Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification

Homeobox genes are prominent regulators of neuronal identity, but the extent to which their function has been probed in animal nervous systems remains limited. In the nematode Caenorhabditis elegans, each individual neuron class is defined by the expression of unique combinations of homeobox genes,...

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Autores: Reilly, Molly B, Tekieli, Tessa, Cros, Cyril, Aguilar, G. Robert, Lao, James, Toker, Itai Antoine, Vidal, Berta, Leyva-Díaz, Eduardo, Bhattacharya, Abhishek, Cook, Steven J., Smith, Jayson J., Kovacevic, Ismar, Gulez, Burcu, Fernández, Robert W., Bradford, Elisabeth F
Tipo de recurso: artículo
Fecha de publicación:2022
País:España
Institución:Universidad Miguel Hernández de Elche
Repositorio:REDIUMH. Depósito Digital de la UMH
OAI Identifier:oai:dspace.umh.es:11000/38431
Acceso en línea:https://hdl.handle.net/11000/38431
Access Level:acceso abierto
Palabra clave:Homeobox genes
Caenorhabditis elegans
NeuroPAL
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spelling Widespread employment of conserved C. elegans homeobox genes in neuronal identity specificationReilly, Molly BTekieli, TessaCros, CyrilAguilar, G. RobertLao, JamesToker, Itai AntoineVidal, BertaLeyva-Díaz, EduardoBhattacharya, AbhishekCook, Steven J.Smith, Jayson J.Kovacevic, IsmarGulez, BurcuFernández, Robert W.Bradford, Elisabeth FHomeobox genesCaenorhabditis elegansNeuroPALHomeobox genes are prominent regulators of neuronal identity, but the extent to which their function has been probed in animal nervous systems remains limited. In the nematode Caenorhabditis elegans, each individual neuron class is defined by the expression of unique combinations of homeobox genes, prompting the question of whether each neuron class indeed requires a homeobox gene for its proper identity specification. We present here progress in addressing this question by extending previous mutant analysis of homeobox gene family members and describing multiple examples of homeobox gene function in different parts of the C. elegans nervous system. To probe homeobox function, we make use of a number of reporter gene tools, including a novel multicolor reporter transgene, NeuroPAL, which permits simultaneous monitoring of the execution of multiple differentiation programs throughout the entire nervous system. Using these tools, we add to the previous characterization of homeobox gene function by identifying neuronal differentiation defects for 14 homeobox genes in 24 distinct neuron classes that are mostly unrelated by location, function and lineage history. 12 of these 24 neuron classes had no homeobox gene function ascribed to them before, while in the other 12 neuron classes, we extend the combinatorial code of transcription factors required for specifying terminal differentiation programs. Furthermore, we demonstrate that in a particular lineage, homeotic identity transformations occur upon loss of a homeobox gene and we show that these transformations are the result of changes in homeobox codes. Combining the present with past analyses, 113 of the 118 neuron classes of C. elegans are now known to require a homeobox gene for proper execution of terminal differentiation programs. Such broad deployment indicates that homeobox function in neuronal identity specification may be an ancestral feature of animal nervous systems.PMCInstitutos de la UMH::Instituto de Neurociencias202520252022info:eu-repo/semantics/articleapplication/pdf41application/pdfhttps://hdl.handle.net/11000/38431reponame:REDIUMH. Depósito Digital de la UMHinstname:Universidad Miguel Hernández de ElcheInglés10.1371/journal.pgen.1010372info:eu-repo/semantics/openAccessAttribution-NonCommercial-NoDerivatives 4.0 Internacionalhttp://creativecommons.org/licenses/by-nc-nd/4.0/oai:dspace.umh.es:11000/384312026-05-27T13:36:21Z
dc.title.none.fl_str_mv Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
title Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
spellingShingle Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
Reilly, Molly B
Homeobox genes
Caenorhabditis elegans
NeuroPAL
title_short Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
title_full Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
