_version_ 1783582234490437632
author Song, Eric
Zhang, Ce
Israelow, Benjamin
Lu-Culligan, Alice
Prado, Alba Vieites
Skriabine, Sophie
Lu, Peiwen
Weizman, Orr-El
Liu, Feimei
Dai, Yile
Szigeti-Buck, Klara
Yasumoto, Yuki
Wang, Guilin
Castaldi, Christopher
Heltke, Jaime
Ng, Evelyn
Wheeler, John
Alfajaro, Mia Madel
Levavasseur, Etienne
Fontes, Benjamin
Ravindra, Neal G.
Van Dijk, David
Mane, Shrikant
Gunel, Murat
Ring, Aaron
Kazmi, Syed A. Jaffar
Zhang, Kai
Wilen, Craig B
Horvath, Tamas L.
Plu, Isabelle
Haik, Stephane
Thomas, Jean-Leon
Louvi, Angeliki
Farhadian, Shelli F.
Huttner, Anita
Seilhean, Danielle
Renier, Nicolas
Bilguvar, Kaya
Iwasaki, Akiko
author_facet Song, Eric
Zhang, Ce
Israelow, Benjamin
Lu-Culligan, Alice
Prado, Alba Vieites
Skriabine, Sophie
Lu, Peiwen
Weizman, Orr-El
Liu, Feimei
Dai, Yile
Szigeti-Buck, Klara
Yasumoto, Yuki
Wang, Guilin
Castaldi, Christopher
Heltke, Jaime
Ng, Evelyn
Wheeler, John
Alfajaro, Mia Madel
Levavasseur, Etienne
Fontes, Benjamin
Ravindra, Neal G.
Van Dijk, David
Mane, Shrikant
Gunel, Murat
Ring, Aaron
Kazmi, Syed A. Jaffar
Zhang, Kai
Wilen, Craig B
Horvath, Tamas L.
Plu, Isabelle
Haik, Stephane
Thomas, Jean-Leon
Louvi, Angeliki
Farhadian, Shelli F.
Huttner, Anita
Seilhean, Danielle
Renier, Nicolas
Bilguvar, Kaya
Iwasaki, Akiko
author_sort Song, Eric
collection PubMed
description Although COVID-19 is considered to be primarily a respiratory disease, SARS-CoV-2 affects multiple organ systems including the central nervous system (CNS). Yet, there is no consensus whether the virus can infect the brain, or what the consequences of CNS infection are. Here, we used three independent approaches to probe the capacity of SARS-CoV-2 to infect the brain. First, using human brain organoids, we observed clear evidence of infection with accompanying metabolic changes in the infected and neighboring neurons. However, no evidence for the type I interferon responses was detected. We demonstrate that neuronal infection can be prevented either by blocking ACE2 with antibodies or by administering cerebrospinal fluid from a COVID-19 patient. Second, using mice overexpressing human ACE2, we demonstrate in vivo that SARS-CoV-2 neuroinvasion, but not respiratory infection, is associated with mortality. Finally, in brain autopsy from patients who died of COVID-19, we detect SARS-CoV-2 in the cortical neurons, and note pathologic features associated with infection with minimal immune cell infiltrates. These results provide evidence for the neuroinvasive capacity of SARS-CoV2, and an unexpected consequence of direct infection of neurons by SARS-CoV-2.
format Online
Article
Text
id pubmed-7491522
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-74915222020-09-16 Neuroinvasion of SARS-CoV-2 in human and mouse brain Song, Eric Zhang, Ce Israelow, Benjamin Lu-Culligan, Alice Prado, Alba Vieites Skriabine, Sophie Lu, Peiwen Weizman, Orr-El Liu, Feimei Dai, Yile Szigeti-Buck, Klara Yasumoto, Yuki Wang, Guilin Castaldi, Christopher Heltke, Jaime Ng, Evelyn Wheeler, John Alfajaro, Mia Madel Levavasseur, Etienne Fontes, Benjamin Ravindra, Neal G. Van Dijk, David Mane, Shrikant Gunel, Murat Ring, Aaron Kazmi, Syed A. Jaffar Zhang, Kai Wilen, Craig B Horvath, Tamas L. Plu, Isabelle Haik, Stephane Thomas, Jean-Leon Louvi, Angeliki Farhadian, Shelli F. Huttner, Anita Seilhean, Danielle Renier, Nicolas Bilguvar, Kaya Iwasaki, Akiko bioRxiv Article Although COVID-19 is considered to be primarily a respiratory disease, SARS-CoV-2 affects multiple organ systems including the central nervous system (CNS). Yet, there is no consensus whether the virus can infect the brain, or what the consequences of CNS infection are. Here, we used three independent approaches to probe the capacity of SARS-CoV-2 to infect the brain. First, using human brain organoids, we observed clear evidence of infection with accompanying metabolic changes in the infected and neighboring neurons. However, no evidence for the type I interferon responses was detected. We demonstrate that neuronal infection can be prevented either by blocking ACE2 with antibodies or by administering cerebrospinal fluid from a COVID-19 patient. Second, using mice overexpressing human ACE2, we demonstrate in vivo that SARS-CoV-2 neuroinvasion, but not respiratory infection, is associated with mortality. Finally, in brain autopsy from patients who died of COVID-19, we detect SARS-CoV-2 in the cortical neurons, and note pathologic features associated with infection with minimal immune cell infiltrates. These results provide evidence for the neuroinvasive capacity of SARS-CoV2, and an unexpected consequence of direct infection of neurons by SARS-CoV-2. Cold Spring Harbor Laboratory 2020-09-08 /pmc/articles/PMC7491522/ /pubmed/32935108 http://dx.doi.org/10.1101/2020.06.25.169946 Text en http://creativecommons.org/licenses/by-nc-nd/4.0/It is made available under a CC-BY-NC-ND 4.0 International license (http://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Article
Song, Eric
Zhang, Ce
Israelow, Benjamin
Lu-Culligan, Alice
Prado, Alba Vieites
Skriabine, Sophie
Lu, Peiwen
Weizman, Orr-El
Liu, Feimei
Dai, Yile
Szigeti-Buck, Klara
Yasumoto, Yuki
Wang, Guilin
Castaldi, Christopher
Heltke, Jaime
Ng, Evelyn
Wheeler, John
Alfajaro, Mia Madel
Levavasseur, Etienne
Fontes, Benjamin
Ravindra, Neal G.
