dendrite pruning inDrosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons

2005

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Regressive events that refine exuberant or inaccurate connections are critical in neuronal development. We used multi-photon, time-lapse imaging to examine how dendrites of Drosophila dendritic arborizing (da) sensory neurons are eliminated during early metamorphosis, and how intrinsic and extrinsic cellular mechanisms control this deconstruction. Removal of the larval dendritic arbor involves two mechanisms: local degeneration and branch retraction. In local degeneration, major branch severing events entail focal disruption of the microtubule cytoskeleton, followed by thinning of the disrupted region, severing and fragmentation. Retraction was observed at distal tips of branches and in proximal stumps after severing events. The pruning program of da neuron dendrites is steroid induced; cell-autonomous dominantnegative inhibition of steroid action blocks local degeneration, although retraction events still occur. Our data suggest that steroid-induced changes in the epidermis may contribute to dendritic retraction. Finally, we find that phagocytic blood cells not only engulf neuronal debris but also attack and sever intact branches that show signs of destabilization.

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Section: Discussionmentioning

confidence: 99%

“…Among those that survive are dendritic arborizing (da) sensory neurons (Usui-Ishihara et al, 2000;Williams and Shepherd, 2002). The large, complex dendritic arbors of these neurons are completely removed during early metamorphosis, before the cells elaborate their adult-specific arbors (Smith and Shepherd, 1996;Williams and Truman, 2004).…”

Section: Introductionmentioning

confidence: 99%

Cellular mechanisms of dendrite pruning inDrosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons

2005

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“…In holometabolous insects, dendritic regression is dependent on hormonal cues (Weeks et al, 1992;Weeks, 1999;Williams and Truman, 2004). Manduca proleg motoneurons are one of the rare systems in which it has been shown that dendritic retraction is accompanied by synapse elimination and, thus, the dismantling of larval motor circuits (Streichert and Weeks, 1995;Gray and Weeks, 2003).…”

Section: Discussionmentioning

confidence: 99%

Activity Affects Dendritic Shape and Synapse Elimination during Steroid Controlled Dendritic Retraction inManduca sexta

Duch¹,

Mentel²

2004

J. Neurosci.

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Insect metamorphosis is a compelling example for dendritic and synaptic remodeling as larval and adult behaviors place distinct demands on the CNS. During the metamorphosis of the moth, Manduca sexta, many larval motoneurons are remodeled to serve a new function in the adult. During late larval life, steroid hormones trigger axonal and dendritic regression as well as larval synapse elimination. These regressive events are accompanied by stereotypical changes in motor behavior during the so-called wandering stages. Both normally occurring changes in dendritic shape and in motor output have previously been analyzed quantitatively for the individually identified motoneuron MN5. This study tested whether activity affected steroid-induced dendritic regression and synapse disassembly in MN5 by means of chronically implanted extracellular electrodes. Stimulating MN5 in vivo in intact, normally developing animals during a developmental period when it usually shows no activity significantly slowed the regression of high-order dendrites. Both physiological and anatomical analysis demonstrated that reduced dendritic regression was accompanied by a significant reduction in larval synapse disassembly. Therefore, steroid-induced alterations of dendritic shape and synaptic connectivity are modified by activity-dependent mechanisms. This interaction might be a common mechanism for rapid adjustments of rigid, inflexible, hormonal programs.

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“…After an initial phase of slow dendrite growth, rapid extension and arborization occurs, characterized by an increased rate of additions and retractions of branches (Wu et al, 1999;Williams and Truman, 2004) and high motility of filopodia on dendritic growth cones (Portera-Cailliau et al, 2003;Williams and Truman, 2004). Subsequently, the dendritic arbor becomes more stable, showing a reduced rate of branch additions and retractions (Wu et al, 1999) and disappearance of growth cone-associated filopodia (PorteraCailliau et al, 2003).…”

Section: Pi3k In Stages Of Dendrite Developmentmentioning

confidence: 99%

Control of Dendritic Arborization by the Phosphoinositide-3′-Kinase–Akt–Mammalian Target of Rapamycin Pathway

Jaworski¹,

Spangler²,

Seeburg³

et al. 2005

J. Neurosci.

531

472

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The molecular mechanisms that determine the size and complexity of the neuronal dendritic tree are unclear. Here, we show that the phosphoinositide-3Ј kinase (PI3K)-Akt-mammalian target of rapamycin (mTOR) signaling pathway promotes the growth and branching of dendrites in cultured hippocampal neurons. Constitutively active mutants of Ras, PI3K, and Akt, or RNA interference (RNAi) knockdown of lipid phosphatase PTEN (phosphatase and tensin homolog deleted on chromosome Ten), induced growth and elaboration of dendrites that was blocked by mTOR inhibitor rapamycin and/or by overexpression of eIF-4E binding protein 1 (4E-BP1), which inhibits translation of 5Ј capped mRNAs. The effect of PI3K on dendrites was lost in more mature neurons (Ͼ14 d in vitro). Dendritic complexity was reduced by inhibition of PI3K and by RNAi knockdown of mTOR or p70 ribosomal S6 kinase (p70S6K, an effector of mTOR). A rapamycin-resistant mutant of mTOR "rescued" the morphogenetic effects of PI3K in the presence of rapamycin. By regulating global and/or local protein translation, and as a convergence point for multiple signaling pathways, mTOR could play a central role in the control of dendrite growth and branching during development and in response to activity.

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Mechanisms of Dendritic Elaboration of Sensory Neurons inDrosophila: Insights fromIn VivoTime Lapse

Cited by 70 publications

References 39 publications

Cellular mechanisms of dendrite pruning inDrosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons

Cellular mechanisms of dendrite pruning inDrosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons

Activity Affects Dendritic Shape and Synapse Elimination during Steroid Controlled Dendritic Retraction inManduca sexta

Control of Dendritic Arborization by the Phosphoinositide-3′-Kinase–Akt–Mammalian Target of Rapamycin Pathway

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