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Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice

Neurological complications affecting the central nervous system have been reported in adult patients infected by Zika virus (ZIKV) but the underlying mechanisms remain unknown. Here, we report that ZIKV replicates in human and mouse adult brain tissue, targeting mature neurons. ZIKV preferentially t...

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Autores principales: Figueiredo, Claudia P., Barros-Aragão, Fernanda G. Q., Neris, Rômulo L. S., Frost, Paula S., Soares, Carolina, Souza, Isis N. O., Zeidler, Julianna D., Zamberlan, Daniele C., de Sousa, Virginia L., Souza, Amanda S., Guimarães, André Luis A., Bellio, Maria, Marcondes de Souza, Jorge, Alves-Leon, Soniza V., Neves, Gilda A., Paula-Neto, Heitor A., Castro, Newton G., De Felice, Fernanda G., Assunção-Miranda, Iranaia, Clarke, Julia R., Da Poian, Andrea T., Ferreira, Sergio T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6728367/
https://www.ncbi.nlm.nih.gov/pubmed/31488835
http://dx.doi.org/10.1038/s41467-019-11866-7
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author Figueiredo, Claudia P.
Barros-Aragão, Fernanda G. Q.
Neris, Rômulo L. S.
Frost, Paula S.
Soares, Carolina
Souza, Isis N. O.
Zeidler, Julianna D.
Zamberlan, Daniele C.
de Sousa, Virginia L.
Souza, Amanda S.
Guimarães, André Luis A.
Bellio, Maria
Marcondes de Souza, Jorge
Alves-Leon, Soniza V.
Neves, Gilda A.
Paula-Neto, Heitor A.
Castro, Newton G.
De Felice, Fernanda G.
Assunção-Miranda, Iranaia
Clarke, Julia R.
Da Poian, Andrea T.
Ferreira, Sergio T.
author_facet Figueiredo, Claudia P.
Barros-Aragão, Fernanda G. Q.
Neris, Rômulo L. S.
Frost, Paula S.
Soares, Carolina
Souza, Isis N. O.
Zeidler, Julianna D.
Zamberlan, Daniele C.
de Sousa, Virginia L.
Souza, Amanda S.
Guimarães, André Luis A.
Bellio, Maria
Marcondes de Souza, Jorge
Alves-Leon, Soniza V.
Neves, Gilda A.
Paula-Neto, Heitor A.
Castro, Newton G.
De Felice, Fernanda G.
Assunção-Miranda, Iranaia
Clarke, Julia R.
Da Poian, Andrea T.
Ferreira, Sergio T.
author_sort Figueiredo, Claudia P.
collection PubMed
description Neurological complications affecting the central nervous system have been reported in adult patients infected by Zika virus (ZIKV) but the underlying mechanisms remain unknown. Here, we report that ZIKV replicates in human and mouse adult brain tissue, targeting mature neurons. ZIKV preferentially targets memory-related brain regions, inhibits hippocampal long-term potentiation and induces memory impairment in adult mice. TNF-α upregulation, microgliosis and upregulation of complement system proteins, C1q and C3, are induced by ZIKV infection. Microglia are found to engulf hippocampal presynaptic terminals during acute infection. Neutralization of TNF-α signaling, blockage of microglial activation or of C1q/C3 prevent synapse and memory impairment in ZIKV-infected mice. Results suggest that ZIKV induces synapse and memory dysfunction via aberrant activation of TNF-α, microglia and complement. Our findings establish a mechanism by which ZIKV affects the adult brain, and point to the need of evaluating cognitive deficits as a potential comorbidity in ZIKV-infected adults.
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spelling pubmed-67283672019-09-09 Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice Figueiredo, Claudia P. Barros-Aragão, Fernanda G. Q. Neris, Rômulo L. S. Frost, Paula S. Soares, Carolina Souza, Isis N. O. Zeidler, Julianna D. Zamberlan, Daniele C. de Sousa, Virginia L. Souza, Amanda S. Guimarães, André Luis A. Bellio, Maria Marcondes de Souza, Jorge Alves-Leon, Soniza V. Neves, Gilda A. Paula-Neto, Heitor A. Castro, Newton G. De Felice, Fernanda G. Assunção-Miranda, Iranaia Clarke, Julia R. Da Poian, Andrea T. Ferreira, Sergio T. Nat Commun Article Neurological complications affecting the central nervous system have been reported in adult patients infected by Zika virus (ZIKV) but the underlying mechanisms remain unknown. Here, we report that ZIKV replicates in human and mouse adult brain tissue, targeting mature neurons. ZIKV preferentially targets memory-related brain regions, inhibits hippocampal long-term potentiation and induces memory impairment in adult mice. TNF-α upregulation, microgliosis and upregulation of complement system proteins, C1q and C3, are induced by ZIKV infection. Microglia are found to engulf hippocampal presynaptic terminals during acute infection. Neutralization of TNF-α signaling, blockage of microglial activation or of C1q/C3 prevent synapse and memory impairment in ZIKV-infected mice. Results suggest that ZIKV induces synapse and memory dysfunction via aberrant activation of TNF-α, microglia and complement. Our findings establish a mechanism by which ZIKV affects the adult brain, and point to the need of evaluating cognitive deficits as a potential comorbidity in ZIKV-infected adults. Nature Publishing Group UK 2019-09-05 /pmc/articles/PMC6728367/ /pubmed/31488835 http://dx.doi.org/10.1038/s41467-019-11866-7 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Figueiredo, Claudia P.
Barros-Aragão, Fernanda G. Q.
Neris, Rômulo L. S.
Frost, Paula S.
Soares, Carolina
Souza, Isis N. O.
Zeidler, Julianna D.
Zamberlan, Daniele C.
de Sousa, Virginia L.
Souza, Amanda S.
Guimarães, André Luis A.
Bellio, Maria
Marcondes de Souza, Jorge
Alves-Leon, Soniza V.
Neves, Gilda A.
Paula-Neto, Heitor A.
Castro, Newton G.
De Felice, Fernanda G.
Assunção-Miranda, Iranaia
Clarke, Julia R.
Da Poian, Andrea T.
Ferreira, Sergio T.
Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title_full Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title_fullStr Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title_full_unstemmed Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title_short Zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
title_sort zika virus replicates in adult human brain tissue and impairs synapses and memory in mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6728367/
https://www.ncbi.nlm.nih.gov/pubmed/31488835
http://dx.doi.org/10.1038/s41467-019-11866-7
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