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Research Article

Impaired learning resulting from Respiratory Syncytial Virus infection

Janyra A. Espinoza, Karen Bohmwald, Pablo F. Céspedes, Roberto S. Gómez, Sebastián A. Riquelme, Claudia M. Cortés, Javier A. Valenzuela, Rodrigo A. Sandoval, Floria C. Pancetti, Susan M. Bueno, Claudia A. Riedel, and Alexis M. Kalergis
PNAS first published May 6, 2013; https://doi.org/10.1073/pnas.1217508110
Janyra A. Espinoza
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
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Karen Bohmwald
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
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Pablo F. Céspedes
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
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Roberto S. Gómez
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
bInstitut National de la Santé et de la Recherche Médicale, Unité 1064, 44093 Nantes, France;
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Sebastián A. Riquelme
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
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Claudia M. Cortés
cMillenium Institute on Immunology and Immunotherapy, Departamento de Ciencias Biológicas, Facultad de Ciencias Biológicas y Facultad de Medicina, Universidad Andrés Bello, Santiago 8370146, Chile;
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Javier A. Valenzuela
dLaboratorio de Neurotoxicología Ambiental, Departamento de Ciencias Biomédicas, Facultad de Medicina, Universidad Católica del Norte, Coquimbo 1781421, Chile; and
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Rodrigo A. Sandoval
dLaboratorio de Neurotoxicología Ambiental, Departamento de Ciencias Biomédicas, Facultad de Medicina, Universidad Católica del Norte, Coquimbo 1781421, Chile; and
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Floria C. Pancetti
dLaboratorio de Neurotoxicología Ambiental, Departamento de Ciencias Biomédicas, Facultad de Medicina, Universidad Católica del Norte, Coquimbo 1781421, Chile; and
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Susan M. Bueno
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
bInstitut National de la Santé et de la Recherche Médicale, Unité 1064, 44093 Nantes, France;
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Claudia A. Riedel
cMillenium Institute on Immunology and Immunotherapy, Departamento de Ciencias Biológicas, Facultad de Ciencias Biológicas y Facultad de Medicina, Universidad Andrés Bello, Santiago 8370146, Chile;
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  • For correspondence: akalergis@bio.puc.cl claudia.riedel@unab.cl
Alexis M. Kalergis
aMillenium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile;
bInstitut National de la Santé et de la Recherche Médicale, Unité 1064, 44093 Nantes, France;
eDepartamento de Reumatología, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago 8331010, Chile
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  • For correspondence: akalergis@bio.puc.cl claudia.riedel@unab.cl
  1. Edited by Peter Palese, Mount Sinai School of Medicine, New York, NY, and approved April 15, 2013 (received for review October 15, 2012)

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Abstract

Respiratory syncytial virus (RSV) is the major cause of respiratory illness in infants worldwide. Neurologic alterations, such as seizures and ataxia, have been associated with RSV infection. We demonstrate the presence of RSV proteins and RNA in zones of the brain—such as the hippocampus, ventromedial hypothalamic nucleus, and brainstem—of infected mice. One month after disease resolution, rodents showed behavioral and cognitive impairment in marble burying (MB) and Morris water maze (MWM) tests. Our data indicate that the learning impairment caused by RSV is a result of a deficient induction of long-term potentiation in the hippocampus of infected animals. In addition, immunization with recombinant bacillus Calmette–Guérin (BCG) expressing RSV nucleoprotein prevented behavioral disorders, corroborating the specific effect of RSV infection over the central nervous system. Our findings provide evidence that RSV can spread from the airways to the central nervous system and cause functional alterations to the brain, both of which can be prevented by proper immunization against RSV.

  • cognition
  • behavior
  • inflammation
  • LTP
  • LTD

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: akalergis{at}bio.puc.cl or claudia.riedel{at}unab.cl.
  • Author contributions: S.M.B., C.A.R., and A.M.K. designed research; J.A.E., K.B., P.F.C., R.S.G., C.M.C., and J.A.V. performed research; S.A.R., R.A.S., and F.C.P. analyzed data; and J.A.E., S.M.B., C.A.R., and A.M.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1217508110/-/DCSupplemental.

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RSV infection in the CNS
Janyra A. Espinoza, Karen Bohmwald, Pablo F. Céspedes, Roberto S. Gómez, Sebastián A. Riquelme, Claudia M. Cortés, Javier A. Valenzuela, Rodrigo A. Sandoval, Floria C. Pancetti, Susan M. Bueno, Claudia A. Riedel, Alexis M. Kalergis
Proceedings of the National Academy of Sciences May 2013, 201217508; DOI: 10.1073/pnas.1217508110

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RSV infection in the CNS
Janyra A. Espinoza, Karen Bohmwald, Pablo F. Céspedes, Roberto S. Gómez, Sebastián A. Riquelme, Claudia M. Cortés, Javier A. Valenzuela, Rodrigo A. Sandoval, Floria C. Pancetti, Susan M. Bueno, Claudia A. Riedel, Alexis M. Kalergis
Proceedings of the National Academy of Sciences May 2013, 201217508; DOI: 10.1073/pnas.1217508110
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