Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila

Class IV ddaC neurons specifically prune larval dendrites without affecting axons during Drosophila metamorphosis. ddaCs distribute the minus ends of microtubules (MTs) to dendrites but the plus ends to axons. However, a requirement of MT minus-end-binding proteins in dendrite-specific pruning remai...

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Main Authors: Yan Wang, Menglong Rui, Quan Tang, Shufeng Bu, Fengwei Yu
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/39964
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author Yan Wang
Menglong Rui
Quan Tang
Shufeng Bu
Fengwei Yu
author_facet Yan Wang
Menglong Rui
Quan Tang
Shufeng Bu
Fengwei Yu
author_sort Yan Wang
collection DOAJ
description Class IV ddaC neurons specifically prune larval dendrites without affecting axons during Drosophila metamorphosis. ddaCs distribute the minus ends of microtubules (MTs) to dendrites but the plus ends to axons. However, a requirement of MT minus-end-binding proteins in dendrite-specific pruning remains completely unknown. Here, we identified Patronin, a minus-end-binding protein, for its crucial and dose-sensitive role in ddaC dendrite pruning. The CKK domain is important for Patronin’s function in dendrite pruning. Moreover, we show that both patronin knockdown and overexpression resulted in a drastic decrease of MT minus ends and a concomitant increase of plus-end-out MTs in ddaC dendrites, suggesting that Patronin stabilizes dendritic minus-end-out MTs. Consistently, attenuation of Klp10A MT depolymerase in patronin mutant neurons significantly restored minus-end-out MTs in dendrites and thereby rescued dendrite-pruning defects. Thus, our study demonstrates that Patronin orients minus-end-out MT arrays in dendrites to promote dendrite-specific pruning mainly through antagonizing Klp10A activity.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).
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spelling doaj.art-6bdc08a6502a43cda62a281011c947a42022-12-22T02:05:02ZengeLife Sciences Publications LtdeLife2050-084X2019-03-01810.7554/eLife.39964Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in DrosophilaYan Wang0Menglong Rui1Quan Tang2Shufeng Bu3Fengwei Yu4https://orcid.org/0000-0003-0268-199XTemasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore; NUS Graduate School for Integrative Sciences and Engineering, Centre for Life Sciences, National University of Singapore, Singapore, SingaporeTemasek Life Sciences Laboratory, National University of Singapore, Singapore, SingaporeTemasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore; Department of Biological Sciences, National University of Singapore, Singapore, SingaporeTemasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore; Department of Biological Sciences, National University of Singapore, Singapore, SingaporeTemasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore; NUS Graduate School for Integrative Sciences and Engineering, Centre for Life Sciences, National University of Singapore, Singapore, Singapore; Department of Biological Sciences, National University of Singapore, Singapore, Singapore; Neuroscience and Behavioral Disorder Program, Duke-NUS Graduate Medical School, National University of Singapore, Singapore, SingaporeClass IV ddaC neurons specifically prune larval dendrites without affecting axons during Drosophila metamorphosis. ddaCs distribute the minus ends of microtubules (MTs) to dendrites but the plus ends to axons. However, a requirement of MT minus-end-binding proteins in dendrite-specific pruning remains completely unknown. Here, we identified Patronin, a minus-end-binding protein, for its crucial and dose-sensitive role in ddaC dendrite pruning. The CKK domain is important for Patronin’s function in dendrite pruning. Moreover, we show that both patronin knockdown and overexpression resulted in a drastic decrease of MT minus ends and a concomitant increase of plus-end-out MTs in ddaC dendrites, suggesting that Patronin stabilizes dendritic minus-end-out MTs. Consistently, attenuation of Klp10A MT depolymerase in patronin mutant neurons significantly restored minus-end-out MTs in dendrites and thereby rescued dendrite-pruning defects. Thus, our study demonstrates that Patronin orients minus-end-out MT arrays in dendrites to promote dendrite-specific pruning mainly through antagonizing Klp10A activity.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).https://elifesciences.org/articles/39964microtubule orientationminus enddendriteneurondendrite morphologypruning
spellingShingle Yan Wang
Menglong Rui
Quan Tang
Shufeng Bu
Fengwei Yu
Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
eLife
microtubule orientation
minus end
dendrite
neuron
dendrite morphology
pruning
title Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
title_full Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
title_fullStr Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
title_full_unstemmed Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
title_short Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila
title_sort patronin governs minus end out orientation of dendritic microtubules to promote dendrite pruning in drosophila
topic microtubule orientation
minus end
dendrite
neuron
dendrite morphology
pruning
url https://elifesciences.org/articles/39964
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AT shufengbu patroningovernsminusendoutorientationofdendriticmicrotubulestopromotedendritepruningindrosophila
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