A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition

Autores
Ohazama, Atsushi; Blackburn, James; Porntaveetus, Thantrira; Ota, Masato S.; Choi, Hong Y.; Johnson, Eric B.; Myers, Philip; Oommen, Shelly; Eto, Kazuhiro; Kessler, John A; Kondo, Takashi; Fraser, Gareth J.; Streelman, J. Todd; Pardiñas, Ulises Francisco J.; Tucker, A. S.; Ortiz, Pablo Edmundo; Charles, C.; Viriot, L.; Herz, J.; Sharpe, P. T.
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface receptor, Lrp4, which modulates multiple signaling pathways, produces incisors with grooved enamel surfaces that exhibit the same molecular characteristics as the tips of molar cusps. Mice with a null mutation of Lrp4 develop extra cusps on molars and have incisors that exhibit clear molar-like cusp and root morphologies. Molecular analysis identifies misregulation of Shh and Bmp signaling in the mutant incisors and suggests an uncoupling of the processes of tooth shape determination and morphogenesis. Incisors thus possess a developmentally suppressed, cuspid crown-like morphogenesis program similar to that in molars that is revealed by loss of Lrp4 activity. Several mammalian species naturally possess multicuspid incisors, suggesting that mammals have the capacity to form multicuspid teeth regardless of location in the oral jaw. Localized loss of enamel may thus have been an intermediary step in the evolution of cusps, both of which use Lrp4-mediated signaling.
Fil: Ohazama, Atsushi. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Blackburn, James. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Porntaveetus, Thantrira. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Ota, Masato S.. Tokyo Medical and Dental University; Japón
Fil: Choi, Hong Y.. University of Texas Southwestern Medical Center; Estados Unidos
Fil: Johnson, Eric B.. University of Texas Southwestern Medical Center; Estados Unidos
Fil: Myers, Philip. University of Michigan; Estados Unidos
Fil: Oommen, Shelly. Guy’s Hospital; Reino Unido
Fil: Eto, Kazuhiro. Tokyo Medical and Dental University; Japón
Fil: Kessler, John A. Northwestern University; Estados Unidos
Fil: Kondo, Takashi. Institute of Physical and Chemical Research; Japón
Fil: Fraser, Gareth J.. Georgia Institute of Technology; Estados Unidos
Fil: Streelman, J. Todd. Georgia Institute of Technology; Estados Unidos
Fil: Pardiñas, Ulises Francisco J.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo. Laboratorio de Geoarqueología; Argentina
Fil: Tucker, A. S.. King’s College London; Reino Unido. Guy’s Hospital; Reino Unido
Fil: Ortiz, Pablo Edmundo. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán; Argentina
Fil: Charles, C.. University of California; Estados Unidos
Fil: Viriot, L.. Université de Lyon; Francia
Fil: Herz, J.. University of Texas; Estados Unidos
Fil: Sharpe, P. T.. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Materia
Cusp
Lrp4
Tooth Development
Evo/Devo
Multicuspid Crown
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:11336/236631
Acceder
id CONICETDig_c22b66db0e066b9fd440dbd16dc3ef76
oai_identifier_str oai:ri.conicet.gov.ar:11336/236631
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentitionOhazama, AtsushiBlackburn, JamesPorntaveetus, ThantriraOta, Masato S.Choi, Hong Y.Johnson, Eric B.Myers, PhilipOommen, ShellyEto, KazuhiroKessler, John AKondo, TakashiFraser, Gareth J.Streelman, J. ToddPardiñas, Ulises Francisco J.Tucker, A. S.Ortiz, Pablo EdmundoCharles, C.Viriot, L.Herz, J.Sharpe, P. T.CuspLrp4Tooth DevelopmentEvo/DevoMulticuspid Crownhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface receptor, Lrp4, which modulates multiple signaling pathways, produces incisors with grooved enamel surfaces that exhibit the same molecular characteristics as the tips of molar cusps. Mice with a null mutation of Lrp4 develop extra cusps on molars and have incisors that exhibit clear molar-like cusp and root morphologies. Molecular analysis identifies misregulation of Shh and Bmp signaling in the mutant incisors and suggests an uncoupling of the processes of tooth shape determination and morphogenesis. Incisors thus possess a