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The SARS-CoV-2 spike (S) and the orthoreovirus p15 cause neuronal and glial fusion

Ramon Martinez-Marmol, Rosina Giordano-Santini, Eva Kaulich, Ann-Na Cho, Md Asrafuzzaman Riyadh, Emilija Robinson, Giuseppe Balistreri, Frédéric A. Meunier, Yazi D. Ke, Lars M. Ittner, Massimo A. Hilliard
doi: https://doi.org/10.1101/2021.09.01.458544
Ramon Martinez-Marmol
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Rosina Giordano-Santini
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Eva Kaulich
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Ann-Na Cho
4Dementia Research Centre, Department of Biomedical Sciences, Faculty of Medicine Health and Human Sciences, Macquarie University, Sydney, Australia
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Md Asrafuzzaman Riyadh
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Emilija Robinson
4Dementia Research Centre, Department of Biomedical Sciences, Faculty of Medicine Health and Human Sciences, Macquarie University, Sydney, Australia
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Giuseppe Balistreri
2Faculty of Biological and Environmental Sciences, Molecular and Integrative Biosciences Research Program, University of Helsinki, Helsinki, Finland
3Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Frédéric A. Meunier
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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Yazi D. Ke
4Dementia Research Centre, Department of Biomedical Sciences, Faculty of Medicine Health and Human Sciences, Macquarie University, Sydney, Australia
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Lars M. Ittner
4Dementia Research Centre, Department of Biomedical Sciences, Faculty of Medicine Health and Human Sciences, Macquarie University, Sydney, Australia
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Massimo A. Hilliard
1Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
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  • For correspondence: m.hilliard@uq.edu.au
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Abstract

Numerous enveloped viruses use specialized surface molecules called fusogens to enter host cells1. During virus replication, these fusogens decorate the host cells membrane enabling them the ability to fuse with neighboring cells, forming syncytia that the viruses use to propagate while evading the immune system. Many of these viruses, including the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), infect the brain and may cause serious neurological symptoms through mechanisms which remain poorly understood2–4. Here we show that expression of either the SARS-CoV-2 spike (S) protein or p15 protein from the baboon orthoreovirus is sufficient to induce fusion between interconnected neurons, as well as between neurons and glial cells. This phenomenon is observed across species, from nematodes to mammals, including human embryonic stem cells-derived neurons and brain organoids. We show that fusion events are progressive, can occur between distant neurites, and lead to the formation of multicellular syncytia. Finally, we reveal that in addition to intracellular molecules, fusion events allow diffusion and movement of large organelles such as mitochondria between fused neurons. Our results provide important mechanistic insights into how SARS-CoV-2 and other viruses could affect the nervous system circuitries causing neurological symptoms.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 01, 2021.
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The SARS-CoV-2 spike (S) and the orthoreovirus p15 cause neuronal and glial fusion
Ramon Martinez-Marmol, Rosina Giordano-Santini, Eva Kaulich, Ann-Na Cho, Md Asrafuzzaman Riyadh, Emilija Robinson, Giuseppe Balistreri, Frédéric A. Meunier, Yazi D. Ke, Lars M. Ittner, Massimo A. Hilliard
bioRxiv 2021.09.01.458544; doi: https://doi.org/10.1101/2021.09.01.458544
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The SARS-CoV-2 spike (S) and the orthoreovirus p15 cause neuronal and glial fusion
Ramon Martinez-Marmol, Rosina Giordano-Santini, Eva Kaulich, Ann-Na Cho, Md Asrafuzzaman Riyadh, Emilija Robinson, Giuseppe Balistreri, Frédéric A. Meunier, Yazi D. Ke, Lars M. Ittner, Massimo A. Hilliard
bioRxiv 2021.09.01.458544; doi: https://doi.org/10.1101/2021.09.01.458544

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