Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor

Autores
Lipovsek, Maria Marcela; Im, Gi Jung; Franchini, Lucia Florencia; Pisciottano, Francisco; Katz, Eleonora; Fuchs, Paul Albert; Elgoyhen, Ana Belen
Año de publicación
2012
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The a9 and a10 cholinergic nicotinic receptor subunits assemble to form the receptor that mediates efferent inhibition of hair cell function within the auditory sensory organ, a mechanism thought to modulate the dynamic range of hearing. In contrast to all nicotinic receptors, which serve excitatory neurotransmission, the activation of a9a10 produces hyperpolarization of hair cells. An evolutionary analysis has shown that the a10 subunit exhibits signatures of positive selection only along the mammalian lineage, strongly suggesting the acquisition of a unique function. To establish whether mammalian a9a10 receptors have acquired distinct functional properties as a consequence of this evolutionary pressure, we compared the properties of rat and chicken recombinant and native a9a10 receptors. Our main finding in the present work is that, in contrast to the high (pCa(2+)/pMonovalents ­10) Ca(2+) permeability reported for rat a9a10 receptors, recombinant and native chicken a9a10 receptors have a much lower permeability (­2) to this cation, comparable to that of neuronal ¥á4¥â2 receptors. Moreover, we show that, in contrast to a10, a7 as well as a4 and a2 nicotinic subunits are under purifying selection in vertebrates, consistent with the conserved Ca(2+) permeability reported across species. These results have important consequences for the activation of signaling cascades that lead to hyperpolarization of hair cells after a9a10 gating at the cholinergic-hair cell synapse. In addition, they suggest that high Ca(2+) permeability of the a9a10 cholinergic nicotinic receptor might have evolved together with other features that have given the mammalian ear an expanded high-frequency sensitivity.
Fil: Lipovsek, Maria Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Im, Gi Jung. University Johns Hopkins; Estados Unidos
Fil: Franchini, Lucia Florencia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Pisciottano, Francisco. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Katz, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Fuchs, Paul Albert. University Johns Hopkins; Estados Unidos
Fil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Materia
evolución
cóclea
canales iónicos
receptores nicotínicos
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
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oai:ri.conicet.gov.ar:11336/273055
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/273055
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptorLipovsek, Maria MarcelaIm, Gi JungFranchini, Lucia FlorenciaPisciottano, FranciscoKatz, EleonoraFuchs, Paul AlbertElgoyhen, Ana Belenevolucióncócleacanales iónicosreceptores nicotínicoshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The a9 and a10 cholinergic nicotinic receptor subunits assemble to form the receptor that mediates efferent inhibition of hair cell function within the auditory sensory organ, a mechanism thought to modulate the dynamic range of hearing. In contrast to all nicotinic receptors, which serve excitatory neurotransmission, the activation of a9a10 produces hyperpolarization of hair cells. An evolutionary analysis has shown that the a10 subunit exhibits signatures of positive selection only along the mammalian lineage, strongly suggesting the acquisition of a unique function. To establish whether mammalian a9a10 receptors have acquired distinct functional properties as a consequence of this evolutionary pressure, we compared the properties of rat and chicken recombinant and native a9a10 receptors. Our main finding in the present work is that, in contrast to the high (pCa(2+)/pMonovalents ­10) Ca(2+) permeability reported for rat a9a10 receptors, recombinant and native chicken a9a10 receptors have a much lower permeability (­2) to this cation, comparable to that of neuronal ¥á4¥â2 receptors. Moreover, we show that, in contrast to a10, a7 as well as a4 and a2 nicotinic subunits are under purifying selection in vertebrates, consistent with the conserved Ca(2+) permeability reported across species. These results have important consequences for the activation of signaling cascades that lead to hyperpolarization of hair cells after a9a10 gating at the cholinergic-hair cell synapse. In addition, they suggest that high Ca(2+) permeability of the a9a10 cholinergic nicotinic receptor might have evolved together with other features that have given the mammalian ear an expanded high-frequency sensitivity.Fil: Lipovsek, Maria Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Im, Gi Jung. University Johns Hopkins; Estados UnidosFil: Franchini, Lucia Florencia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Pisciottano, Francisco. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Katz, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Fuchs, Paul Albert. University Johns Hopkins; Estados UnidosFil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaNational Academy of Sciences2012-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/273055Lipovsek, Maria Marcela; Im, Gi Jung; Franchini, Lucia Florencia; Pisciottano, Francisco; Katz, Eleonora; et al.; Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 2-2012; 4308-43130027-8424CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/10.1073/pnas.1115488109info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1115488109info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:50:52Zoai:ri.conicet.gov.ar:11336/273055instacron: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:34982025-10-22 11:50:52.664CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
title Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
spellingShingle Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
Lipovsek, Maria Marcela
evolución
cóclea
canales iónicos
