Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans

Autores
Hughes, Kiley; Shah, Ashka; Bai, Xiaofei; Adams, Jessica; Bauer, Rosemary; Jackson, Janelle; Harris, Emily; Ficca, Alyson; Freebairn, Ploy; Mohammed, Shawn; Fernandez, Eliana Mailen; Bainbridge, Chance; Brocco, Marcela Adriana; Stein, Wolfgang; Vidal Gadea, Andrés G.
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the tissues they are expressed in remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have 12 isoforms. These isoforms share many transmembrane domains but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. We used transcriptional and translational reporters to show that putative promoter sequences immediately upstream of the start codon of long pezo-1 isoforms predominantly drive green fluorescent protein (GFP) expression in mesodermally derived tissues (such as muscle and glands). In contrast, sequences upstream of shorter pezo-1 isoforms resulted in GFP expression primarily in neurons. Putative promoters upstream of different isoforms drove GFP expression in different cells of the same organs of the digestive system. The observed unique pattern of complementary expression suggests that different isoforms could possess distinct functions within these organs. We used mutant analysis to show that pharyngeal muscles and glands require long pezo-1 isoforms to respond appropriately to the presence of food. The number of pezo-1 isoforms in C. elegans, their putative differential pattern of expression, and roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors.
Fil: Hughes, Kiley. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Shah, Ashka. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Bai, Xiaofei. National Institutes of Health; Estados Unidos
Fil: Adams, Jessica. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Bauer, Rosemary. University of Chicago; Estados Unidos
Fil: Jackson, Janelle. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Harris, Emily. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Ficca, Alyson. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Freebairn, Ploy. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Mohammed, Shawn. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Fernandez, Eliana Mailen. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Bainbridge, Chance. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Brocco, Marcela Adriana. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Stein, Wolfgang. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Vidal Gadea, Andrés G.. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Materia
BEHAVIOR
MECHANOSENSATION
PEZO-1
PHARYNGEAL GLANDS
PHARYNGEAL PUMPING
PIEZO
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/182475
Acceder
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegansHughes, KileyShah, AshkaBai, XiaofeiAdams, JessicaBauer, RosemaryJackson, JanelleHarris, EmilyFicca, AlysonFreebairn, PloyMohammed, ShawnFernandez, Eliana MailenBainbridge, ChanceBrocco, Marcela AdrianaStein, WolfgangVidal Gadea, Andrés G.BEHAVIORMECHANOSENSATIONPEZO-1PHARYNGEAL GLANDSPHARYNGEAL PUMPINGPIEZOhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the tissues they are expressed in remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have 12 isoforms. These isoforms share many transmembrane domains but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. We used transcriptional and translational reporters to show that putative promoter sequences immediately upstream of the start codon of long pezo-1 isoforms predominantly drive green fluorescent protein (GFP) expression in mesodermally derived tissues (such as muscle and glands). In contrast, sequences upstream of shorter pezo-1 isoforms resulted in GFP expression primarily in neurons. Putative promoters upstream of different isoforms drove GFP expression in different cells of the same organs of the digestive system. The observed unique pattern of complementary expression suggests that different isoforms could possess distinct functions within these organs. We used mutant analysis to show that pharyngeal muscles and glands require long pezo-1 isoforms to respond appropriately to the presence of food. The number of pezo-1 isoforms in C. elegans, their putative differential pattern of expression, and roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors.Fil: Hughes, Kiley. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Shah, Ashka. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Bai, Xiaofei. National Institutes of Health; Estados UnidosFil: Adams, Jessica. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Bauer, Rosemary. University of Chicago; Estados UnidosFil: Jackson, Janelle. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Harris, Emily. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Ficca, Alyson. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Freebairn, Ploy. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Mohammed, Shawn. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Fernandez, Eliana Mailen. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Bainbridge, Chance. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Brocco, Marcela Adriana. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Stein, Wolfgang. University Of Illinois. Deparment Of Biological Science; Estados UnidosFil: Vidal Gadea, Andrés G.. University Of Illinois. Deparment Of Biological Science; Estados UnidosGenetics Society of America2021-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/182475Hughes, Kiley; Shah, Ashka; Bai, Xiaofei; Adams, Jessica; Bauer, Rosemary; et al.; Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans; Genetics Society of America; G3: Genes, Genomes, Genetics; 12; 3; 12-2021; 1-132160-1836CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/g3journal/advance-article/doi/10.1093/g3journal/jkab429/6462202info:eu-repo/semantics/altIdentifier/doi/10.1093/g3journal/jkab429info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:12:45Zoai:ri.conicet.gov.ar:11336/182475instacron: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 10:12:45.329CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
title Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
spellingShingle Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
Hughes, Kiley
BEHAVIOR
MECHANOSENSATION
PEZO-1
PHARYNGEAL GLANDS
PHARYNGEAL PUMPING
PIEZO
title_short Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
title_full Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
title_fullStr Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
title_full_unstemmed Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
title_sort Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
dc.creator.none.fl_str_mv Hughes, Kiley
Shah, Ashka
Bai, Xiaofei
Adams, Jessica
Bauer, Rosemary
Jackson, Janelle
Harris, Emily
Ficca, Alyson
Freebairn, Ploy
Mohammed, Shawn
Fernandez, Eliana Mailen
Bainbridge, Chance
Brocco, Marcela Adriana
Stein, Wolfgang
Vidal Gadea, Andrés G.
