A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds

Eve R. Schneider; Evan O. Anderson; Viktor V. Feketa; Marco Mastrotto; Yury A. Nikolaev; Elena O. Gracheva; Sviatoslav N. Bagriantsev

doi:10.1016/j.celrep.2019.01.100

A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds

Eve R. Schneider, Evan O. Anderson, Viktor V. Feketa, Marco Mastrotto, Yury A. Nikolaev, Elena O. Gracheva, Sviatoslav N. Bagriantsev

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20 Scopus citations

Abstract

A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system.

Original language	English
Pages (from-to)	1979-1987.e3
Journal	Cell Reports
Volume	26
Issue number	8
DOIs	https://doi.org/10.1016/j.celrep.2019.01.100
State	Published - Feb 19 2019

Bibliographical note

Funding Information:
We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation . E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation . V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.).

Funding Information:
We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation. E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation. V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.).

Publisher Copyright:
© 2019 The Author(s)

Keywords

Piezo1
Piezo2
duck
mechanoreceptor
mechanosensation
mechanosensitivity
sensory adaptation
sensory physiology
somatosensitivity
touch

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology (all)

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10.1016/j.celrep.2019.01.100

Cite this

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title = "A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds",

abstract = "A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system.",

keywords = "Piezo1, Piezo2, duck, mechanoreceptor, mechanosensation, mechanosensitivity, sensory adaptation, sensory physiology, somatosensitivity, touch",

author = "Schneider, {Eve R.} and Anderson, {Evan O.} and Feketa, {Viktor V.} and Marco Mastrotto and Nikolaev, {Yury A.} and Gracheva, {Elena O.} and Bagriantsev, {Sviatoslav N.}",

note = "Funding Information: We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation . E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation . V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.). Funding Information: We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation. E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation. V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.). Publisher Copyright: {\textcopyright} 2019 The Author(s)",

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AU - Anderson, Evan O.

AU - Feketa, Viktor V.

AU - Mastrotto, Marco

AU - Nikolaev, Yury A.

AU - Gracheva, Elena O.

AU - Bagriantsev, Sviatoslav N.

N1 - Funding Information: We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation . E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation . V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.). Funding Information: We thank members of the Gracheva and Bagriantsev laboratories for their contributions throughout the project, Kate McGrew and Alicia Berlin from the USGS Patuxent Wildlife Research Center, Nick Tiberio from Livingston Ripley Waterfowl Conservancy, and the Metzer Farms staff for providing bird eggs. E.R.S. is a postdoctoral fellow of the Arnold and Mabel Beckman Foundation. E.O.A. is an Edward L. Tatum fellow and was partially supported by the Gruber Foundation. V.V.F. is a James Hudson Brown-Alexander B. Coxe fellow. This study was partly funded by NIH grant 1R01NS091300-01A1 (to E.O.G.), NSF CAREER grant 1453167 (to S.N.B.), and NIH grant 1R01NS097547-01A1 (to S.N.B.). Publisher Copyright: © 2019 The Author(s)

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N2 - A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system.

AB - A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system.

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KW - Piezo2

KW - duck

KW - mechanoreceptor

KW - mechanosensation

KW - mechanosensitivity

KW - sensory adaptation

KW - sensory physiology

KW - somatosensitivity

KW - touch

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JO - Cell Reports

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ER -

A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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