Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans

Autores
Chute, Christopher D.; DiLoreto, Elizabeth M.; Zhang, Ying K.; Reilly, Douglas K.; Rayes, Diego Hernán; Coyle, Veronica L.; Choi, Hee June; Alkema, Mark J.; Schroeder, Frank C.; Srinivasan, Jagan
Año de publicación
2019
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.
Fil: Chute, Christopher D.. Worcester Polytechnic Institute; Estados Unidos
Fil: DiLoreto, Elizabeth M.. Worcester Polytechnic Institute; Estados Unidos
Fil: Zhang, Ying K.. Cornell University; Estados Unidos
Fil: Reilly, Douglas K.. Worcester Polytechnic Institute; Estados Unidos
Fil: Rayes, Diego Hernán. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca. Instituto de Investigaciones Bioquímicas de Bahía Blanca. Universidad Nacional del Sur. Instituto de Investigaciones Bioquímicas de Bahía Blanca; Argentina. Universidad Nacional del Sur. Departamento de Biología, Bioquímica y Farmacia; Argentina
Fil: Coyle, Veronica L.. Worcester Polytechnic Institute; Estados Unidos
Fil: Choi, Hee June. Worcester Polytechnic Institute; Estados Unidos
Fil: Alkema, Mark J.. University of Massachussets; Estados Unidos
Fil: Schroeder, Frank C.. Cornell University; Estados Unidos
Fil: Srinivasan, Jagan. Worcester Polytechnic Institute; Estados Unidos
Materia
Tyra-2
pheromone
communication
behavior
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/99041
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/99041
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Co-option of neurotransmitter signaling for inter-organismal communication in C. elegansChute, Christopher D.DiLoreto, Elizabeth M.Zhang, Ying K.Reilly, Douglas K.Rayes, Diego HernánCoyle, Veronica L.Choi, Hee JuneAlkema, Mark J.Schroeder, Frank C.Srinivasan, JaganTyra-2pheromonecommunicationbehaviorhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.Fil: Chute, Christopher D.. Worcester Polytechnic Institute; Estados UnidosFil: DiLoreto, Elizabeth M.. Worcester Polytechnic Institute; Estados UnidosFil: Zhang, Ying K.. Cornell University; Estados UnidosFil: Reilly, Douglas K.. Worcester Polytechnic Institute; Estados UnidosFil: Rayes, Diego Hernán. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca. Instituto de Investigaciones Bioquímicas de Bahía Blanca. Universidad Nacional del Sur. Instituto de Investigaciones Bioquímicas de Bahía Blanca; Argentina. Universidad Nacional del Sur. Departamento de Biología, Bioquímica y Farmacia; ArgentinaFil: Coyle, Veronica L.. Worcester Polytechnic Institute; Estados UnidosFil: Choi, Hee June. Worcester Polytechnic Institute; Estados UnidosFil: Alkema, Mark J.. University of Massachussets; Estados UnidosFil: Schroeder, Frank C.. Cornell University; Estados UnidosFil: Srinivasan, Jagan. Worcester Polytechnic Institute; Estados UnidosNature2019-07-18info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/99041Chute, Christopher D.; DiLoreto, Elizabeth M.; Zhang, Ying K.; Reilly, Douglas K.; Rayes, Diego Hernán; et al.; Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans; Nature; Nature Communications; 10; 1; 18-7-2019; 1-132041-1723CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-019-11240-7info:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-019-11240-7info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:32:20Zoai:ri.conicet.gov.ar:11336/99041instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:32:20.652CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
title Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
spellingShingle Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
Chute, Christopher D.
Tyra-2
pheromone
communication
behavior
title_short Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
title_full Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
title_fullStr Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
title_full_unstemmed Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
title_sort Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans
dc.creator.none.fl_str_mv Chute, Christopher D.
DiLoreto, Elizabeth M.
Zhang, Ying K.
Reilly, Douglas K.
Rayes, Diego Hernán
Coyle, Veronica L.
Choi, Hee June
Alkema, Mark J.
Schroeder, Frank C.
Srinivasan, Jagan
author Chute, Christopher D.
author_facet Chute, Christopher D.
DiLoreto, Elizabeth M.
Zhang, Ying K.
Reilly, Douglas K.
Rayes, Diego Hernán
Coyle, Veronica L.
Choi, Hee June
Alkema, Mark J.
Schroeder, Frank C.
Srinivasan, Jagan
author_role author
author2 DiLoreto, Elizabeth M.
Zhang, Ying K.
Reilly, Douglas K.
Rayes, Diego Hernán
Coyle, Veronica L.
Choi, Hee June
Alkema, Mark J.
Schroeder, Frank C.
Srinivasan, Jagan
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Tyra-2
pheromone
communication
behavior
topic Tyra-2
pheromone
communication
behavior
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.
Fil: Chute, Christopher D.. Worcester Polytechnic Institute; Estados Unidos
Fil: DiLoreto, Elizabeth M.. Worcester Polytechnic Institute; Estados Unidos
Fil: Zhang, Ying K.. Cornell University; Estados Unidos
Fil: Reilly, Douglas K.. Worcester Polytechnic Institute; Estados Unidos
Fil: Rayes, Diego Hernán. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca. Instituto de Investigaciones Bioquímicas de Bahía Blanca. Universidad Nacional del Sur. Instituto de Investigaciones Bioquímicas de Bahía Blanca; Argentina. Universidad Nacional del Sur. Departamento de Biología, Bioquímica y Farmacia; Argentina
Fil: Coyle, Veronica L.. Worcester Polytechnic Institute; Estados Unidos
Fil: Choi, Hee June. Worcester Polytechnic Institute; Estados Unidos
Fil: Alkema, Mark J.. University of Massachussets; Estados Unidos
Fil: Schroeder, Frank C.. Cornell University; Estados Unidos
Fil: Srinivasan, Jagan. Worcester Polytechnic Institute; Estados Unidos
description Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.
publishDate 2019
dc.date.none.fl_str_mv 2019-07-18
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/99041
Chute, Christopher D.; DiLoreto, Elizabeth M.; Zhang, Ying K.; Reilly, Douglas K.; Rayes, Diego Hernán; et al.; Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans; Nature; Nature Communications; 10; 1; 18-7-2019; 1-13
2041-1723
CONICET Digital
CONICET
url http://hdl.handle.net/11336/99041
identifier_str_mv Chute, Christopher D.; DiLoreto, Elizabeth M.; Zhang, Ying K.; Reilly, Douglas K.; Rayes, Diego Hernán; et al.; Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans; Nature; Nature Communications; 10; 1; 18-7-2019; 1-13
2041-1723
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-019-11240-7
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-019-11240-7
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature
publisher.none.fl_str_mv Nature
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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