Brain exposure to SARS-CoV-2 virions perturbs synaptic homeostasis
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is associated with short- and long-term neurological complications. The variety of symptoms makes it difficult to unravel molecular mechanisms underlying neurological sequalae after coronavirus disease 2019 (COVID-19). Here we sh...
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| Veröffentlicht in: | Nature microbiology 2024-05, Vol.9 (5), p.1189-1206 |
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| creator | Partiot, Emma Hirschler, Aurélie Colomb, Sophie Lutz, Willy Claeys, Tine Delalande, François Deffieu, Maika S. Bare, Yonis Roels, Judith R. E. Gorda, Barbara Bons, Joanna Callon, Domitille Andreoletti, Laurent Labrousse, Marc Jacobs, Frank M. J. Rigau, Valérie Charlot, Benoit Martens, Lennart Carapito, Christine Ganesh, Gowrishankar Gaudin, Raphael |
| description | Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is associated with short- and long-term neurological complications. The variety of symptoms makes it difficult to unravel molecular mechanisms underlying neurological sequalae after coronavirus disease 2019 (COVID-19). Here we show that SARS-CoV-2 triggers the up-regulation of synaptic components and perturbs local electrical field potential. Using cerebral organoids, organotypic culture of human brain explants from individuals without COVID-19 and post-mortem brain samples from individuals with COVID-19, we find that neural cells are permissive to SARS-CoV-2 to a low extent. SARS-CoV-2 induces aberrant presynaptic morphology and increases expression of the synaptic components Bassoon, latrophilin-3 (LPHN3) and fibronectin leucine-rich transmembrane protein-3 (FLRT3). Furthermore, we find that LPHN3-agonist treatment with Stachel partially restored organoid electrical activity and reverted SARS-CoV-2-induced aberrant presynaptic morphology. Finally, we observe accumulation of relatively static virions at LPHN3–FLRT3 synapses, suggesting that local hindrance can contribute to synaptic perturbations. Together, our study provides molecular insights into SARS-CoV-2–brain interactions, which may contribute to COVID-19-related neurological disorders.
Exposing cerebral organoids and post-mortem brain explants to SARS-CoV-2 virus particles alters expression of synaptic proteins and potentially affects synaptic function by blocking LPHN3 and FLRT3 synapses. |
| doi_str_mv | 10.1038/s41564-024-01657-2 |
| format | Article |
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E.</creatorcontrib><creatorcontrib>Gorda, Barbara</creatorcontrib><creatorcontrib>Bons, Joanna</creatorcontrib><creatorcontrib>Callon, Domitille</creatorcontrib><creatorcontrib>Andreoletti, Laurent</creatorcontrib><creatorcontrib>Labrousse, Marc</creatorcontrib><creatorcontrib>Jacobs, Frank M. J.</creatorcontrib><creatorcontrib>Rigau, Valérie</creatorcontrib><creatorcontrib>Charlot, Benoit</creatorcontrib><creatorcontrib>Martens, Lennart</creatorcontrib><creatorcontrib>Carapito, Christine</creatorcontrib><creatorcontrib>Ganesh, Gowrishankar</creatorcontrib><creatorcontrib>Gaudin, Raphael</creatorcontrib><title>Brain exposure to SARS-CoV-2 virions perturbs synaptic homeostasis</title><title>Nature microbiology</title><addtitle>Nat Microbiol</addtitle><addtitle>Nat Microbiol</addtitle><description>Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is associated with short- and long-term neurological complications. The variety of symptoms makes it difficult to unravel molecular mechanisms underlying neurological sequalae after coronavirus disease 2019 (COVID-19). Here we show that SARS-CoV-2 triggers the up-regulation of synaptic components and perturbs local electrical field potential. Using cerebral organoids, organotypic culture of human brain explants from individuals without COVID-19 and post-mortem brain samples from individuals with COVID-19, we find that neural cells are permissive to SARS-CoV-2 to a low extent. SARS-CoV-2 induces aberrant presynaptic morphology and increases expression of the synaptic components Bassoon, latrophilin-3 (LPHN3) and fibronectin leucine-rich transmembrane protein-3 (FLRT3). Furthermore, we find that LPHN3-agonist treatment with Stachel partially restored organoid electrical activity and reverted SARS-CoV-2-induced aberrant presynaptic morphology. Finally, we observe accumulation of relatively static virions at LPHN3–FLRT3 synapses, suggesting that local hindrance can contribute to synaptic perturbations. Together, our study provides molecular insights into SARS-CoV-2–brain interactions, which may contribute to COVID-19-related neurological disorders.
