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

Atsushi Ohazama; James Blackburn; Thantrira Porntaveetus; Masato S. Ota; Hong Y. Choi; Eric B. Johnson; Philip Myers; Shelly Oommen; Kazuhiro Eto; John A. Kessler; Takashi Kondo; Gareth J. Fraser; Todd Streelman; Ulyses F. J. Pardinas; Abigail S. Tucker; Pablo E. Ortiz; Cyril Charles; Laurent Viriot; Joachim Herz; Paul T. Sharpe

doi:10.1073/pnas.0907236107

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

Atsushi Ohazama, James Blackburn, Thantrira Porntaveetus, Masato S. Ota, Hong Y. Choi, Eric B. Johnson, Philip Myers, Shelly Oommen, Kazuhiro Eto, John A. Kessler, Takashi Kondo, Gareth J. Fraser, Todd Streelman, Ulyses F. J. Pardinas, Abigail S. Tucker, Pablo E. Ortiz, Cyril Charles, Laurent Viriot, Joachim Herz, Paul T. Sharpe

Centre for Craniofacial & Regenerative Biology

Research output: Contribution to journal › Article › peer-review

36 Citations (Scopus)

Abstract

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.

Original language	English
Pages (from-to)	92 - 97
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	107
Issue number	1
DOIs	https://doi.org/10.1073/pnas.0907236107
Publication status	Published - 2010

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Ohazama, A., Blackburn, J., Porntaveetus, T., Ota, M. S., Choi, H. Y., Johnson, E. B., Myers, P., Oommen, S., Eto, K., Kessler, J. A., Kondo, T., Fraser, G. J., Streelman, T., Pardinas, U. F. J., Tucker, A. S., Ortiz, P. E., Charles, C., Viriot, L., Herz, J., & Sharpe, P. T. (2010). A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition. Proceedings of the National Academy of Sciences of the United States of America, 107(1), 92 - 97. https://doi.org/10.1073/pnas.0907236107

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title = "A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition",

abstract = "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.",

author = "Atsushi Ohazama and James Blackburn and Thantrira Porntaveetus and Ota, {Masato S.} and Choi, {Hong Y.} and Johnson, {Eric B.} and Philip Myers and Shelly Oommen and Kazuhiro Eto and Kessler, {John A.} and Takashi Kondo and Fraser, {Gareth J.} and Todd Streelman and Pardinas, {Ulyses F. J.} and Tucker, {Abigail S.} and Ortiz, {Pablo E.} and Cyril Charles and Laurent Viriot and Joachim Herz and Sharpe, {Paul T.}",

year = "2010",

doi = "10.1073/pnas.0907236107",

language = "English",

volume = "107",

pages = "92 -- 97",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "1091-6490",

publisher = "National Acad Sciences",

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Ohazama, A , Blackburn, J, Porntaveetus, T, Ota, MS, Choi, HY, Johnson, EB, Myers, P, Oommen, S, Eto, K, Kessler, JA, Kondo, T, Fraser, GJ, Streelman, T, Pardinas, UFJ, Tucker, AS, Ortiz, PE, Charles, C, Viriot, L, Herz, J & Sharpe, PT 2010, 'A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition', Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 92 - 97. https://doi.org/10.1073/pnas.0907236107

TY - JOUR

T1 - A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition

AU - Ohazama, Atsushi

AU - Blackburn, James

AU - Porntaveetus, Thantrira

AU - Ota, Masato S.

AU - Choi, Hong Y.

AU - Johnson, Eric B.

AU - Myers, Philip

AU - Oommen, Shelly

AU - Eto, Kazuhiro

AU - Kessler, John A.

AU - Kondo, Takashi

AU - Fraser, Gareth J.

AU - Streelman, Todd

AU - Pardinas, Ulyses F. J.

AU - Tucker, Abigail S.

AU - Ortiz, Pablo E.

AU - Charles, Cyril

AU - Viriot, Laurent

AU - Herz, Joachim

AU - Sharpe, Paul T.

PY - 2010

Y1 - 2010

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.0907236107

DO - 10.1073/pnas.0907236107

M3 - Article

SN - 1091-6490

VL - 107

SP - 92

EP - 97

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 1

ER -

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

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