The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.

In neurogenesis, neural cell fate specification is generally triggered by proneural transcription factors. Whilst the role of proneural factors in fate specification is well studied, the link between neural specification and the cellular pathways that ultimately must be activated to construct specia...

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Main Authors: Sebastián Cachero, T Ian Simpson, Petra I Zur Lage, Lina Ma, Fay G Newton, Eimear E Holohan, J Douglas Armstrong, Andrew P Jarman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC3023811?pdf=render
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author Sebastián Cachero
T Ian Simpson
Petra I Zur Lage
Lina Ma
Fay G Newton
Eimear E Holohan
J Douglas Armstrong
Andrew P Jarman
author_facet Sebastián Cachero
T Ian Simpson
Petra I Zur Lage
Lina Ma
Fay G Newton
Eimear E Holohan
J Douglas Armstrong
Andrew P Jarman
author_sort Sebastián Cachero
collection DOAJ
description In neurogenesis, neural cell fate specification is generally triggered by proneural transcription factors. Whilst the role of proneural factors in fate specification is well studied, the link between neural specification and the cellular pathways that ultimately must be activated to construct specialised neurons is usually obscure. High-resolution temporal profiling of gene expression reveals the events downstream of atonal proneural gene function during the development of Drosophila chordotonal (mechanosensory) neurons. Among other findings, this reveals the onset of expression of genes required for construction of the ciliary dendrite, a key specialisation of mechanosensory neurons. We determine that atonal activates this cellular differentiation pathway in several ways. Firstly, atonal directly regulates Rfx, a well-known highly conserved ciliogenesis transcriptional regulator. Unexpectedly, differences in Rfx regulation by proneural factors may underlie variations in ciliary dendrite specialisation in different sensory neuronal lineages. In contrast, fd3F encodes a novel forkhead family transcription factor that is exclusively expressed in differentiating chordotonal neurons. fd3F regulates genes required for specialized aspects of chordotonal dendrite physiology. In addition to these intermediate transcriptional regulators, we show that atonal directly regulates a novel gene, dilatory, that is directly associated with ciliogenesis during neuronal differentiation. Our analysis demonstrates how early cell fate specification factors can regulate structural and physiological differentiation of neuronal cell types. It also suggests a model for how subtype differentiation in different neuronal lineages may be regulated by different proneural factors. In addition, it provides a paradigm for how transcriptional regulation may modulate the ciliogenesis pathway to give rise to structurally and functionally specialised ciliary dendrites.
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spelling doaj.art-c97cd70a54824f1a88123db0f4d0d5512022-12-21T22:04:34ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852011-01-0191e100056810.1371/journal.pbio.1000568The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.Sebastián CacheroT Ian SimpsonPetra I Zur LageLina MaFay G NewtonEimear E HolohanJ Douglas ArmstrongAndrew P JarmanIn neurogenesis, neural cell fate specification is generally triggered by proneural transcription factors. Whilst the role of proneural factors in fate specification is well studied, the link between neural specification and the cellular pathways that ultimately must be activated to construct specialised neurons is usually obscure. High-resolution temporal profiling of gene expression reveals the events downstream of atonal proneural gene function during the development of Drosophila chordotonal (mechanosensory) neurons. Among other findings, this reveals the onset of expression of genes required for construction of the ciliary dendrite, a key specialisation of mechanosensory neurons. We determine that atonal activates this cellular differentiation pathway in several ways. Firstly, atonal directly regulates Rfx, a well-known highly conserved ciliogenesis transcriptional regulator. Unexpectedly, differences in Rfx regulation by proneural factors may underlie variations in ciliary dendrite specialisation in different sensory neuronal lineages. In contrast, fd3F encodes a novel forkhead family transcription factor that is exclusively expressed in differentiating chordotonal neurons. fd3F regulates genes required for specialized aspects of chordotonal dendrite physiology. In addition to these intermediate transcriptional regulators, we show that atonal directly regulates a novel gene, dilatory, that is directly associated with ciliogenesis during neuronal differentiation. Our analysis demonstrates how early cell fate specification factors can regulate structural and physiological differentiation of neuronal cell types. It also suggests a model for how subtype differentiation in different neuronal lineages may be regulated by different proneural factors. In addition, it provides a paradigm for how transcriptional regulation may modulate the ciliogenesis pathway to give rise to structurally and functionally specialised ciliary dendrites.http://europepmc.org/articles/PMC3023811?pdf=render
spellingShingle Sebastián Cachero
T Ian Simpson
Petra I Zur Lage
Lina Ma
Fay G Newton
Eimear E Holohan
J Douglas Armstrong
Andrew P Jarman
The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
PLoS Biology
title The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
title_full The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
title_fullStr The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
title_full_unstemmed The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
title_short The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons.
title_sort gene regulatory cascade linking proneural specification with differentiation in drosophila sensory neurons
url http://europepmc.org/articles/PMC3023811?pdf=render
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