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Articles, Development/Plasticity/Repair

The CB1 Cannabinoid Receptor Drives Corticospinal Motor Neuron Differentiation through the Ctip2/Satb2 Transcriptional Regulation Axis

Javier Díaz-Alonso, Tania Aguado, Chia-Shan Wu, Javier Palazuelos, Clementine Hofmann, Patricia Garcez, François Guillemot, Hui-Chen Lu, Beat Lutz, Manuel Guzmán and Ismael Galve-Roperh
Journal of Neuroscience 21 November 2012, 32 (47) 16651-16665; DOI: https://doi.org/10.1523/JNEUROSCI.0681-12.2012
Javier Díaz-Alonso
1Research Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), 28049 Madrid, Spain,
2Department of Biochemistry and Molecular Biology I, Ramón y Cajal Institute of Health Research and Neurochemistry Research Institute, Complutense University, 28040 Madrid, Spain,
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Tania Aguado
1Research Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), 28049 Madrid, Spain,
2Department of Biochemistry and Molecular Biology I, Ramón y Cajal Institute of Health Research and Neurochemistry Research Institute, Complutense University, 28040 Madrid, Spain,
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Chia-Shan Wu
3The Cain Foundation Laboratories, Jan and Dan Duncan Neurological Research Institute, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030,
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Javier Palazuelos
1Research Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), 28049 Madrid, Spain,
2Department of Biochemistry and Molecular Biology I, Ramón y Cajal Institute of Health Research and Neurochemistry Research Institute, Complutense University, 28040 Madrid, Spain,
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Clementine Hofmann
4Institute of Physiological Chemistry, Medical Center of the Johannes Gutenberg University Mainz, 55128 Mainz, Germany,
5Focus Program Translational Neuroscience, Johannes Gutenberg University, 55131 Mainz, Germany, and
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Patricia Garcez
6Division of Molecular Neurobiology, National Institute of Medical Research, London, NW7 1AA, United Kingdom
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François Guillemot
6Division of Molecular Neurobiology, National Institute of Medical Research, London, NW7 1AA, United Kingdom
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Hui-Chen Lu
3The Cain Foundation Laboratories, Jan and Dan Duncan Neurological Research Institute, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030,
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Beat Lutz
4Institute of Physiological Chemistry, Medical Center of the Johannes Gutenberg University Mainz, 55128 Mainz, Germany,
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Manuel Guzmán
1Research Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), 28049 Madrid, Spain,
2Department of Biochemistry and Molecular Biology I, Ramón y Cajal Institute of Health Research and Neurochemistry Research Institute, Complutense University, 28040 Madrid, Spain,
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Ismael Galve-Roperh
1Research Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), 28049 Madrid, Spain,
2Department of Biochemistry and Molecular Biology I, Ramón y Cajal Institute of Health Research and Neurochemistry Research Institute, Complutense University, 28040 Madrid, Spain,
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Abstract

The generation and specification of pyramidal neuron subpopulations during development relies on a complex network of transcription factors. The CB1 cannabinoid receptor is the major molecular target of endocannabinoids and marijuana active compounds. This receptor has been shown to influence neural progenitor proliferation and axonal growth, but its involvement in neuronal differentiation and the functional impact in the adulthood caused by altering its signaling during brain development are not known. Here we show that the CB1 receptor, by preventing Satb2 (special AT-rich binding protein 2)-mediated repression, increased Ctip2 (COUP-TF interacting protein 2) promoter activity, and Ctip2-positive neuron generation. Unbalanced neurogenic fate determination found in complete CB1−/− mice and in glutamatergic neuron-specific Nex–CB1−/− mice induced overt alterations in corticospinal motor neuron generation and subcerebral connectivity, thereby resulting in an impairment of skilled motor function in adult mice. Likewise, genetic deletion of CB1 receptors in Thy1–YFP–H mice elicited alterations in corticospinal tract development. Altogether, these data demonstrate that the CB1 receptor contributes to the generation of deep-layer cortical neurons by coupling endocannabinoid signals from the neurogenic niche to the intrinsic proneurogenic Ctip2/Satb2 axis, thus influencing appropriate subcerebral projection neuron specification and corticospinal motor function in the adulthood.

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The Journal of Neuroscience: 32 (47)
Journal of Neuroscience
Vol. 32, Issue 47
21 Nov 2012
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The CB1 Cannabinoid Receptor Drives Corticospinal Motor Neuron Differentiation through the Ctip2/Satb2 Transcriptional Regulation Axis
Javier Díaz-Alonso, Tania Aguado, Chia-Shan Wu, Javier Palazuelos, Clementine Hofmann, Patricia Garcez, François Guillemot, Hui-Chen Lu, Beat Lutz, Manuel Guzmán, Ismael Galve-Roperh
Journal of Neuroscience 21 November 2012, 32 (47) 16651-16665; DOI: 10.1523/JNEUROSCI.0681-12.2012

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The CB1 Cannabinoid Receptor Drives Corticospinal Motor Neuron Differentiation through the Ctip2/Satb2 Transcriptional Regulation Axis
Javier Díaz-Alonso, Tania Aguado, Chia-Shan Wu, Javier Palazuelos, Clementine Hofmann, Patricia Garcez, François Guillemot, Hui-Chen Lu, Beat Lutz, Manuel Guzmán, Ismael Galve-Roperh
Journal of Neuroscience 21 November 2012, 32 (47) 16651-16665; DOI: 10.1523/JNEUROSCI.0681-12.2012
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