title_fullStr Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
title_full_unstemmed Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
title_sort Widespread employment of conserved C. elegans homeobox genes in neuronal identity specification
dc.creator.none.fl_str_mv Reilly, Molly B
Tekieli, Tessa
Cros, Cyril
Aguilar, G. Robert
Lao, James
Toker, Itai Antoine
Vidal, Berta
Leyva-Díaz, Eduardo
Bhattacharya, Abhishek
Cook, Steven J.
Smith, Jayson J.
Kovacevic, Ismar
Gulez, Burcu
Fernández, Robert W.
Bradford, Elisabeth F
author Reilly, Molly B
author_facet Reilly, Molly B
Tekieli, Tessa
Cros, Cyril
Aguilar, G. Robert
Lao, James
Toker, Itai Antoine
Vidal, Berta
Leyva-Díaz, Eduardo
Bhattacharya, Abhishek
Cook, Steven J.
Smith, Jayson J.
Kovacevic, Ismar
Gulez, Burcu
Fernández, Robert W.
Bradford, Elisabeth F
author_role author
author2 Tekieli, Tessa
Cros, Cyril
Aguilar, G. Robert
Lao, James
Toker, Itai Antoine
Vidal, Berta
Leyva-Díaz, Eduardo
Bhattacharya, Abhishek
Cook, Steven J.
Smith, Jayson J.
Kovacevic, Ismar
Gulez, Burcu
Fernández, Robert W.
Bradford, Elisabeth F
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Institutos de la UMH::Instituto de Neurociencias
dc.subject.none.fl_str_mv Homeobox genes
Caenorhabditis elegans
NeuroPAL
topic Homeobox genes
Caenorhabditis elegans
NeuroPAL
description Homeobox genes are prominent regulators of neuronal identity, but the extent to which their function has been probed in animal nervous systems remains limited. In the nematode Caenorhabditis elegans, each individual neuron class is defined by the expression of unique combinations of homeobox genes, prompting the question of whether each neuron class indeed requires a homeobox gene for its proper identity specification. We present here progress in addressing this question by extending previous mutant analysis of homeobox gene family members and describing multiple examples of homeobox gene function in different parts of the C. elegans nervous system. To probe homeobox function, we make use of a number of reporter gene tools, including a novel multicolor reporter transgene, NeuroPAL, which permits simultaneous monitoring of the execution of multiple differentiation programs throughout the entire nervous system. Using these tools, we add to the previous characterization of homeobox gene function by identifying neuronal differentiation defects for 14 homeobox genes in 24 distinct neuron classes that are mostly unrelated by location, function and lineage history. 12 of these 24 neuron classes had no homeobox gene function ascribed to them before, while in the other 12 neuron classes, we extend the combinatorial code of transcription factors required for specifying terminal differentiation programs. Furthermore, we demonstrate that in a particular lineage, homeotic identity transformations occur upon loss of a homeobox gene and we show that these transformations are the result of changes in homeobox codes. Combining the present with past analyses, 113 of the 118 neuron classes of C. elegans are now known to require a homeobox gene for proper execution of terminal differentiation programs. Such broad deployment indicates that homeobox function in neuronal identity specification may be an ancestral feature of animal nervous systems.
publishDate 2022
dc.date.none.fl_str_mv 2022
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/11000/38431
url https://hdl.handle.net/11000/38431
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv 10.1371/journal.pgen.1010372
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
Attribution-NonCommercial-NoDerivatives 4.0 Internacional
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
rights_invalid_str_mv Attribution-NonCommercial-NoDerivatives 4.0 Internacional
http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.format.none.fl_str_mv application/pdf
41
application/pdf
dc.publisher.none.fl_str_mv PMC
publisher.none.fl_str_mv PMC
dc.source.none.fl_str_mv reponame:REDIUMH. Depósito Digital de la UMH
instname:Universidad Miguel Hernández de Elche
instname_str Universidad Miguel Hernández de Elche
reponame_str REDIUMH. Depósito Digital de la UMH
collection REDIUMH. Depósito Digital de la UMH
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,81155

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