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Cover ArticleArticles, Cellular/Molecular

Coxsackievirus Adenovirus Receptor Loss Impairs Adult Neurogenesis, Synapse Content, and Hippocampus Plasticity

Charleine Zussy, Fabien Loustalot, Felix Junyent, Fabrizio Gardoni, Cyril Bories, Jorge Valero, Michel G. Desarménien, Florence Bernex, Daniel Henaff, Neus Bayo-Puxan, Jin-Wen Chen, Nicolas Lonjon, Yves de Koninck, João O. Malva, Jeffrey M. Bergelson, Monica di Luca, Giampietro Schiavo, Sara Salinas and Eric J. Kremer
Journal of Neuroscience 14 September 2016, 36 (37) 9558-9571; https://doi.org/10.1523/JNEUROSCI.0132-16.2016
Charleine Zussy
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Fabien Loustalot
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Felix Junyent
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Fabrizio Gardoni
3Università degli Studi di Milano, Department of Pharmacological Sciences and Centre of Excellence on Neurodegenerative Diseases, 20122 Milan, Italy,
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Cyril Bories
4Mental Health Institute of Quebec and Department of Psychiatry and Neuroscience, Faculty of Medicine, Laval University, Quebec City, G1V 0A6 Quebec, Canada,
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Jorge Valero
10Center for Neuroscience and Cell Biology, Faculty of Medicine, University of Coimbra, 3004-504 Coimbra, Portugal
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Michel G. Desarménien
2Université de Montpellier, 34000 Montpellier, France,
5Institut de Génomique Fonctionnelle, Centre National de la Recherche Scientifique, Inserm, 34394 Montpellier, France,
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Florence Bernex
6Institut Régional du Cancer Montpellier, Inserm, 34090 Montpellier, France,
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Daniel Henaff
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Neus Bayo-Puxan
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Jin-Wen Chen
7Division of Infectious Diseases, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania 19104,
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Nicolas Lonjon
8Département de Neurochirurgie, Hôpital Gui de Chauliac, 34000 Montpellier, France,
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Yves de Koninck
4Mental Health Institute of Quebec and Department of Psychiatry and Neuroscience, Faculty of Medicine, Laval University, Quebec City, G1V 0A6 Quebec, Canada,
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João O. Malva
10Center for Neuroscience and Cell Biology, Faculty of Medicine, University of Coimbra, 3004-504 Coimbra, Portugal
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Jeffrey M. Bergelson
7Division of Infectious Diseases, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania 19104,
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Monica di Luca
3Università degli Studi di Milano, Department of Pharmacological Sciences and Centre of Excellence on Neurodegenerative Diseases, 20122 Milan, Italy,
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Giampietro Schiavo
9Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom, and
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Sara Salinas
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Eric J. Kremer
1Institut de Génétique Moléculaire de Montpellier, Centre National de la Recherche Scientifique 5535, 34293 Montpellier, France,
2Université de Montpellier, 34000 Montpellier, France,
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Abstract

Although we are beginning to understand the late stage of neurodegenerative diseases, the molecular defects associated with the initiation of impaired cognition are poorly characterized. Here, we demonstrate that in the adult brain, the coxsackievirus and adenovirus receptor (CAR) is located on neuron projections, at the presynapse in mature neurons, and on the soma of immature neurons in the hippocampus. In a proinflammatory or diseased environment, CAR is lost from immature neurons in the hippocampus. Strikingly, in hippocampi of patients at early stages of late-onset Alzheimer's disease (AD), CAR levels are significantly reduced. Similarly, in triple-transgenic AD mice, CAR levels in hippocampi are low and further reduced after systemic inflammation. Genetic deletion of CAR from the mouse brain triggers deficits in adult neurogenesis and synapse homeostasis that lead to impaired hippocampal plasticity and cognitive deficits. We propose that post-translational CAR loss of function contributes to cognitive defects in healthy and diseased-primed brains.

SIGNIFICANCE STATEMENT This study addressed the role of the coxsackievirus and adenovirus receptor (CAR), a single-pass cell adhesion molecule, in the adult brain. Our results demonstrate that CAR is expressed by mature neurons throughout the brain. In addition, we propose divergent roles for CAR in immature neurons, during neurogenesis, and at the mature synapse. Notably, CAR loss of function also affects hippocampal plasticity.

  • adult neurogenesis
  • Alzheimer's disease
  • coxsakievirus and adenovirus receptor
  • inflammation
  • synapse
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The Journal of Neuroscience: 36 (37)
Journal of Neuroscience
Vol. 36, Issue 37
14 Sep 2016
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Coxsackievirus Adenovirus Receptor Loss Impairs Adult Neurogenesis, Synapse Content, and Hippocampus Plasticity
Charleine Zussy, Fabien Loustalot, Felix Junyent, Fabrizio Gardoni, Cyril Bories, Jorge Valero, Michel G. Desarménien, Florence Bernex, Daniel Henaff, Neus Bayo-Puxan, Jin-Wen Chen, Nicolas Lonjon, Yves de Koninck, João O. Malva, Jeffrey M. Bergelson, Monica di Luca, Giampietro Schiavo, Sara Salinas, Eric J. Kremer
Journal of Neuroscience 14 September 2016, 36 (37) 9558-9571; DOI: 10.1523/JNEUROSCI.0132-16.2016

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Coxsackievirus Adenovirus Receptor Loss Impairs Adult Neurogenesis, Synapse Content, and Hippocampus Plasticity
Charleine Zussy, Fabien Loustalot, Felix Junyent, Fabrizio Gardoni, Cyril Bories, Jorge Valero, Michel G. Desarménien, Florence Bernex, Daniel Henaff, Neus Bayo-Puxan, Jin-Wen Chen, Nicolas Lonjon, Yves de Koninck, João O. Malva, Jeffrey M. Bergelson, Monica di Luca, Giampietro Schiavo, Sara Salinas, Eric J. Kremer
Journal of Neuroscience 14 September 2016, 36 (37) 9558-9571; DOI: 10.1523/JNEUROSCI.0132-16.2016
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Keywords

  • adult neurogenesis
  • Alzheimer's disease
  • coxsakievirus and adenovirus receptor
  • inflammation
  • synapse

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