receptores nicotínicos
title_short Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
title_full Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
title_fullStr Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
title_full_unstemmed Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
title_sort Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor
dc.creator.none.fl_str_mv Lipovsek, Maria Marcela
Im, Gi Jung
Franchini, Lucia Florencia
Pisciottano, Francisco
Katz, Eleonora
Fuchs, Paul Albert
Elgoyhen, Ana Belen
author Lipovsek, Maria Marcela
author_facet Lipovsek, Maria Marcela
Im, Gi Jung
Franchini, Lucia Florencia
Pisciottano, Francisco
Katz, Eleonora
Fuchs, Paul Albert
Elgoyhen, Ana Belen
author_role author
author2 Im, Gi Jung
Franchini, Lucia Florencia
Pisciottano, Francisco
Katz, Eleonora
Fuchs, Paul Albert
Elgoyhen, Ana Belen
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv evolución
cóclea
canales iónicos
receptores nicotínicos
topic evolución
cóclea
canales iónicos
receptores nicotínicos
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 a9 and a10 cholinergic nicotinic receptor subunits assemble to form the receptor that mediates efferent inhibition of hair cell function within the auditory sensory organ, a mechanism thought to modulate the dynamic range of hearing. In contrast to all nicotinic receptors, which serve excitatory neurotransmission, the activation of a9a10 produces hyperpolarization of hair cells. An evolutionary analysis has shown that the a10 subunit exhibits signatures of positive selection only along the mammalian lineage, strongly suggesting the acquisition of a unique function. To establish whether mammalian a9a10 receptors have acquired distinct functional properties as a consequence of this evolutionary pressure, we compared the properties of rat and chicken recombinant and native a9a10 receptors. Our main finding in the present work is that, in contrast to the high (pCa(2+)/pMonovalents ­10) Ca(2+) permeability reported for rat a9a10 receptors, recombinant and native chicken a9a10 receptors have a much lower permeability (­2) to this cation, comparable to that of neuronal ¥á4¥â2 receptors. Moreover, we show that, in contrast to a10, a7 as well as a4 and a2 nicotinic subunits are under purifying selection in vertebrates, consistent with the conserved Ca(2+) permeability reported across species. These results have important consequences for the activation of signaling cascades that lead to hyperpolarization of hair cells after a9a10 gating at the cholinergic-hair cell synapse. In addition, they suggest that high Ca(2+) permeability of the a9a10 cholinergic nicotinic receptor might have evolved together with other features that have given the mammalian ear an expanded high-frequency sensitivity.
Fil: Lipovsek, Maria Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Im, Gi Jung. University Johns Hopkins; Estados Unidos
Fil: Franchini, Lucia Florencia. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Pisciottano, Francisco. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Katz, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Fuchs, Paul Albert. University Johns Hopkins; Estados Unidos
Fil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
description The a9 and a10 cholinergic nicotinic receptor subunits assemble to form the receptor that mediates efferent inhibition of hair cell function within the auditory sensory organ, a mechanism thought to modulate the dynamic range of hearing. In contrast to all nicotinic receptors, which serve excitatory neurotransmission, the activation of a9a10 produces hyperpolarization of hair cells. An evolutionary analysis has shown that the a10 subunit exhibits signatures of positive selection only along the mammalian lineage, strongly suggesting the acquisition of a unique function. To establish whether mammalian a9a10 receptors have acquired distinct functional properties as a consequence of this evolutionary pressure, we compared the properties of rat and chicken recombinant and native a9a10 receptors. Our main finding in the present work is that, in contrast to the high (pCa(2+)/pMonovalents ­10) Ca(2+) permeability reported for rat a9a10 receptors, recombinant and native chicken a9a10 receptors have a much lower permeability (­2) to this cation, comparable to that of neuronal ¥á4¥â2 receptors. Moreover, we show that, in contrast to a10, a7 as well as a4 and a2 nicotinic subunits are under purifying selection in vertebrates, consistent with the conserved Ca(2+) permeability reported across species. These results have important consequences for the activation of signaling cascades that lead to hyperpolarization of hair cells after a9a10 gating at the cholinergic-hair cell synapse. In addition, they suggest that high Ca(2+) permeability of the a9a10 cholinergic nicotinic receptor might have evolved together with other features that have given the mammalian ear an expanded high-frequency sensitivity.
publishDate 2012
dc.date.none.fl_str_mv 2012-02
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/11336/273055
Lipovsek, Maria Marcela; Im, Gi Jung; Franchini, Lucia Florencia; Pisciottano, Francisco; Katz, Eleonora; et al.; Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 2-2012; 4308-4313
0027-8424
CONICET Digital
CONICET
url http://hdl.handle.net/11336/273055
identifier_str_mv Lipovsek, Maria Marcela; Im, Gi Jung; Franchini, Lucia Florencia; Pisciottano, Francisco; Katz, Eleonora; et al.; Phylogenetic differences in calcium permeability of the auditory hair cell cholinergic nicotinic receptor; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 2-2012; 4308-4313
0027-8424
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.pnas.org/doi/10.1073/pnas.1115488109
info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1115488109
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
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
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 12.982451

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