Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity

Mammalian Bornavirus (BoDV-1) typically causes a fatal neurologic disorder in horses and sheep, and was recently shown to cause fatal encephalitis in humans with and without transplant reception. It has been suggested that BoDV-1 enters the central nervous system (CNS) via the olfactory pathway. How...

Full description

Bibliographic Details
Main Authors: Alexandra Kupke, Sabrina Becker, Konstantin Wewetzer, Barbara Ahlemeyer, Markus Eickmann, Christiane Herden
Format: Article
Language:English
Published: MDPI AG 2019-03-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:http://www.mdpi.com/1422-0067/20/6/1318
_version_ 1811197656698978304
author Alexandra Kupke
Sabrina Becker
Konstantin Wewetzer
Barbara Ahlemeyer
Markus Eickmann
Christiane Herden
author_facet Alexandra Kupke
Sabrina Becker
Konstantin Wewetzer
Barbara Ahlemeyer
Markus Eickmann
Christiane Herden
author_sort Alexandra Kupke
collection DOAJ
description Mammalian Bornavirus (BoDV-1) typically causes a fatal neurologic disorder in horses and sheep, and was recently shown to cause fatal encephalitis in humans with and without transplant reception. It has been suggested that BoDV-1 enters the central nervous system (CNS) via the olfactory pathway. However, (I) susceptible cell types that replicate the virus for successful spread, and (II) the role of olfactory ensheathing cells (OECs), remained unclear. To address this, we studied the intranasal infection of adult rats with BoDV-1 in vivo and in vitro, using olfactory mucosal (OM) cell cultures and the cultures of purified OECs. Strikingly, in vitro and in vivo, viral antigen and mRNA were present from four days post infection (dpi) onwards in the olfactory receptor neurons (ORNs), but also in all other cell types of the OM, and constantly in the OECs. In contrast, in vivo, BoDV-1 genomic RNA was only detectable in adult and juvenile ORNs, nerve fibers, and in OECs from 7 dpi on. In vitro, the rate of infection of OECs was significantly higher than that of the OM cells, pointing to a crucial role of OECs for infection via the olfactory pathway. Thus, this study provides important insights into the transmission of neurotropic viral infections with a zoonotic potential.
first_indexed 2024-04-12T01:17:29Z
format Article
id doaj.art-46e83028d6f645fcac809a5ab29d5908
institution Directory Open Access Journal
issn 1422-0067
language English
last_indexed 2024-04-12T01:17:29Z
publishDate 2019-03-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-46e83028d6f645fcac809a5ab29d59082022-12-22T03:53:53ZengMDPI AGInternational Journal of Molecular Sciences1422-00672019-03-01206131810.3390/ijms20061318ijms20061318Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential ContagiosityAlexandra Kupke0Sabrina Becker1Konstantin Wewetzer2Barbara Ahlemeyer3Markus Eickmann4Christiane Herden5Institute of Veterinary Pathology, Justus Liebig University, 35392 Giessen, GermanyInstitute of Veterinary Pathology, Justus Liebig University, 35392 Giessen, GermanyInstitute of Functional and Applied Anatomy, Hannover Medical School, 30625 Hannover, GermanyInstitute for Anatomy and Cell Biology, Division of Medical Cell Biology, Justus Liebig University, 35385 Giessen, GermanyInstitute of Virology, Philipps University, 35043 Marburg, GermanyInstitute of Veterinary Pathology, Justus Liebig University, 35392 Giessen, GermanyMammalian Bornavirus (BoDV-1) typically causes a fatal neurologic disorder in horses and sheep, and was recently shown to cause fatal encephalitis in humans with and without transplant reception. It has been suggested that BoDV-1 enters the central nervous system (CNS) via the olfactory pathway. However, (I) susceptible cell types that replicate the virus for successful spread, and (II) the role of olfactory ensheathing cells (OECs), remained unclear. To address this, we studied the intranasal infection of adult rats with BoDV-1 in vivo and in vitro, using olfactory mucosal (OM) cell cultures and the cultures of purified OECs. Strikingly, in vitro and in vivo, viral antigen and mRNA were present from four days post infection (dpi) onwards in the olfactory receptor neurons (ORNs), but also in all other cell types of the OM, and constantly in the OECs. In contrast, in vivo, BoDV-1 genomic RNA was only detectable in adult and juvenile ORNs, nerve fibers, and in OECs from 7 dpi on. In vitro, the rate of infection of OECs was significantly higher than that of the OM cells, pointing to a crucial role of OECs for infection via the olfactory pathway. Thus, this study provides important insights into the transmission of neurotropic viral infections with a zoonotic potential.http://www.mdpi.com/1422-0067/20/6/1318borna disease virusinitial phaseolfactory epitheliumolfactory ensheathing cellsOECsin vivoin vitro
spellingShingle Alexandra Kupke
Sabrina Becker
Konstantin Wewetzer
Barbara Ahlemeyer
Markus Eickmann
Christiane Herden
Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
International Journal of Molecular Sciences
borna disease virus
initial phase
olfactory epithelium
olfactory ensheathing cells
OECs
in vivo
in vitro
title Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
title_full Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
title_fullStr Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
title_full_unstemmed Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
title_short Intranasal Borna Disease Virus (BoDV-1) Infection: Insights into Initial Steps and Potential Contagiosity
title_sort intranasal borna disease virus bodv 1 infection insights into initial steps and potential contagiosity
topic borna disease virus
initial phase
olfactory epithelium
olfactory ensheathing cells
OECs
in vivo
in vitro
url http://www.mdpi.com/1422-0067/20/6/1318
work_keys_str_mv AT alexandrakupke intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity
AT sabrinabecker intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity
AT konstantinwewetzer intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity
AT barbaraahlemeyer intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity
AT markuseickmann intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity
AT christianeherden intranasalbornadiseasevirusbodv1infectioninsightsintoinitialstepsandpotentialcontagiosity