A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis

Localizing messenger RNAs at specific subcellular sites is a conserved mechanism for targeting the synthesis of cytoplasmic proteins to distinct subcellular domains, thereby generating the asymmetric protein distributions necessary for cellular and developmental polarity. However, the full range of...

Full description

Bibliographic Details
Main Authors: Mala Misra, Hendia Edmund, Darragh Ennis, Marissa A. Schlueter, Jessica E. Marot, Janet Tambasco, Ida Barlow, Sara Sigurbjornsdottir, Renjith Mathew, Ana Maria Vallés, Waldemar Wojciech, Siegfried Roth, Ilan Davis, Maria Leptin, Elizabeth R. Gavis
Format: Article
Language:English
Published: Oxford University Press 2016-08-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.116.030353
id doaj-2bad0e4bb34c4c1da8dd52894465a0b5
record_format Article
spelling doaj-2bad0e4bb34c4c1da8dd52894465a0b52021-07-02T09:48:56ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362016-08-01682397240510.1534/g3.116.03035315A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite MorphogenesisMala MisraHendia EdmundDarragh EnnisMarissa A. SchlueterJessica E. MarotJanet TambascoIda BarlowSara SigurbjornsdottirRenjith MathewAna Maria VallésWaldemar WojciechSiegfried RothIlan DavisMaria LeptinElizabeth R. GavisLocalizing messenger RNAs at specific subcellular sites is a conserved mechanism for targeting the synthesis of cytoplasmic proteins to distinct subcellular domains, thereby generating the asymmetric protein distributions necessary for cellular and developmental polarity. However, the full range of transcripts that are asymmetrically distributed in specialized cell types, and the significance of their localization, especially in the nervous system, are not known. We used the EP-MS2 method, which combines EP transposon insertion with the MS2/MCP in vivo fluorescent labeling system, to screen for novel localized transcripts in polarized cells, focusing on the highly branched Drosophila class IV dendritic arborization neurons. Of a total of 541 lines screened, we identified 55 EP-MS2 insertions producing transcripts that were enriched in neuronal processes, particularly in dendrites. The 47 genes identified by these insertions encode molecularly diverse proteins, and are enriched for genes that function in neuronal development and physiology. RNAi-mediated knockdown confirmed roles for many of the candidate genes in dendrite morphogenesis. We propose that the transport of mRNAs encoded by these genes into the dendrites allows their expression to be regulated on a local scale during the dynamic developmental processes of dendrite outgrowth, branching, and/or remodeling.http://g3journal.org/lookup/doi/10.1534/g3.116.030353mRNA localizationlocal translationdendritic arborization neuronmultidendritic neuronDrosophila peripheral nervous system
collection DOAJ
language English
format Article
sources DOAJ
author Mala Misra
Hendia Edmund
Darragh Ennis
Marissa A. Schlueter
Jessica E. Marot
Janet Tambasco
Ida Barlow
Sara Sigurbjornsdottir
Renjith Mathew
Ana Maria Vallés
Waldemar Wojciech
Siegfried Roth
Ilan Davis
Maria Leptin
Elizabeth R. Gavis
spellingShingle Mala Misra
Hendia Edmund
Darragh Ennis
Marissa A. Schlueter
Jessica E. Marot
Janet Tambasco
Ida Barlow
Sara Sigurbjornsdottir
Renjith Mathew
Ana Maria Vallés
Waldemar Wojciech
Siegfried Roth
Ilan Davis
Maria Leptin
Elizabeth R. Gavis
A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
G3: Genes, Genomes, Genetics
mRNA localization
local translation
dendritic arborization neuron
multidendritic neuron
Drosophila peripheral nervous system
author_facet Mala Misra
Hendia Edmund
Darragh Ennis
Marissa A. Schlueter
Jessica E. Marot
Janet Tambasco
Ida Barlow
Sara Sigurbjornsdottir
Renjith Mathew
Ana Maria Vallés
Waldemar Wojciech
Siegfried Roth
Ilan Davis
Maria Leptin
Elizabeth R. Gavis
author_sort Mala Misra
title A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
title_short A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
title_full A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
title_fullStr A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
title_full_unstemmed A Genome-Wide Screen for Dendritically Localized RNAs Identifies Genes Required for Dendrite Morphogenesis
title_sort genome-wide screen for dendritically localized rnas identifies genes required for dendrite morphogenesis
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2016-08-01
description Localizing messenger RNAs at specific subcellular sites is a conserved mechanism for targeting the synthesis of cytoplasmic proteins to distinct subcellular domains, thereby generating the asymmetric protein distributions necessary for cellular and developmental polarity. However, the full range of transcripts that are asymmetrically distributed in specialized cell types, and the significance of their localization, especially in the nervous system, are not known. We used the EP-MS2 method, which combines EP transposon insertion with the MS2/MCP in vivo fluorescent labeling system, to screen for novel localized transcripts in polarized cells, focusing on the highly branched Drosophila class IV dendritic arborization neurons. Of a total of 541 lines screened, we identified 55 EP-MS2 insertions producing transcripts that were enriched in neuronal processes, particularly in dendrites. The 47 genes identified by these insertions encode molecularly diverse proteins, and are enriched for genes that function in neuronal development and physiology. RNAi-mediated knockdown confirmed roles for many of the candidate genes in dendrite morphogenesis. We propose that the transport of mRNAs encoded by these genes into the dendrites allows their expression to be regulated on a local scale during the dynamic developmental processes of dendrite outgrowth, branching, and/or remodeling.
topic mRNA localization
local translation
dendritic arborization neuron
multidendritic neuron
Drosophila peripheral nervous system
url http://g3journal.org/lookup/doi/10.1534/g3.116.030353
work_keys_str_mv AT malamisra agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT hendiaedmund agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT darraghennis agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT marissaaschlueter agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT jessicaemarot agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT janettambasco agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT idabarlow agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT sarasigurbjornsdottir agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT renjithmathew agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT anamariavalles agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT waldemarwojciech agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT siegfriedroth agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT ilandavis agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT marialeptin agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT elizabethrgavis agenomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT malamisra genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT hendiaedmund genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT darraghennis genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT marissaaschlueter genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT jessicaemarot genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT janettambasco genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT idabarlow genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT sarasigurbjornsdottir genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT renjithmathew genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT anamariavalles genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT waldemarwojciech genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT siegfriedroth genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT ilandavis genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT marialeptin genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
AT elizabethrgavis genomewidescreenfordendriticallylocalizedrnasidentifiesgenesrequiredfordendritemorphogenesis
_version_ 1721332738456289280