developmentally suppressed, cuspid crown-like morphogenesis program similar to that in molars that is revealed by loss of Lrp4 activity. Several mammalian species naturally possess multicuspid incisors, suggesting that mammals have the capacity to form multicuspid teeth regardless of location in the oral jaw. Localized loss of enamel may thus have been an intermediary step in the evolution of cusps, both of which use Lrp4-mediated signaling.Fil: Ohazama, Atsushi. Guy’s Hospital; Reino Unido. King’s College London; Reino UnidoFil: Blackburn, James. Guy’s Hospital; Reino Unido. King’s College London; Reino UnidoFil: Porntaveetus, Thantrira. Guy’s Hospital; Reino Unido. King’s College London; Reino UnidoFil: Ota, Masato S.. Tokyo Medical and Dental University; JapónFil: Choi, Hong Y.. University of Texas Southwestern Medical Center; Estados UnidosFil: Johnson, Eric B.. University of Texas Southwestern Medical Center; Estados UnidosFil: Myers, Philip. University of Michigan; Estados UnidosFil: Oommen, Shelly. Guy’s Hospital; Reino UnidoFil: Eto, Kazuhiro. Tokyo Medical and Dental University; JapónFil: Kessler, John A. Northwestern University; Estados UnidosFil: Kondo, Takashi. Institute of Physical and Chemical Research; JapónFil: Fraser, Gareth J.. Georgia Institute of Technology; Estados UnidosFil: Streelman, J. Todd. Georgia Institute of Technology; Estados UnidosFil: Pardiñas, Ulises Francisco J.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo. Laboratorio de Geoarqueología; ArgentinaFil: Tucker, A. S.. King’s College London; Reino Unido. Guy’s Hospital; Reino UnidoFil: Ortiz, Pablo Edmundo. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán; ArgentinaFil: Charles, C.. University of California; Estados UnidosFil: Viriot, L.. Université de Lyon; FranciaFil: Herz, J.. University of Texas; Estados UnidosFil: Sharpe, P. T.. Guy’s Hospital; Reino Unido. King’s College London; Reino UnidoNational Academy of Sciences2010-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/236631Ohazama, Atsushi; Blackburn, James; Porntaveetus, Thantrira; Ota, Masato S.; Choi, Hong Y.; et al.; A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 107; 1; 1-2010; 92-970027-8424CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.0907236107info:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/full/10.1073/pnas.0907236107info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:22:10Zoai:ri.conicet.gov.ar:11336/236631instacron: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:34982025-10-15 14:22:10.549CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
title A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
spellingShingle A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
Ohazama, Atsushi
Cusp
Lrp4
Tooth Development
Evo/Devo
Multicuspid Crown
title_short A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
title_full A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
title_fullStr A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
title_full_unstemmed A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
title_sort A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition
dc.creator.none.fl_str_mv Ohazama, Atsushi
Blackburn, James
Porntaveetus, Thantrira
Ota, Masato S.
Choi, Hong Y.
Johnson, Eric B.
Myers, Philip
Oommen, Shelly
Eto, Kazuhiro
Kessler, John A
Kondo, Takashi
Fraser, Gareth J.
Streelman, J. Todd
Pardiñas, Ulises Francisco J.
Tucker, A. S.
Ortiz, Pablo Edmundo
Charles, C.
Viriot, L.
Herz, J.
Sharpe, P. T.
author Ohazama, Atsushi
author_facet Ohazama, Atsushi
Blackburn, James
Porntaveetus, Thantrira
Ota, Masato S.
Choi, Hong Y.
Johnson, Eric B.
Myers, Philip
Oommen, Shelly
Eto, Kazuhiro
Kessler, John A
Kondo, Takashi
Fraser, Gareth J.
Streelman, J. Todd
Pardiñas, Ulises Francisco J.
Tucker, A. S.
Ortiz, Pablo Edmundo
Charles, C.
Viriot, L.
Herz, J.
Sharpe, P. T.
author_role author
author2 Blackburn, James
Porntaveetus, Thantrira
Ota, Masato S.
Choi, Hong Y.
Johnson, Eric B.
Myers, Philip
Oommen, Shelly
Eto, Kazuhiro
Kessler, John A
Kondo, Takashi
Fraser, Gareth J.
Streelman, J. Todd
Pardiñas, Ulises Francisco J.
Tucker, A. S.
