Neuroinvasion and anosmia are independent phenomena upon infection with SARS-CoV-2 and its variants

Guilherme Dias de Melo, Victoire Perraud, Flavio Alvarez, Alba Vieites-Prado, Seonhee Kim, Lauriane Kergoat, Anthony Coleon, Bettina Salome Trüeb, Magali Tichit, Aurèle Piazza, Agnès Thierry, David Hardy, Nicolas Wolff, Sandie Munier, Romain Koszul, Etienne Simon-Lorière, Volker Thiel, Marc Lecuit, Pierre-Marie Lledo, Nicolas Renier, Florence Larrous and Hervé Bourhy ()
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Guilherme Dias de Melo: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Victoire Perraud: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Flavio Alvarez: Université Paris Cité, Channel Receptors Unit
Alba Vieites-Prado: , Sorbonne Université, INSERM U1127
Seonhee Kim: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Lauriane Kergoat: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Anthony Coleon: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Bettina Salome Trüeb: University of Bern
Magali Tichit: Université Paris Cité, Histopathology Platform
Aurèle Piazza: Université Paris Cité, Spatial Regulation of Genomes Laboratory
Agnès Thierry: Université Paris Cité, Spatial Regulation of Genomes Laboratory
David Hardy: Université Paris Cité, Histopathology Platform
Nicolas Wolff: Université Paris Cité, Channel Receptors Unit
Sandie Munier: Université Paris Cité, Molecular Genetics of RNA viruses Unit
Romain Koszul: Université Paris Cité, Spatial Regulation of Genomes Laboratory
Etienne Simon-Lorière: Université Paris Cité, Evolutionary Genomics of RNA Viruses Group
Volker Thiel: University of Bern
Marc Lecuit: Université Paris Cité, Inserm U1117, Biology of Infection Unit
Pierre-Marie Lledo: Perception and Memory Unit, F-75015 Paris
Nicolas Renier: , Sorbonne Université, INSERM U1127
Florence Larrous: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit
Hervé Bourhy: Université Paris Cité, Lyssavirus Epidemiology and Neuropathology Unit

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract Anosmia was identified as a hallmark of COVID-19 early in the pandemic, however, with the emergence of variants of concern, the clinical profile induced by SARS-CoV-2 infection has changed, with anosmia being less frequent. Here, we assessed the clinical, olfactory and neuroinflammatory conditions of golden hamsters infected with the original Wuhan SARS-CoV-2 strain, its isogenic ORF7-deletion mutant and three variants: Gamma, Delta, and Omicron/BA.1. We show that infected animals develop a variant-dependent clinical disease including anosmia, and that the ORF7 of SARS-CoV-2 contributes to the induction of olfactory dysfunction. Conversely, all SARS-CoV-2 variants are neuroinvasive, regardless of the clinical presentation they induce. Taken together, this confirms that neuroinvasion and anosmia are independent phenomena upon SARS-CoV-2 infection. Using newly generated nanoluciferase-expressing SARS-CoV-2, we validate the olfactory pathway as a major entry point into the brain in vivo and demonstrate in vitro that SARS-CoV-2 travels retrogradely and anterogradely along axons in microfluidic neuron-epithelial networks.

Date: 2023
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DOI: 10.1038/s41467-023-40228-7

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