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Featured ArticleArticles, Cellular/Molecular

Orexin–Corticotropin-Releasing Factor Receptor Heteromers in the Ventral Tegmental Area as Targets for Cocaine

Gemma Navarro, César Quiroz, David Moreno-Delgado, Adam Sierakowiak, Kimberly McDowell, Estefanía Moreno, William Rea, Ning-Sheng Cai, David Aguinaga, Lesley A. Howell, Felix Hausch, Antonio Cortés, Josefa Mallol, Vicent Casadó, Carme Lluís, Enric I. Canela, Sergi Ferré and Peter J. McCormick
Journal of Neuroscience 29 April 2015, 35 (17) 6639-6653; DOI: https://doi.org/10.1523/JNEUROSCI.4364-14.2015
Gemma Navarro
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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César Quiroz
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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David Moreno-Delgado
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Adam Sierakowiak
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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Kimberly McDowell
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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Estefanía Moreno
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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William Rea
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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Ning-Sheng Cai
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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David Aguinaga
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Lesley A. Howell
3School of Pharmacy, University of East Anglia, Norwich, NR4 7TJ, United Kingdom, and
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Felix Hausch
4Max Planck Institute of Psychiatry, 80804 Munich, Germany
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Antonio Cortés
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Josefa Mallol
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Vicent Casadó
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Carme Lluís
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Enric I. Canela
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
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Sergi Ferré
2Integrative Neurobiology Section, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland 21224,
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Peter J. McCormick
1Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Center for Biomedical Research in Neurodegenerative Diseases Network and Institute of Biomedicine of the University of Barcelona, 08028 Barcelona, Spain,
3School of Pharmacy, University of East Anglia, Norwich, NR4 7TJ, United Kingdom, and
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Abstract

Release of the neuropeptides corticotropin-releasing factor (CRF) and orexin-A in the ventral tegmental area (VTA) play an important role in stress-induced cocaine-seeking behavior. We provide evidence for pharmacologically significant interactions between CRF and orexin-A that depend on oligomerization of CRF1 receptor (CRF1R) and orexin OX1 receptors (OX1R). CRF1R–OX1R heteromers are the conduits of a negative crosstalk between orexin-A and CRF as demonstrated in transfected cells and rat VTA, in which they significantly modulate dendritic dopamine release. The cocaine target σ1 receptor (σ1R) also associates with the CRF1R–OX1R heteromer. Cocaine binding to the σ1R–CRF1R–OX1R complex promotes a long-term disruption of the orexin-A–CRF negative crosstalk. Through this mechanism, cocaine sensitizes VTA cells to the excitatory effects of both CRF and orexin-A, thus providing a mechanism by which stress induces cocaine seeking.

  • cocaine
  • CRF receptor
  • GPCR heteromer
  • orexin receptor
  • sigma receptor
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The Journal of Neuroscience: 35 (17)
Journal of Neuroscience
Vol. 35, Issue 17
29 Apr 2015
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Orexin–Corticotropin-Releasing Factor Receptor Heteromers in the Ventral Tegmental Area as Targets for Cocaine
Gemma Navarro, César Quiroz, David Moreno-Delgado, Adam Sierakowiak, Kimberly McDowell, Estefanía Moreno, William Rea, Ning-Sheng Cai, David Aguinaga, Lesley A. Howell, Felix Hausch, Antonio Cortés, Josefa Mallol, Vicent Casadó, Carme Lluís, Enric I. Canela, Sergi Ferré, Peter J. McCormick
Journal of Neuroscience 29 April 2015, 35 (17) 6639-6653; DOI: 10.1523/JNEUROSCI.4364-14.2015

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Orexin–Corticotropin-Releasing Factor Receptor Heteromers in the Ventral Tegmental Area as Targets for Cocaine
Gemma Navarro, César Quiroz, David Moreno-Delgado, Adam Sierakowiak, Kimberly McDowell, Estefanía Moreno, William Rea, Ning-Sheng Cai, David Aguinaga, Lesley A. Howell, Felix Hausch, Antonio Cortés, Josefa Mallol, Vicent Casadó, Carme Lluís, Enric I. Canela, Sergi Ferré, Peter J. McCormick
Journal of Neuroscience 29 April 2015, 35 (17) 6639-6653; DOI: 10.1523/JNEUROSCI.4364-14.2015
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Keywords

  • cocaine
  • CRF receptor
  • GPCR heteromer
  • orexin receptor
  • sigma receptor

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