Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas.
BACKGROUND:Rift Valley fever virus (RVFV) is an arbovirus of the order Bunyavirales that causes severe disease in ruminants and humans. Outbreaks in sheep herds are characterised by newborn fatalities and abortion storms. The association of RVFV infections with abortions of ovines and other ruminant...
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ftdoajarticles:oai:doaj.org/article:76e9fa8139644b00a751a1d84676df93 2023-05-15T15:13:24+02:00 Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. Judith Oymans Paul J Wichgers Schreur Lucien van Keulen Jet Kant Jeroen Kortekaas 2020-01-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0007898 https://doaj.org/article/76e9fa8139644b00a751a1d84676df93 EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0007898 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0007898 https://doaj.org/article/76e9fa8139644b00a751a1d84676df93 PLoS Neglected Tropical Diseases, Vol 14, Iss 1, p e0007898 (2020) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2020 ftdoajarticles https://doi.org/10.1371/journal.pntd.0007898 2022-12-31T07:16:57Z BACKGROUND:Rift Valley fever virus (RVFV) is an arbovirus of the order Bunyavirales that causes severe disease in ruminants and humans. Outbreaks in sheep herds are characterised by newborn fatalities and abortion storms. The association of RVFV infections with abortions of ovines and other ruminants is well recognized, whereas the pathology resulting in abortion has remained undescribed. Accumulating evidence suggests that RVFV is abortogenic in humans as well, warranting more research on the interaction of RVFV with the ruminant and human placenta. METHODOLOGY/PRINCIPAL FINDINGS:Pregnant ewes were inoculated with a highly virulent strain of RVFV and necropsied at different days post infection. Tissues were collected and analysed by PCR, virus isolation, and immunohistochemistry. The results show that RVFV replicates efficiently in maternal placental epithelial cells before the virus infects foetal trophoblasts. Moreover, the virus was shown to bypass the maternal epithelial cell layer by directly targeting foetal trophoblasts in the haemophagous zone, a region of the ovine placenta where maternal blood is in direct contact with foetal cells. Abortion was associated with widespread necrosis of placental tissues accompanied with severe haemorrhages. Experiments with human placental explants revealed that the same virus strain replicates efficiently in both cyto- and syncytiotrophoblasts. CONCLUSIONS/SIGNIFICANCE:This study demonstrates that RVFV targets the foetal-maternal interface in both ovine and human placentas. The virus was shown to cross the ovine placental barrier via two distinct routes, ultimately resulting in placental and foetal demise followed by abortion. Our finding that RVFV replicates efficiently in human trophoblasts underscores the risk of RVFV infection for human pregnancy. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 14 1 e0007898 |
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Open Polar |
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Directory of Open Access Journals: DOAJ Articles |
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ftdoajarticles |
language |
English |
topic |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
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Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 Judith Oymans Paul J Wichgers Schreur Lucien van Keulen Jet Kant Jeroen Kortekaas Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
topic_facet |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
description |
BACKGROUND:Rift Valley fever virus (RVFV) is an arbovirus of the order Bunyavirales that causes severe disease in ruminants and humans. Outbreaks in sheep herds are characterised by newborn fatalities and abortion storms. The association of RVFV infections with abortions of ovines and other ruminants is well recognized, whereas the pathology resulting in abortion has remained undescribed. Accumulating evidence suggests that RVFV is abortogenic in humans as well, warranting more research on the interaction of RVFV with the ruminant and human placenta. METHODOLOGY/PRINCIPAL FINDINGS:Pregnant ewes were inoculated with a highly virulent strain of RVFV and necropsied at different days post infection. Tissues were collected and analysed by PCR, virus isolation, and immunohistochemistry. The results show that RVFV replicates efficiently in maternal placental epithelial cells before the virus infects foetal trophoblasts. Moreover, the virus was shown to bypass the maternal epithelial cell layer by directly targeting foetal trophoblasts in the haemophagous zone, a region of the ovine placenta where maternal blood is in direct contact with foetal cells. Abortion was associated with widespread necrosis of placental tissues accompanied with severe haemorrhages. Experiments with human placental explants revealed that the same virus strain replicates efficiently in both cyto- and syncytiotrophoblasts. CONCLUSIONS/SIGNIFICANCE:This study demonstrates that RVFV targets the foetal-maternal interface in both ovine and human placentas. The virus was shown to cross the ovine placental barrier via two distinct routes, ultimately resulting in placental and foetal demise followed by abortion. Our finding that RVFV replicates efficiently in human trophoblasts underscores the risk of RVFV infection for human pregnancy. |
format |
Article in Journal/Newspaper |
author |
Judith Oymans Paul J Wichgers Schreur Lucien van Keulen Jet Kant Jeroen Kortekaas |
author_facet |
Judith Oymans Paul J Wichgers Schreur Lucien van Keulen Jet Kant Jeroen Kortekaas |
author_sort |
Judith Oymans |
title |
Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
title_short |
Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
title_full |
Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
title_fullStr |
Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
title_full_unstemmed |
Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
title_sort |
rift valley fever virus targets the maternal-foetal interface in ovine and human placentas. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2020 |
url |
https://doi.org/10.1371/journal.pntd.0007898 https://doaj.org/article/76e9fa8139644b00a751a1d84676df93 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic |
genre_facet |
Arctic |
op_source |
PLoS Neglected Tropical Diseases, Vol 14, Iss 1, p e0007898 (2020) |
op_relation |
https://doi.org/10.1371/journal.pntd.0007898 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0007898 https://doaj.org/article/76e9fa8139644b00a751a1d84676df93 |
op_doi |
https://doi.org/10.1371/journal.pntd.0007898 |
container_title |
PLOS Neglected Tropical Diseases |
container_volume |
14 |
container_issue |
1 |
container_start_page |
e0007898 |
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