Exposing cerebral organoids and post-mortem brain explants to SARS-CoV-2 virus particles alters expression of synaptic proteins and potentially affects synaptic function by blocking LPHN3 and FLRT3 synapses.</description><subject>13</subject><subject>13/106</subject><subject>14/63</subject><subject>631/326/596/2557</subject><subject>631/80/304</subject><subject>Bassoon protein</subject><subject>Biomedical and Life Sciences</subject><subject>Cell culture</subject><subject>Cellular Biology</subject><subject>Cognitive science</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>Explants</subject><subject>Fibronectin</subject><subject>Homeostasis</subject><subject>Infectious Diseases</subject><subject>Life Sciences</subject><subject>Medical Microbiology</subject><subject>Microbiology</subject><subject>Microbiology and Parasitology</subject><subject>Molecular modelling</subject><subject>Morphology</subject><subject>Neurological complications</subject><subject>Neurological diseases</subject><subject>Neuroscience</subject><subject>Organoids</subject><subject>Parasitology</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Virions</subject><subject>Virology</subject><issn>2058-5276</issn><issn>2058-5276</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kUtLxDAUhYMoKuofcCEFN7qopjfPLsfBFwwIjroNmTbVykxTc1vRf2_Gjg9cuAgJud89OTeHkP2MnmSU6VPkmZA8pRBXJoVKYY1sAxU6FaDk-q_zFtlDfKY0YiCllptki2nBdQ5sm5ydBVs3iXtrPfbBJZ1PpqPbaTr2Dykkr3WofYNJ60LXhxkm-N7YtquL5MkvnMfOYo27ZKOyc3R7q32H3F-c342v0snN5fV4NEkLTvMuVa4oo1EKikbjDnhVUlbqTAmXC6ZnilprS23LqiyAU57bXMwqKXOueOZUxnbI8aD7ZOemDfXChnfjbW2uRhOzvKNcMMiFfl2yRwPbBv_SO-zMosbCzee2cb5HwyiAkEprHdHDP-iz70MTJ4mUYEwCwFIQBqoIHjG46ttBRs0yEDMEYmIg5jMQA7HpYCXdzxau_G75-v4IsAHAWGoeXfh5-x_ZDwBskr8</recordid><startdate>20240501</startdate><enddate>20240501</enddate><creator>Partiot, Emma</creator><creator>Hirschler, Aurélie</creator><creator>Colomb, Sophie</creator><creator>Lutz, Willy</creator><creator>Claeys, Tine</creator><creator>Delalande, François</creator><creator>Deffieu, Maika S.</creator><creator>Bare, Yonis</creator><creator>Roels, Judith R. 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The variety of symptoms makes it difficult to unravel molecular mechanisms underlying neurological sequalae after coronavirus disease 2019 (COVID-19). Here we show that SARS-CoV-2 triggers the up-regulation of synaptic components and perturbs local electrical field potential. Using cerebral organoids, organotypic culture of human brain explants from individuals without COVID-19 and post-mortem brain samples from individuals with COVID-19, we find that neural cells are permissive to SARS-CoV-2 to a low extent. SARS-CoV-2 induces aberrant presynaptic morphology and increases expression of the synaptic components Bassoon, latrophilin-3 (LPHN3) and fibronectin leucine-rich transmembrane protein-3 (FLRT3). Furthermore, we find that LPHN3-agonist treatment with Stachel partially restored organoid electrical activity and reverted SARS-CoV-2-induced aberrant presynaptic morphology. Finally, we observe accumulation of relatively static virions at LPHN3–FLRT3 synapses, suggesting that local hindrance can contribute to synaptic perturbations. Together, our study provides molecular insights into SARS-CoV-2–brain interactions, which may contribute to COVID-19-related neurological disorders.
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| identifier | ISSN: 2058-5276 |
| ispartof | Nature microbiology, 2024-05, Vol.9 (5), p.1189-1206 |
| issn | 2058-5276 2058-5276 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_04532958v1 |
| source | SpringerLink Journals; Nature Journals Online |
| subjects | 13 13/106 14/63 631/326/596/2557 631/80/304 Bassoon protein Biomedical and Life Sciences Cell culture Cellular Biology Cognitive science Coronaviruses COVID-19 Explants Fibronectin Homeostasis Infectious Diseases Life Sciences Medical Microbiology Microbiology Microbiology and Parasitology Molecular modelling Morphology Neurological complications Neurological diseases Neuroscience Organoids Parasitology Severe acute respiratory syndrome coronavirus 2 Virions Virology |
| title | Brain exposure to SARS-CoV-2 virions perturbs synaptic homeostasis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-16T09%3A16%3A57IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Brain%20exposure%20to%20SARS-CoV-2%20virions%20perturbs%20synaptic%20homeostasis&rft.jtitle=Nature%20microbiology&rft.au=Partiot,%20Emma&rft.date=2024-05-01&rft.volume=9&rft.issue=5&rft.spage=1189&rft.epage=1206&rft.pages=1189-1206&rft.issn=2058-5276&rft.eissn=2058-5276&rft_id=info:doi/10.1038/s41564-024-01657-2&rft_dat=%3Cproquest_hal_p%3E3053362221%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3053362221&rft_id=info:pmid/38548923&rfr_iscdi=true |