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Molecular Pharmacology

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Research ArticleArticle

Axon-to-Glia Interaction Regulates GABAA Receptor Expression in Oligodendrocytes

Rogelio O. Arellano, María Victoria Sánchez-Gómez, Elena Alberdi, Manuel Canedo-Antelo, Juan Carlos Chara, Aitor Palomino, Alberto Pérez-Samartín and Carlos Matute
Molecular Pharmacology January 2016, 89 (1) 63-74; DOI: https://doi.org/10.1124/mol.115.100594
Rogelio O. Arellano
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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María Victoria Sánchez-Gómez
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Elena Alberdi
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Manuel Canedo-Antelo
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Juan Carlos Chara
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Aitor Palomino
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Alberto Pérez-Samartín
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Carlos Matute
Achucarro Basque Center for Neuroscience, Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas, and Departamento de Neurociencias, Universidad del País Vasco, Leioa, Spain (R.O.A., M.V.S.-G., E.A., M.C.-A., J.C.C., A.P., A.P.-S., C.M.); and Instituto de Neurobiología, Laboratorio de Neurofisiología Celular, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México (R.O.A.)
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Abstract

Myelination requires oligodendrocyte-neuron communication, and both neurotransmitters and contact interactions are essential for this process. Oligodendrocytes are endowed with neurotransmitter receptors whose expression levels and properties may change during myelination. However, only scant information is available about the extent and timing of these changes or how they are regulated by oligodendrocyte-neuron interactions. Here, we used electrophysiology to study the expression of ionotropic GABA, glutamate, and ATP receptors in oligodendrocytes derived from the optic nerve and forebrain cultured either alone or in the presence of dorsal root ganglion neurons. We observed that oligodendrocytes from both regions responded to these transmitters at 1 day in culture. After the first day in culture, however, GABA sensitivity diminished drastically to less than 10%, while that of glutamate and ATP remained constant. In contrast, the GABA response amplitude was sustained and remained stable in oligodendrocytes cocultured with dorsal root ganglion neurons. Immunochemistry and pharmacological properties of the responses indicated that they were mediated by distinctive GABAA receptors and that in coculture with neurons, the oligodendrocytes bearing the receptors were those in direct contact with axons. These results reveal that GABAA receptor regulation in oligodendrocytes is driven by axonal cues and that GABA signaling may play a role in myelination and/or during axon-glia recognition.

Footnotes

    • Received June 29, 2015.
    • Accepted November 3, 2015.
  • This study was funded by the Ministerio de Economía y Competitividad/Fondos Europeos de Desarrollo Regional [Grants SAF2010-21547 and SAF2013-45084-R] and the Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas [Grant PRY-15-404].

  • Some information reported herein was presented as follows: Arellano RO, Sánchez-Gómez MV, Alberdi E, Canedo M, Palomino A, Pérez-Samartín A, and Matute C (2015) Neuron and glia interaction regulates GABAA receptor expression in the oligodendrocyte membrane. XII European Meeting on Glial Cells in Health and Disease; on July 15 and 16, 2015; Bilbao, Spain. Network Glia, Berlin, Germany.

  • dx.doi.org/10.1124/mol.115.100594.

  • Copyright © 2015 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 89 (1)
Molecular Pharmacology
Vol. 89, Issue 1
1 Jan 2016
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Research ArticleArticle

GABAA Receptor Expression in Myelinating Oligodendrocytes

Rogelio O. Arellano, María Victoria Sánchez-Gómez, Elena Alberdi, Manuel Canedo-Antelo, Juan Carlos Chara, Aitor Palomino, Alberto Pérez-Samartín and Carlos Matute
Molecular Pharmacology January 1, 2016, 89 (1) 63-74; DOI: https://doi.org/10.1124/mol.115.100594

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Research ArticleArticle

GABAA Receptor Expression in Myelinating Oligodendrocytes

Rogelio O. Arellano, María Victoria Sánchez-Gómez, Elena Alberdi, Manuel Canedo-Antelo, Juan Carlos Chara, Aitor Palomino, Alberto Pérez-Samartín and Carlos Matute
Molecular Pharmacology January 1, 2016, 89 (1) 63-74; DOI: https://doi.org/10.1124/mol.115.100594
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