Cargando…

The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila

Dendrites are the primary points of sensory or synaptic inputs to a neuron and play an essential role in synaptic integration and neural function. Despite the functional importance of dendrites, relatively less is known about the underlying mechanisms regulating cell-type specific dendritic patterni...

Descripción completa

Detalles Bibliográficos
Autores principales: Bhattacharjee, Shatabdi, Iyer, Eswar Prasad R., Iyer, Srividya Chandramouli, Nanda, Sumit, Rubaharan, Myurajan, Ascoli, Giorgio A., Cox, Daniel N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9948997/
https://www.ncbi.nlm.nih.gov/pubmed/36824896
http://dx.doi.org/10.1101/2023.02.15.528686
_version_ 1784892889828950016
author Bhattacharjee, Shatabdi
Iyer, Eswar Prasad R.
Iyer, Srividya Chandramouli
Nanda, Sumit
Rubaharan, Myurajan
Ascoli, Giorgio A.
Cox, Daniel N.
author_facet Bhattacharjee, Shatabdi
Iyer, Eswar Prasad R.
Iyer, Srividya Chandramouli
Nanda, Sumit
Rubaharan, Myurajan
Ascoli, Giorgio A.
Cox, Daniel N.
author_sort Bhattacharjee, Shatabdi
collection PubMed
description Dendrites are the primary points of sensory or synaptic inputs to a neuron and play an essential role in synaptic integration and neural function. Despite the functional importance of dendrites, relatively less is known about the underlying mechanisms regulating cell-type specific dendritic patterning. Herein, we have dissected functional roles of a previously uncharacterized gene, CG3995, in cell-type specific dendritic development in Drosophila melanogaster. CG3995, which we have named bedwarfed (bdwf), encodes a zinc-finger BED-type protein which is required for proportional growth and branching of dendritic arbors, exhibits nucleocytoplasmic expression, and functions in both transcriptional and translational cellular pathways. At the transcriptional level, we demonstrate a reciprocal regulatory relationship between Bdwf and the homeodomain transcription factor (TF) Cut. We show that Cut positively regulates Bdwf expression and that Bdwf acts as a downstream effector of Cut-mediated dendritic development, whereas overexpression of Bdwf negatively regulates Cut expression in multidendritic sensory neurons. Proteomic analyses revealed that Bdwf interacts with ribosomal proteins and disruption of these proteins produced phenotypically similar dendritic hypotrophy defects as observed in bdwf mutant neurons. We further demonstrate that Bdwf and its ribosomal protein interactors are required for normal microtubule and F-actin cytoskeletal architecture. Finally, our findings reveal that Bdwf is required to promote protein translation and ribosome trafficking along the dendritic arbor. Taken together, these results provide new insights into the complex, combinatorial and multi-functional roles of transcription factors (TFs) in directing diversification of cell-type specific dendritic development.
format Online
Article
Text
id pubmed-9948997
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-99489972023-02-24 The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila Bhattacharjee, Shatabdi Iyer, Eswar Prasad R. Iyer, Srividya Chandramouli Nanda, Sumit Rubaharan, Myurajan Ascoli, Giorgio A. Cox, Daniel N. bioRxiv Article Dendrites are the primary points of sensory or synaptic inputs to a neuron and play an essential role in synaptic integration and neural function. Despite the functional importance of dendrites, relatively less is known about the underlying mechanisms regulating cell-type specific dendritic patterning. Herein, we have dissected functional roles of a previously uncharacterized gene, CG3995, in cell-type specific dendritic development in Drosophila melanogaster. CG3995, which we have named bedwarfed (bdwf), encodes a zinc-finger BED-type protein which is required for proportional growth and branching of dendritic arbors, exhibits nucleocytoplasmic expression, and functions in both transcriptional and translational cellular pathways. At the transcriptional level, we demonstrate a reciprocal regulatory relationship between Bdwf and the homeodomain transcription factor (TF) Cut. We show that Cut positively regulates Bdwf expression and that Bdwf acts as a downstream effector of Cut-mediated dendritic development, whereas overexpression of Bdwf negatively regulates Cut expression in multidendritic sensory neurons. Proteomic analyses revealed that Bdwf interacts with ribosomal proteins and disruption of these proteins produced phenotypically similar dendritic hypotrophy defects as observed in bdwf mutant neurons. We further demonstrate that Bdwf and its ribosomal protein interactors are required for normal microtubule and F-actin cytoskeletal architecture. Finally, our findings reveal that Bdwf is required to promote protein translation and ribosome trafficking along the dendritic arbor. Taken together, these results provide new insights into the complex, combinatorial and multi-functional roles of transcription factors (TFs) in directing diversification of cell-type specific dendritic development. Cold Spring Harbor Laboratory 2023-02-15 /pmc/articles/PMC9948997/ /pubmed/36824896 http://dx.doi.org/10.1101/2023.02.15.528686 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Bhattacharjee, Shatabdi
Iyer, Eswar Prasad R.
Iyer, Srividya Chandramouli
Nanda, Sumit
Rubaharan, Myurajan
Ascoli, Giorgio A.
Cox, Daniel N.
The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title_full The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title_fullStr The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title_full_unstemmed The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title_short The Zinc-BED transcription factor Bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in Drosophila
title_sort zinc-bed transcription factor bedwarfed promotes proportional dendritic growth and branching through transcriptional and translational regulation in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9948997/
https://www.ncbi.nlm.nih.gov/pubmed/36824896
http://dx.doi.org/10.1101/2023.02.15.528686
work_keys_str_mv AT bhattacharjeeshatabdi thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT iyereswarprasadr thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT iyersrividyachandramouli thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT nandasumit thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT rubaharanmyurajan thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT ascoligiorgioa thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT coxdanieln thezincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT bhattacharjeeshatabdi zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT iyereswarprasadr zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT iyersrividyachandramouli zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT nandasumit zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT rubaharanmyurajan zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT ascoligiorgioa zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila
AT coxdanieln zincbedtranscriptionfactorbedwarfedpromotesproportionaldendriticgrowthandbranchingthroughtranscriptionalandtranslationalregulationindrosophila