Van Dijk, David
Mane, Shrikant
Gunel, Murat
Ring, Aaron
Kazmi, Syed A. Jaffar
Zhang, Kai
Wilen, Craig B
Horvath, Tamas L.
Plu, Isabelle
Haik, Stephane
Thomas, Jean-Leon
Louvi, Angeliki
Farhadian, Shelli F.
Huttner, Anita
Seilhean, Danielle
Renier, Nicolas
Bilguvar, Kaya
Iwasaki, Akiko
Neuroinvasion of SARS-CoV-2 in human and mouse brain
title Neuroinvasion of SARS-CoV-2 in human and mouse brain
title_full Neuroinvasion of SARS-CoV-2 in human and mouse brain
title_fullStr Neuroinvasion of SARS-CoV-2 in human and mouse brain
title_full_unstemmed Neuroinvasion of SARS-CoV-2 in human and mouse brain
title_short Neuroinvasion of SARS-CoV-2 in human and mouse brain
title_sort neuroinvasion of sars-cov-2 in human and mouse brain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7491522/
https://www.ncbi.nlm.nih.gov/pubmed/32935108
http://dx.doi.org/10.1101/2020.06.25.169946
work_keys_str_mv AT songeric neuroinvasionofsarscov2inhumanandmousebrain
AT zhangce neuroinvasionofsarscov2inhumanandmousebrain
AT israelowbenjamin neuroinvasionofsarscov2inhumanandmousebrain
AT luculliganalice neuroinvasionofsarscov2inhumanandmousebrain
AT pradoalbavieites neuroinvasionofsarscov2inhumanandmousebrain
AT skriabinesophie neuroinvasionofsarscov2inhumanandmousebrain
AT lupeiwen neuroinvasionofsarscov2inhumanandmousebrain
AT weizmanorrel neuroinvasionofsarscov2inhumanandmousebrain
AT liufeimei neuroinvasionofsarscov2inhumanandmousebrain
AT daiyile neuroinvasionofsarscov2inhumanandmousebrain
AT szigetibuckklara neuroinvasionofsarscov2inhumanandmousebrain
AT yasumotoyuki neuroinvasionofsarscov2inhumanandmousebrain
AT wangguilin neuroinvasionofsarscov2inhumanandmousebrain
AT castaldichristopher neuroinvasionofsarscov2inhumanandmousebrain
AT heltkejaime neuroinvasionofsarscov2inhumanandmousebrain
AT ngevelyn neuroinvasionofsarscov2inhumanandmousebrain
AT wheelerjohn neuroinvasionofsarscov2inhumanandmousebrain
AT alfajaromiamadel neuroinvasionofsarscov2inhumanandmousebrain
AT levavasseuretienne neuroinvasionofsarscov2inhumanandmousebrain
AT fontesbenjamin neuroinvasionofsarscov2inhumanandmousebrain
AT ravindranealg neuroinvasionofsarscov2inhumanandmousebrain
AT vandijkdavid neuroinvasionofsarscov2inhumanandmousebrain
AT maneshrikant neuroinvasionofsarscov2inhumanandmousebrain
AT gunelmurat neuroinvasionofsarscov2inhumanandmousebrain
AT ringaaron neuroinvasionofsarscov2inhumanandmousebrain
AT kazmisyedajaffar neuroinvasionofsarscov2inhumanandmousebrain
AT zhangkai neuroinvasionofsarscov2inhumanandmousebrain
AT wilencraigb neuroinvasionofsarscov2inhumanandmousebrain
AT horvathtamasl neuroinvasionofsarscov2inhumanandmousebrain
AT pluisabelle neuroinvasionofsarscov2inhumanandmousebrain
AT haikstephane neuroinvasionofsarscov2inhumanandmousebrain
AT thomasjeanleon neuroinvasionofsarscov2inhumanandmousebrain
AT louviangeliki neuroinvasionofsarscov2inhumanandmousebrain
AT farhadianshellif neuroinvasionofsarscov2inhumanandmousebrain
AT huttneranita neuroinvasionofsarscov2inhumanandmousebrain
AT seilheandanielle neuroinvasionofsarscov2inhumanandmousebrain
AT reniernicolas neuroinvasionofsarscov2inhumanandmousebrain
AT bilguvarkaya neuroinvasionofsarscov2inhumanandmousebrain
AT iwasakiakiko neuroinvasionofsarscov2inhumanandmousebrain