Neuroinvasion of SARS-CoV-2 in human and mouse brain

Нейроинвазия SARS-CoV-2 в головной мозг человека и мыши
David van Dijk, Shelli Farhadian, Alice Lu-Culligan, Yuki Yasumoto, Feimei Liu, Klara Szigeti‐Buck, Aaron M. Ring, Tamás L. Horváth, Akiko Iwasaki, Eric Song, Orr-El Weizman, Craig B. Wilen, Shrikant Mane, Peiwen Lu, Nicolas Renier, Kaya Bilgüvar, Murat Günel, Neal G. Ravindra, Stéphane Haı̈k, Anita Hüttner, Jean‐Léon Thomas, Danielle Seilhean, Mia Madel Alfajaro, Etienne Levavasseur, Isabelle Plu, Benjamin Israelow, Alba Vieites‐Prado, Ce Zhang, Sophie Skriabine, Yile Dai, Guilin Wang, Christopher Castaldi, Jaime Heltke, Evelyn Ng, John F. Wheeler, Benjamin Fontes, Syed A. Jaffar Kazmi, Kai Zhang, Angeliki Louvi
2020-12-11

ACE2 receptorSARS-CoV-2 neuroinvasioncortical neuronshuman brain organoidsneuronal infection
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 on the consequences of CNS infections. 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 infected and neighboring neurons. However, no evidence for type I interferon responses was detected. We demonstrate that neuronal infection can be prevented by blocking ACE2 with antibodies or by administering cerebrospinal fluid from a COVID-19 patient. Second, using mice overexpressing human ACE2, we demonstrate SARS-CoV-2 neuroinvasion in vivo. Finally, in autopsies from patients who died of COVID-19, we detect SARS-CoV-2 in cortical neurons and note pathological features associated with infection with minimal immune cell infiltrates. These results provide evidence for the neuroinvasive capacity of SARS-CoV-2 and an unexpected consequence of direct infection of neurons by SARS-CoV-2.
1
Autopsy samples from patients who died of COVID-19 reveal SARS-CoV-2 in cortical neurons and infection-associated pathology with minimal immune-cell infiltration.
2
Blocking ACE2 with antibodies or administering cerebrospinal fluid from a COVID-19 patient prevents neuronal infection in brain organoids.
3
Mice overexpressing human ACE2 develop SARS-CoV-2 neuroinvasion in vivo.
4
SARS-CoV-2 infects human brain organoids, causing metabolic changes in infected and neighboring neurons without detectable type I interferon responses.
5
The findings establish SARS-CoV-2 neuroinvasive capacity and indicate direct neuronal infection as a potentially important consequence of infection.

SARS-CoV-2 infection of the human and mouse central nervous system, including brain organoids, hACE2-expressing mice, and cortical neurons from COVID-19 autopsies

The neuroinvasive capacity and neuronal consequences of SARS-CoV-2 infection, including neuronal metabolic changes, type I interferon responses, pathological features, and antibody/CSF-mediated prevention of infection

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Publication Date
2020-12-11
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Authors
David van Dijk
Shelli Farhadian
Alice Lu-Culligan
Yuki Yasumoto
Feimei Liu
Klara Szigeti‐Buck
Aaron M. Ring
Tamás L. Horváth
Akiko Iwasaki
Eric Song
Orr-El Weizman
Craig B. Wilen
Shrikant Mane
Peiwen Lu
Nicolas Renier
Kaya Bilgüvar
Murat Günel
Neal G. Ravindra
Stéphane Haı̈k
Anita Hüttner
Jean‐Léon Thomas
Danielle Seilhean
Mia Madel Alfajaro
Etienne Levavasseur
Isabelle Plu
Benjamin Israelow
Alba Vieites‐Prado
Ce Zhang
Sophie Skriabine
Yile Dai
Guilin Wang
Christopher Castaldi
Jaime Heltke
Evelyn Ng
John F. Wheeler
Benjamin Fontes
Syed A. Jaffar Kazmi
Kai Zhang
Angeliki Louvi
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