Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells

Autores
Scarinci, María Noelia; Gutierrez, Brenda Celeste; Albarracín, Virginia Helena; Cantero, Maria del Rocio; Cantiello, Horacio Fabio
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The primary cilium is a non-motile sensory organelle that transduces environmental cues into cellular responses. It comprises an axoneme, a core of nine doublet microtubules (MTs) coated by a specialized membrane populated by receptors, and a high density of ion channels. Dysfunctional primary cilia generate the pathogenesis of several diseases known as ciliopathies. However, the electrical role of MTs in ciliary signaling remains largely unknown. Herein, we determined by the patch clamp technique the electrical activity of cytoplasmic and axonemal MTs from wild-type LLC-PK1 renal epithelial cells. We observed electrical oscillations with fundamental frequencies at ∼39 Hz and ∼93 Hz in sheets of cytoplasmic MTs. We also studied in situ and isolated, intact and Triton X-permeabilized primary cilia, observing electrical oscillations with peak frequencies at either 29–49 Hz (non-permeabilized) or ∼40–49 Hz (permeabilized) and ∼93 Hz (both). We applied Empirical Mode Decomposition (EMD), Continuous Wavelet Transform (CWT), and Cross-Correlation Analysis (CCA) to assess the differences and the coherence in the Time-Frequency domains of electrical oscillations between cytoplasmic and axonemal MTs. The data indicate that axonemal and cytoplasmic MTs show different patterns of electrical oscillations preserving coherence at specific frequency peaks that may serve as electromagnetic communication between compartments. Further, the electrical behavior of axonemal MTs was modified by siRNA deletion of polycystin-2 (PC2), which lengthens primary cilia, thus linking ciliary channels to the morphological and electrical behavior of cilia in ciliopathies. The encompassed evidence indicates that the primary cilium behaves as an electrical antenna, with an excitable MT structure that produces electrical oscillations whose synchronization and propagation constitute a novel cell signaling mechanism.
Fil: Scarinci, María Noelia. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Gutierrez, Brenda Celeste. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Albarracín, Virginia Helena. Universidad Nacional de Tucumán; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cantero, Maria del Rocio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Cantiello, Horacio Fabio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Materia
ELECTRICAL OSCILLATIONS
PRIMARY CILIUM
MICROTUBULES
CYTOSKELETON
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:11336/232994
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/232994
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cellsScarinci, María NoeliaGutierrez, Brenda CelesteAlbarracín, Virginia HelenaCantero, Maria del RocioCantiello, Horacio FabioELECTRICAL OSCILLATIONSPRIMARY CILIUMMICROTUBULESCYTOSKELETONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The primary cilium is a non-motile sensory organelle that transduces environmental cues into cellular responses. It comprises an axoneme, a core of nine doublet microtubules (MTs) coated by a specialized membrane populated by receptors, and a high density of ion channels. Dysfunctional primary cilia generate the pathogenesis of several diseases known as ciliopathies. However, the electrical role of MTs in ciliary signaling remains largely unknown. Herein, we determined by the patch clamp technique the electrical activity of cytoplasmic and axonemal MTs from wild-type LLC-PK1 renal epithelial cells. We observed electrical oscillations with fundamental frequencies at ∼39 Hz and ∼93 Hz in sheets of cytoplasmic MTs. We also studied in situ and isolated, intact and Triton X-permeabilized primary cilia, observing electrical oscillations with peak frequencies at either 29–49 Hz (non-permeabilized) or ∼40–49 Hz (permeabilized) and ∼93 Hz (both). We applied Empirical Mode Decomposition (EMD), Continuous Wavelet Transform (CWT), and Cross-Correlation Analysis (CCA) to assess the differences and the coherence in the Time-Frequency domains of electrical oscillations between cytoplasmic and axonemal MTs. The data indicate that axonemal and cytoplasmic MTs show different patterns of electrical oscillations preserving coherence at specific frequency peaks that may serve as electromagnetic communication between compartments. Further, the electrical behavior of axonemal MTs was modified by siRNA deletion of polycystin-2 (PC2), which lengthens primary cilia, thus linking ciliary channels to the morphological and electrical behavior of cilia in ciliopathies. The encompassed evidence indicates that the primary cilium behaves as an electrical antenna, with an excitable MT structure that produces electrical oscillations whose synchronization and propagation constitute a novel cell signaling mechanism.Fil: Scarinci, María Noelia. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; ArgentinaFil: Gutierrez, Brenda Celeste. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; ArgentinaFil: Albarracín, Virginia Helena. Universidad Nacional de Tucumán; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Cantero, Maria del Rocio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; ArgentinaFil: Cantiello, Horacio Fabio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; ArgentinaFrontiers Media2023-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/232994Scarinci, María Noelia; Gutierrez, Brenda Celeste; Albarracín, Virginia Helena; Cantero, Maria del Rocio; Cantiello, Horacio Fabio; Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells; Frontiers Media; Frontiers in Molecular Biosciences; 10; 11-2023; 1-162296-889XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fmolb.2023.1214532/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fmolb.2023.1214532info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:11:41Zoai:ri.conicet.gov.ar:11336/232994instacron: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 10:11:41.551CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
title Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
spellingShingle Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
Scarinci, María Noelia
ELECTRICAL OSCILLATIONS
PRIMARY CILIUM
MICROTUBULES
CYTOSKELETON
title_short Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
title_full Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
