Retinoic Acid from the Meninges Regulates Cortical Neuron Generation

Julie A. Siegenthaler; Amir M. Ashique; Konstantinos Zarbalis; Katelin P. Patterson; Jonathan H. Hecht; Maureen A. Kane; Alexandra E. Folias; Youngshik Choe; Scott R. May; Tsutomu Kume; Joseph L. Napoli; Andrew S. Peterson; Samuel J. Pleasure

doi:10.1016/j.cell.2009.10.004

Retinoic Acid from the Meninges Regulates Cortical Neuron Generation

Julie A. Siegenthaler, Amir M. Ashique, Konstantinos Zarbalis, Katelin P. Patterson, Jonathan H. Hecht, Maureen A. Kane, Alexandra E. Folias, Youngshik Choe, Scott R. May, Tsutomu Kume, Joseph L. Napoli, Andrew S. Peterson, Samuel J. Pleasure^*

^*Corresponding author for this work

Medicine, Cardiology Division

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

336 Scopus citations

Abstract

Extrinsic signals controlling generation of neocortical neurons during embryonic life have been difficult to identify. In this study we demonstrate that the dorsal forebrain meninges communicate with the adjacent radial glial endfeet and influence cortical development. We took advantage of Foxc1 mutant mice with defects in forebrain meningeal formation. Foxc1 dosage and loss of meninges correlated with a dramatic reduction in both neuron and intermediate progenitor production and elongation of the neuroepithelium. Several types of experiments demonstrate that retinoic acid (RA) is the key component of this secreted activity. In addition, Rdh10- and Raldh2-expressing cells in the dorsal meninges were either reduced or absent in the Foxc1 mutants, and Rdh10 mutants had a cortical phenotype similar to the Foxc1 null mutants. Lastly, in utero RA treatment rescued the cortical phenotype in Foxc1 mutants. These results establish RA as a potent, meningeal-derived cue required for successful corticogenesis.

Original language	English (US)
Pages (from-to)	597-609
Number of pages	13
Journal	Cell
Volume	139
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2009.10.004
State	Published - Oct 30 2009

Funding

We thank Dr. Grant Li for technical assistance and helpful discussions, Dr. Brad Pawlikowski for critical review of the manuscript, and Drs. John Rubenstein and Arturo Alvarez-Buylla for helpful discussion. This work was supported by grants from the NIH (R01DA017627), Autism Speaks, and the AHA/AAN.

Keywords

MOLNEURO

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2009.10.004

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title = "Retinoic Acid from the Meninges Regulates Cortical Neuron Generation",

abstract = "Extrinsic signals controlling generation of neocortical neurons during embryonic life have been difficult to identify. In this study we demonstrate that the dorsal forebrain meninges communicate with the adjacent radial glial endfeet and influence cortical development. We took advantage of Foxc1 mutant mice with defects in forebrain meningeal formation. Foxc1 dosage and loss of meninges correlated with a dramatic reduction in both neuron and intermediate progenitor production and elongation of the neuroepithelium. Several types of experiments demonstrate that retinoic acid (RA) is the key component of this secreted activity. In addition, Rdh10- and Raldh2-expressing cells in the dorsal meninges were either reduced or absent in the Foxc1 mutants, and Rdh10 mutants had a cortical phenotype similar to the Foxc1 null mutants. Lastly, in utero RA treatment rescued the cortical phenotype in Foxc1 mutants. These results establish RA as a potent, meningeal-derived cue required for successful corticogenesis.",

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author = "Siegenthaler, {Julie A.} and Ashique, {Amir M.} and Konstantinos Zarbalis and Patterson, {Katelin P.} and Hecht, {Jonathan H.} and Kane, {Maureen A.} and Folias, {Alexandra E.} and Youngshik Choe and May, {Scott R.} and Tsutomu Kume and Napoli, {Joseph L.} and Peterson, {Andrew S.} and Pleasure, {Samuel J.}",

note = "Funding Information: We thank Dr. Grant Li for technical assistance and helpful discussions, Dr. Brad Pawlikowski for critical review of the manuscript, and Drs. John Rubenstein and Arturo Alvarez-Buylla for helpful discussion. This work was supported by grants from the NIH (R01DA017627), Autism Speaks, and the AHA/AAN. ",

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AU - Siegenthaler, Julie A.

AU - Ashique, Amir M.

AU - Zarbalis, Konstantinos

AU - Patterson, Katelin P.

AU - Hecht, Jonathan H.

AU - Kane, Maureen A.

AU - Folias, Alexandra E.

AU - Choe, Youngshik

AU - May, Scott R.

AU - Kume, Tsutomu

AU - Napoli, Joseph L.

AU - Peterson, Andrew S.

AU - Pleasure, Samuel J.

N1 - Funding Information: We thank Dr. Grant Li for technical assistance and helpful discussions, Dr. Brad Pawlikowski for critical review of the manuscript, and Drs. John Rubenstein and Arturo Alvarez-Buylla for helpful discussion. This work was supported by grants from the NIH (R01DA017627), Autism Speaks, and the AHA/AAN.

PY - 2009/10/30

Y1 - 2009/10/30

N2 - Extrinsic signals controlling generation of neocortical neurons during embryonic life have been difficult to identify. In this study we demonstrate that the dorsal forebrain meninges communicate with the adjacent radial glial endfeet and influence cortical development. We took advantage of Foxc1 mutant mice with defects in forebrain meningeal formation. Foxc1 dosage and loss of meninges correlated with a dramatic reduction in both neuron and intermediate progenitor production and elongation of the neuroepithelium. Several types of experiments demonstrate that retinoic acid (RA) is the key component of this secreted activity. In addition, Rdh10- and Raldh2-expressing cells in the dorsal meninges were either reduced or absent in the Foxc1 mutants, and Rdh10 mutants had a cortical phenotype similar to the Foxc1 null mutants. Lastly, in utero RA treatment rescued the cortical phenotype in Foxc1 mutants. These results establish RA as a potent, meningeal-derived cue required for successful corticogenesis.

AB - Extrinsic signals controlling generation of neocortical neurons during embryonic life have been difficult to identify. In this study we demonstrate that the dorsal forebrain meninges communicate with the adjacent radial glial endfeet and influence cortical development. We took advantage of Foxc1 mutant mice with defects in forebrain meningeal formation. Foxc1 dosage and loss of meninges correlated with a dramatic reduction in both neuron and intermediate progenitor production and elongation of the neuroepithelium. Several types of experiments demonstrate that retinoic acid (RA) is the key component of this secreted activity. In addition, Rdh10- and Raldh2-expressing cells in the dorsal meninges were either reduced or absent in the Foxc1 mutants, and Rdh10 mutants had a cortical phenotype similar to the Foxc1 null mutants. Lastly, in utero RA treatment rescued the cortical phenotype in Foxc1 mutants. These results establish RA as a potent, meningeal-derived cue required for successful corticogenesis.

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Retinoic Acid from the Meninges Regulates Cortical Neuron Generation

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