Ortiz, Pablo Edmundo
Charles, C.
Viriot, L.
Herz, J.
Sharpe, P. T.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cusp
Lrp4
Tooth Development
Evo/Devo
Multicuspid Crown
topic Cusp
Lrp4
Tooth Development
Evo/Devo
Multicuspid Crown
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface receptor, Lrp4, which modulates multiple signaling pathways, produces incisors with grooved enamel surfaces that exhibit the same molecular characteristics as the tips of molar cusps. Mice with a null mutation of Lrp4 develop extra cusps on molars and have incisors that exhibit clear molar-like cusp and root morphologies. Molecular analysis identifies misregulation of Shh and Bmp signaling in the mutant incisors and suggests an uncoupling of the processes of tooth shape determination and morphogenesis. Incisors thus possess a developmentally suppressed, cuspid crown-like morphogenesis program similar to that in molars that is revealed by loss of Lrp4 activity. Several mammalian species naturally possess multicuspid incisors, suggesting that mammals have the capacity to form multicuspid teeth regardless of location in the oral jaw. Localized loss of enamel may thus have been an intermediary step in the evolution of cusps, both of which use Lrp4-mediated signaling.
Fil: Ohazama, Atsushi. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Blackburn, James. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Porntaveetus, Thantrira. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
Fil: Ota, Masato S.. Tokyo Medical and Dental University; Japón
Fil: Choi, Hong Y.. University of Texas Southwestern Medical Center; Estados Unidos
Fil: Johnson, Eric B.. University of Texas Southwestern Medical Center; Estados Unidos
Fil: Myers, Philip. University of Michigan; Estados Unidos
Fil: Oommen, Shelly. Guy’s Hospital; Reino Unido
Fil: Eto, Kazuhiro. Tokyo Medical and Dental University; Japón
Fil: Kessler, John A. Northwestern University; Estados Unidos
Fil: Kondo, Takashi. Institute of Physical and Chemical Research; Japón
Fil: Fraser, Gareth J.. Georgia Institute of Technology; Estados Unidos
Fil: Streelman, J. Todd. Georgia Institute of Technology; Estados Unidos
Fil: Pardiñas, Ulises Francisco J.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo. Laboratorio de Geoarqueología; Argentina
Fil: Tucker, A. S.. King’s College London; Reino Unido. Guy’s Hospital; Reino Unido
Fil: Ortiz, Pablo Edmundo. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán; Argentina
Fil: Charles, C.. University of California; Estados Unidos
Fil: Viriot, L.. Université de Lyon; Francia
Fil: Herz, J.. University of Texas; Estados Unidos
Fil: Sharpe, P. T.. Guy’s Hospital; Reino Unido. King’s College London; Reino Unido
description Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface receptor, Lrp4, which modulates multiple signaling pathways, produces incisors with grooved enamel surfaces that exhibit the same molecular characteristics as the tips of molar cusps. Mice with a null mutation of Lrp4 develop extra cusps on molars and have incisors that exhibit clear molar-like cusp and root morphologies. Molecular analysis identifies misregulation of Shh and Bmp signaling in the mutant incisors and suggests an uncoupling of the processes of tooth shape determination and morphogenesis. Incisors thus possess a developmentally suppressed, cuspid crown-like morphogenesis program similar to that in molars that is revealed by loss of Lrp4 activity. Several mammalian species naturally possess multicuspid incisors, suggesting that mammals have the capacity to form multicuspid teeth regardless of location in the oral jaw. Localized loss of enamel may thus have been an intermediary step in the evolution of cusps, both of which use Lrp4-mediated signaling.
publishDate 2010
dc.date.none.fl_str_mv 2010-01
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/11336/236631
Ohazama, Atsushi; Blackburn, James; Porntaveetus, Thantrira; Ota, Masato S.; Choi, Hong Y.; et al.; A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 107; 1; 1-2010; 92-97
0027-8424
CONICET Digital
CONICET
url http://hdl.handle.net/11336/236631
identifier_str_mv Ohazama, Atsushi; Blackburn, James; Porntaveetus, Thantrira; Ota, Masato S.; Choi, Hong Y.; et al.; A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 107; 1; 1-2010; 92-97
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/doi/10.1073/pnas.0907236107
info:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/full/10.1073/pnas.0907236107
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
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 13.22299

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