title_fullStr Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
title_full_unstemmed Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
title_sort Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells
dc.creator.none.fl_str_mv Scarinci, María Noelia
Gutierrez, Brenda Celeste
Albarracín, Virginia Helena
Cantero, Maria del Rocio
Cantiello, Horacio Fabio
author Scarinci, María Noelia
author_facet Scarinci, María Noelia
Gutierrez, Brenda Celeste
Albarracín, Virginia Helena
Cantero, Maria del Rocio
Cantiello, Horacio Fabio
author_role author
author2 Gutierrez, Brenda Celeste
Albarracín, Virginia Helena
Cantero, Maria del Rocio
Cantiello, Horacio Fabio
author2_role author
author
author
author
dc.subject.none.fl_str_mv ELECTRICAL OSCILLATIONS
PRIMARY CILIUM
MICROTUBULES
CYTOSKELETON
topic ELECTRICAL OSCILLATIONS
PRIMARY CILIUM
MICROTUBULES
CYTOSKELETON
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The primary cilium is a non-motile sensory organelle that transduces environmental cues into cellular responses. It comprises an axoneme, a core of nine doublet microtubules (MTs) coated by a specialized membrane populated by receptors, and a high density of ion channels. Dysfunctional primary cilia generate the pathogenesis of several diseases known as ciliopathies. However, the electrical role of MTs in ciliary signaling remains largely unknown. Herein, we determined by the patch clamp technique the electrical activity of cytoplasmic and axonemal MTs from wild-type LLC-PK1 renal epithelial cells. We observed electrical oscillations with fundamental frequencies at ∼39 Hz and ∼93 Hz in sheets of cytoplasmic MTs. We also studied in situ and isolated, intact and Triton X-permeabilized primary cilia, observing electrical oscillations with peak frequencies at either 29–49 Hz (non-permeabilized) or ∼40–49 Hz (permeabilized) and ∼93 Hz (both). We applied Empirical Mode Decomposition (EMD), Continuous Wavelet Transform (CWT), and Cross-Correlation Analysis (CCA) to assess the differences and the coherence in the Time-Frequency domains of electrical oscillations between cytoplasmic and axonemal MTs. The data indicate that axonemal and cytoplasmic MTs show different patterns of electrical oscillations preserving coherence at specific frequency peaks that may serve as electromagnetic communication between compartments. Further, the electrical behavior of axonemal MTs was modified by siRNA deletion of polycystin-2 (PC2), which lengthens primary cilia, thus linking ciliary channels to the morphological and electrical behavior of cilia in ciliopathies. The encompassed evidence indicates that the primary cilium behaves as an electrical antenna, with an excitable MT structure that produces electrical oscillations whose synchronization and propagation constitute a novel cell signaling mechanism.
Fil: Scarinci, María Noelia. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Gutierrez, Brenda Celeste. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Albarracín, Virginia Helena. Universidad Nacional de Tucumán; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cantero, Maria del Rocio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
Fil: Cantiello, Horacio Fabio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet Noa Sur. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo. - Universidad Nacional de Santiago del Estero. Instituto Multidisciplinario de Salud, Tecnologia y Desarrollo.; Argentina
description The primary cilium is a non-motile sensory organelle that transduces environmental cues into cellular responses. It comprises an axoneme, a core of nine doublet microtubules (MTs) coated by a specialized membrane populated by receptors, and a high density of ion channels. Dysfunctional primary cilia generate the pathogenesis of several diseases known as ciliopathies. However, the electrical role of MTs in ciliary signaling remains largely unknown. Herein, we determined by the patch clamp technique the electrical activity of cytoplasmic and axonemal MTs from wild-type LLC-PK1 renal epithelial cells. We observed electrical oscillations with fundamental frequencies at ∼39 Hz and ∼93 Hz in sheets of cytoplasmic MTs. We also studied in situ and isolated, intact and Triton X-permeabilized primary cilia, observing electrical oscillations with peak frequencies at either 29–49 Hz (non-permeabilized) or ∼40–49 Hz (permeabilized) and ∼93 Hz (both). We applied Empirical Mode Decomposition (EMD), Continuous Wavelet Transform (CWT), and Cross-Correlation Analysis (CCA) to assess the differences and the coherence in the Time-Frequency domains of electrical oscillations between cytoplasmic and axonemal MTs. The data indicate that axonemal and cytoplasmic MTs show different patterns of electrical oscillations preserving coherence at specific frequency peaks that may serve as electromagnetic communication between compartments. Further, the electrical behavior of axonemal MTs was modified by siRNA deletion of polycystin-2 (PC2), which lengthens primary cilia, thus linking ciliary channels to the morphological and electrical behavior of cilia in ciliopathies. The encompassed evidence indicates that the primary cilium behaves as an electrical antenna, with an excitable MT structure that produces electrical oscillations whose synchronization and propagation constitute a novel cell signaling mechanism.
publishDate 2023
dc.date.none.fl_str_mv 2023-11
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/11336/232994
Scarinci, María Noelia; Gutierrez, Brenda Celeste; Albarracín, Virginia Helena; Cantero, Maria del Rocio; Cantiello, Horacio Fabio; Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells; Frontiers Media; Frontiers in Molecular Biosciences; 10; 11-2023; 1-16
2296-889X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/232994
identifier_str_mv Scarinci, María Noelia; Gutierrez, Brenda Celeste; Albarracín, Virginia Helena; Cantero, Maria del Rocio; Cantiello, Horacio Fabio; Role of the microtubules in the electrical activity of the primary cilium of renal epithelial cells; Frontiers Media; Frontiers in Molecular Biosciences; 10; 11-2023; 1-16
2296-889X
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.frontiersin.org/articles/10.3389/fmolb.2023.1214532/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fmolb.2023.1214532
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 Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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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