Development of dendrite polarity in Drosophila neurons

Abstract

BackgroundDrosophila neurons have dendrites that contain minus-end-out microtubules. This microtubule arrangement is different from that of cultured mammalian neurons, which have mixed polarity microtubules in dendrites.ResultsTo determine whether Drosophila and mammalian dendrites have a common microtubule organization during development, we analyzed microtubule polarity in Drosophila dendritic arborization neuron dendrites at different stages of outgrowth from the cell body in vivo. As dendrites initially extended, they contained mixed polarity microtubules, like mammalian neurons developing in culture. Over a period of several days this mixed microtubule array gradually matured to a minus-end-out array. To determine whether features characteristic of dendrites were localized before uniform polarity was attained, we analyzed dendritic markers as dendrites developed. In all cases the markers took on their characteristic distribution while dendrites had mixed polarity. An axonal marker was also quite well excluded from dendrites throughout development, although this was perhaps more efficient in mature neurons. To confirm that dendrite character could be acquired in Drosophila while microtubules were mixed, we genetically disrupted uniform dendritic microtubule organization. Dendritic markers also localized correctly in this case.ConclusionsWe conclude that developing Drosophila dendrites initially have mixed microtubule polarity. Over time they mature to uniform microtubule polarity. Dendrite identity is established before the mature microtubule arrangement is attained, during the period of mixed microtubule polarity.

The microtubule-severing protein fidgetin acts after dendrite injury to promote their degeneration

“…The protein could either be present in the dendrite before injury, but inactive, or could be locally translated in dendrites after injury. Ribosomes are present in dendrites of dendritic arborization neurons and concentrate at dendrite branch points (Hill et al, 2012) so either mechanism is possible. In future studies, it will be extremely interesting to determine how injury controls fidgetin levels or activity.…”

FoxO regulates microtubule dynamics and polarity to promote dendrite branching in Drosophila sensory neurons

“…Such studies have established that da neuron dendrites have mixed MT polarity during developmental stages characterized by rapid dendrite growth and branching (Hill et al, 2012). In other words, MT polymers are a mixture of plus-end-out (anterograde polymerizing) and minus-end-out (retrograde polymerizing) filaments.…”

Microtubule nucleation and organization in dendrites

“…49 In the differentiating dendrite, microtubule nucleation and polymerization events occur away from the centrosome and throughout the growing arbor. 20,[27][28][29]35 Although microtubule nucleation events are spread throughout the arbor, specific foci repeatedly give rise to microtubules, suggesting that particular subcellular structures within the dendrite have microtubule nucleating activity. Other structures, in addition to the centrosome, can focus g-tubulin-mediated microtubule nucleation.…”

“…Immature differentiating dendrites have a larger balance of anterograde distal microtubules than mature dendrites and anterograde polymerization events are concentrated in the growing terminal regions. 17,[27][28][29]35 The polymerization of plus-end distal microtubules drives neurite outgrowth during neuron differentiation, 59 and live imaging of growing dendrites in vivo shows anterograde polymerizing microtubules extending the termini of emerging branches leading to outgrowth and stabilization 20,35 (Fig. 3A).…”

“…8,26 Both plus-or minus-end directed microtubule arrays are established in dendrites from the earliest stages of neurite outgrowth. 17,20,[27][28][29] One mechanism to achieve this organization is via the action of microtubule motor proteins. Motor proteins either anchored to the cell cortex or spanning two microtubules can facilitate the sliding of preassembled microtubules from the soma into the dendrite.…”