author Hughes, Kiley
author_facet Hughes, Kiley
Shah, Ashka
Bai, Xiaofei
Adams, Jessica
Bauer, Rosemary
Jackson, Janelle
Harris, Emily
Ficca, Alyson
Freebairn, Ploy
Mohammed, Shawn
Fernandez, Eliana Mailen
Bainbridge, Chance
Brocco, Marcela Adriana
Stein, Wolfgang
Vidal Gadea, Andrés G.
author_role author
author2 Shah, Ashka
Bai, Xiaofei
Adams, Jessica
Bauer, Rosemary
Jackson, Janelle
Harris, Emily
Ficca, Alyson
Freebairn, Ploy
Mohammed, Shawn
Fernandez, Eliana Mailen
Bainbridge, Chance
Brocco, Marcela Adriana
Stein, Wolfgang
Vidal Gadea, Andrés G.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv BEHAVIOR
MECHANOSENSATION
PEZO-1
PHARYNGEAL GLANDS
PHARYNGEAL PUMPING
PIEZO
topic BEHAVIOR
MECHANOSENSATION
PEZO-1
PHARYNGEAL GLANDS
PHARYNGEAL PUMPING
PIEZO
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the tissues they are expressed in remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have 12 isoforms. These isoforms share many transmembrane domains but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. We used transcriptional and translational reporters to show that putative promoter sequences immediately upstream of the start codon of long pezo-1 isoforms predominantly drive green fluorescent protein (GFP) expression in mesodermally derived tissues (such as muscle and glands). In contrast, sequences upstream of shorter pezo-1 isoforms resulted in GFP expression primarily in neurons. Putative promoters upstream of different isoforms drove GFP expression in different cells of the same organs of the digestive system. The observed unique pattern of complementary expression suggests that different isoforms could possess distinct functions within these organs. We used mutant analysis to show that pharyngeal muscles and glands require long pezo-1 isoforms to respond appropriately to the presence of food. The number of pezo-1 isoforms in C. elegans, their putative differential pattern of expression, and roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors.
Fil: Hughes, Kiley. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Shah, Ashka. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Bai, Xiaofei. National Institutes of Health; Estados Unidos
Fil: Adams, Jessica. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Bauer, Rosemary. University of Chicago; Estados Unidos
Fil: Jackson, Janelle. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Harris, Emily. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Ficca, Alyson. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Freebairn, Ploy. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Mohammed, Shawn. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Fernandez, Eliana Mailen. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Bainbridge, Chance. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Brocco, Marcela Adriana. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Stein, Wolfgang. University Of Illinois. Deparment Of Biological Science; Estados Unidos
Fil: Vidal Gadea, Andrés G.. University Of Illinois. Deparment Of Biological Science; Estados Unidos
description Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the tissues they are expressed in remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have 12 isoforms. These isoforms share many transmembrane domains but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. We used transcriptional and translational reporters to show that putative promoter sequences immediately upstream of the start codon of long pezo-1 isoforms predominantly drive green fluorescent protein (GFP) expression in mesodermally derived tissues (such as muscle and glands). In contrast, sequences upstream of shorter pezo-1 isoforms resulted in GFP expression primarily in neurons. Putative promoters upstream of different isoforms drove GFP expression in different cells of the same organs of the digestive system. The observed unique pattern of complementary expression suggests that different isoforms could possess distinct functions within these organs. We used mutant analysis to show that pharyngeal muscles and glands require long pezo-1 isoforms to respond appropriately to the presence of food. The number of pezo-1 isoforms in C. elegans, their putative differential pattern of expression, and roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors.
publishDate 2021
dc.date.none.fl_str_mv 2021-12
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/11336/182475
Hughes, Kiley; Shah, Ashka; Bai, Xiaofei; Adams, Jessica; Bauer, Rosemary; et al.; Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans; Genetics Society of America; G3: Genes, Genomes, Genetics; 12; 3; 12-2021; 1-13
2160-1836
CONICET Digital
CONICET
url http://hdl.handle.net/11336/182475
identifier_str_mv Hughes, Kiley; Shah, Ashka; Bai, Xiaofei; Adams, Jessica; Bauer, Rosemary; et al.; Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans; Genetics Society of America; G3: Genes, Genomes, Genetics; 12; 3; 12-2021; 1-13
2160-1836
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://academic.oup.com/g3journal/advance-article/doi/10.1093/g3journal/jkab429/6462202
info:eu-repo/semantics/altIdentifier/doi/10.1093/g3journal/jkab429
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Genetics Society of America
publisher.none.fl_str_mv Genetics Society of America
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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