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Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA

Bornaviruses, which chronically infect many species, can cause severe neurological diseases in some animal species; their association with human neuropsychiatric disorders is, however, debatable. The epidemiology of Borna disease virus (BDV), as for other members of the family Bornaviridae, is large...

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Autores principales: Kinnunen, Paula Maria, Inkeroinen, Hanna, Ilander, Mette, Kallio, Eva Riikka, Heikkilä, Henna Pauliina, Koskela, Esa, Mappes, Tapio, Palva, Airi, Vaheri, Antti, Kipar, Anja, Vapalahti, Olli
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174072/
https://www.ncbi.nlm.nih.gov/pubmed/21935357
http://dx.doi.org/10.1371/journal.pone.0023622
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author Kinnunen, Paula Maria
Inkeroinen, Hanna
Ilander, Mette
Kallio, Eva Riikka
Heikkilä, Henna Pauliina
Koskela, Esa
Mappes, Tapio
Palva, Airi
Vaheri, Antti
Kipar, Anja
Vapalahti, Olli
author_facet Kinnunen, Paula Maria
Inkeroinen, Hanna
Ilander, Mette
Kallio, Eva Riikka
Heikkilä, Henna Pauliina
Koskela, Esa
Mappes, Tapio
Palva, Airi
Vaheri, Antti
Kipar, Anja
Vapalahti, Olli
author_sort Kinnunen, Paula Maria
collection PubMed
description Bornaviruses, which chronically infect many species, can cause severe neurological diseases in some animal species; their association with human neuropsychiatric disorders is, however, debatable. The epidemiology of Borna disease virus (BDV), as for other members of the family Bornaviridae, is largely unknown, although evidence exists for a reservoir in small mammals, for example bank voles (Myodes glareolus). In addition to the current exogenous infections and despite the fact that bornaviruses have an RNA genome, bornavirus sequences integrated into the genomes of several vertebrates millions of years ago. Our hypothesis is that the bank vole, a common wild rodent species in traditional BDV-endemic areas, can serve as a viral host; we therefore explored whether this species can be infected with BDV, and if so, how the virus spreads and whether viral RNA is transcribed into DNA in vivo. We infected neonate bank voles intracerebrally with BDV and euthanized them 2 to 8 weeks post-infection. Specific Ig antibodies were detectable in 41%. Histological evaluation revealed no significant pathological alterations, but BDV RNA and antigen were detectable in all infected brains. Immunohistology demonstrated centrifugal spread throughout the nervous tissue, because viral antigen was widespread in peripheral nerves and ganglia, including the mediastinum, esophagus, and urinary bladder. This was associated with viral shedding in feces, of which 54% were BDV RNA-positive, and urine at 17%. BDV nucleocapsid gene DNA occurred in 66% of the infected voles, and, surprisingly, occasionally also phosphoprotein DNA. Thus, intracerebral BDV infection of bank vole led to systemic infection of the nervous tissue and viral excretion, as well as frequent reverse transcription of the BDV genome, enabling genomic integration. This first experimental bornavirus infection in wild mammals confirms the recent findings regarding bornavirus DNA, and suggests that bank voles are capable of bornavirus transmission.
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spelling pubmed-31740722011-09-20 Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA Kinnunen, Paula Maria Inkeroinen, Hanna Ilander, Mette Kallio, Eva Riikka Heikkilä, Henna Pauliina Koskela, Esa Mappes, Tapio Palva, Airi Vaheri, Antti Kipar, Anja Vapalahti, Olli PLoS One Research Article Bornaviruses, which chronically infect many species, can cause severe neurological diseases in some animal species; their association with human neuropsychiatric disorders is, however, debatable. The epidemiology of Borna disease virus (BDV), as for other members of the family Bornaviridae, is largely unknown, although evidence exists for a reservoir in small mammals, for example bank voles (Myodes glareolus). In addition to the current exogenous infections and despite the fact that bornaviruses have an RNA genome, bornavirus sequences integrated into the genomes of several vertebrates millions of years ago. Our hypothesis is that the bank vole, a common wild rodent species in traditional BDV-endemic areas, can serve as a viral host; we therefore explored whether this species can be infected with BDV, and if so, how the virus spreads and whether viral RNA is transcribed into DNA in vivo. We infected neonate bank voles intracerebrally with BDV and euthanized them 2 to 8 weeks post-infection. Specific Ig antibodies were detectable in 41%. Histological evaluation revealed no significant pathological alterations, but BDV RNA and antigen were detectable in all infected brains. Immunohistology demonstrated centrifugal spread throughout the nervous tissue, because viral antigen was widespread in peripheral nerves and ganglia, including the mediastinum, esophagus, and urinary bladder. This was associated with viral shedding in feces, of which 54% were BDV RNA-positive, and urine at 17%. BDV nucleocapsid gene DNA occurred in 66% of the infected voles, and, surprisingly, occasionally also phosphoprotein DNA. Thus, intracerebral BDV infection of bank vole led to systemic infection of the nervous tissue and viral excretion, as well as frequent reverse transcription of the BDV genome, enabling genomic integration. This first experimental bornavirus infection in wild mammals confirms the recent findings regarding bornavirus DNA, and suggests that bank voles are capable of bornavirus transmission. Public Library of Science 2011-08-22 /pmc/articles/PMC3174072/ /pubmed/21935357 http://dx.doi.org/10.1371/journal.pone.0023622 Text en Kinnunen et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kinnunen, Paula Maria
Inkeroinen, Hanna
Ilander, Mette
Kallio, Eva Riikka
Heikkilä, Henna Pauliina
Koskela, Esa
Mappes, Tapio
Palva, Airi
Vaheri, Antti
Kipar, Anja
Vapalahti, Olli
Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title_full Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title_fullStr Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title_full_unstemmed Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title_short Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA
title_sort intracerebral borna disease virus infection of bank voles leading to peripheral spread and reverse transcription of viral rna
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174072/
https://www.ncbi.nlm.nih.gov/pubmed/21935357
http://dx.doi.org/10.1371/journal.pone.0023622
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