Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.

The generation of distinct neuronal subtypes at different axial levels relies upon both anteroposterior and temporal cues. However, the integration between these cues is poorly understood. In the Drosophila central nervous system, the segmentally repeated neuroblast 5-6 generates a unique group of n...

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Autores principales: Daniel Karlsson, Magnus Baumgardt, Stefan Thor
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Publicado: Public Library of Science (PLoS) 2010
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spelling oai:doaj.org-article:68bb0d582aa9412e9b5cd18a4f7b2aa22021-12-02T19:54:51ZSegment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.1544-91731545-788510.1371/journal.pbio.1000368https://doaj.org/article/68bb0d582aa9412e9b5cd18a4f7b2aa22010-05-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20485487/pdf/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885The generation of distinct neuronal subtypes at different axial levels relies upon both anteroposterior and temporal cues. However, the integration between these cues is poorly understood. In the Drosophila central nervous system, the segmentally repeated neuroblast 5-6 generates a unique group of neurons, the Apterous (Ap) cluster, only in thoracic segments. Recent studies have identified elaborate genetic pathways acting to control the generation of these neurons. These insights, combined with novel markers, provide a unique opportunity for addressing how anteroposterior and temporal cues are integrated to generate segment-specific neuronal subtypes. We find that Pbx/Meis, Hox, and temporal genes act in three different ways. Posteriorly, Pbx/Meis and posterior Hox genes block lineage progression within an early temporal window, by triggering cell cycle exit. Because Ap neurons are generated late in the thoracic 5-6 lineage, this prevents generation of Ap cluster cells in the abdomen. Thoracically, Pbx/Meis and anterior Hox genes integrate with late temporal genes to specify Ap clusters, via activation of a specific feed-forward loop. In brain segments, "Ap cluster cells" are present but lack both proper Hox and temporal coding. Only by simultaneously altering Hox and temporal gene activity in all segments can Ap clusters be generated throughout the neuroaxis. This study provides the first detailed analysis, to our knowledge, of an identified neuroblast lineage along the entire neuroaxis, and confirms the concept that lineal homologs of truncal neuroblasts exist throughout the developing brain. We furthermore provide the first insight into how Hox/Pbx/Meis anteroposterior and temporal cues are integrated within a defined lineage, to specify unique neuronal identities only in thoracic segments. This study reveals a surprisingly restricted, yet multifaceted, function of both anteroposterior and temporal cues with respect to lineage control and cell fate specification.Daniel KarlssonMagnus BaumgardtStefan ThorPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 8, Iss 5, p e1000368 (2010)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Daniel Karlsson
Magnus Baumgardt
Stefan Thor
Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
description The generation of distinct neuronal subtypes at different axial levels relies upon both anteroposterior and temporal cues. However, the integration between these cues is poorly understood. In the Drosophila central nervous system, the segmentally repeated neuroblast 5-6 generates a unique group of neurons, the Apterous (Ap) cluster, only in thoracic segments. Recent studies have identified elaborate genetic pathways acting to control the generation of these neurons. These insights, combined with novel markers, provide a unique opportunity for addressing how anteroposterior and temporal cues are integrated to generate segment-specific neuronal subtypes. We find that Pbx/Meis, Hox, and temporal genes act in three different ways. Posteriorly, Pbx/Meis and posterior Hox genes block lineage progression within an early temporal window, by triggering cell cycle exit. Because Ap neurons are generated late in the thoracic 5-6 lineage, this prevents generation of Ap cluster cells in the abdomen. Thoracically, Pbx/Meis and anterior Hox genes integrate with late temporal genes to specify Ap clusters, via activation of a specific feed-forward loop. In brain segments, "Ap cluster cells" are present but lack both proper Hox and temporal coding. Only by simultaneously altering Hox and temporal gene activity in all segments can Ap clusters be generated throughout the neuroaxis. This study provides the first detailed analysis, to our knowledge, of an identified neuroblast lineage along the entire neuroaxis, and confirms the concept that lineal homologs of truncal neuroblasts exist throughout the developing brain. We furthermore provide the first insight into how Hox/Pbx/Meis anteroposterior and temporal cues are integrated within a defined lineage, to specify unique neuronal identities only in thoracic segments. This study reveals a surprisingly restricted, yet multifaceted, function of both anteroposterior and temporal cues with respect to lineage control and cell fate specification.
format article
author Daniel Karlsson
Magnus Baumgardt
Stefan Thor
author_facet Daniel Karlsson
Magnus Baumgardt
Stefan Thor
author_sort Daniel Karlsson
title Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
title_short Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
title_full Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
title_fullStr Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
title_full_unstemmed Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
title_sort segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues.
publisher Public Library of Science (PLoS)
publishDate 2010
url https://doaj.org/article/68bb0d582aa9412e9b5cd18a4f7b2aa2
work_keys_str_mv AT danielkarlsson segmentspecificneuronalsubtypespecificationbytheintegrationofanteroposteriorandtemporalcues
AT magnusbaumgardt segmentspecificneuronalsubtypespecificationbytheintegrationofanteroposteriorandtemporalcues
AT stefanthor segmentspecificneuronalsubtypespecificationbytheintegrationofanteroposteriorandtemporalcues
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