SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters
Abstract Coronavirus disease 2019 (COVID-19, caused by severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2)) is primarily a respiratory illness. However, various extrapulmonary manifestations have been reported in patients with severe forms of COVID-19. Notably, SARS-CoV-2 was shown to direc...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Nature Publishing Group
2023-02-01
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| Series: | Cell Death and Disease |
| Online Access: | https://doi.org/10.1038/s41419-023-05574-w |
| _version_ | 1828041445204819968 |
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| author | Gemma Bogard Johanna Barthelemy Aline Hantute-Ghesquier Valentin Sencio Patricia Brito-Rodrigues Karin Séron Cyril Robil Anne Flourens Florence Pinet Delphine Eberlé François Trottein Martine Duterque-Coquillaud Isabelle Wolowczuk |
| author_facet | Gemma Bogard Johanna Barthelemy Aline Hantute-Ghesquier Valentin Sencio Patricia Brito-Rodrigues Karin Séron Cyril Robil Anne Flourens Florence Pinet Delphine Eberlé François Trottein Martine Duterque-Coquillaud Isabelle Wolowczuk |
| author_sort | Gemma Bogard |
| collection | DOAJ |
| description | Abstract Coronavirus disease 2019 (COVID-19, caused by severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2)) is primarily a respiratory illness. However, various extrapulmonary manifestations have been reported in patients with severe forms of COVID-19. Notably, SARS-CoV-2 was shown to directly trigger white adipose tissue (WAT) dysfunction, which in turn drives insulin resistance, dyslipidemia, and other adverse outcomes in patients with COVID-19. Although advanced age is the greatest risk factor for COVID-19 severity, published data on the impact of SARS-CoV-2 infection on WAT in aged individuals are scarce. Here, we characterized the response of subcutaneous and visceral WAT depots to SARS-CoV-2 infection in young adult and aged golden hamsters. In both age groups, infection was associated with a decrease in adipocyte size in the two WAT depots; this effect was partly due to changes in tissue’s lipid metabolism and persisted for longer in aged hamsters than in young-adult hamsters. In contrast, only the subcutaneous WAT depot contained crown-like structures (CLSs) in which dead adipocytes were surrounded by SARS-CoV-2-infected macrophages, some of them forming syncytial multinucleated cells. Importantly, older age predisposed to a unique manifestation of viral disease in the subcutaneous WAT depot during SARS-CoV-2 infection; the persistence of very large CLSs was indicative of an age-associated defect in the clearance of dead adipocytes by macrophages. Moreover, we uncovered age-related differences in plasma lipid profiles during SARS-CoV-2 infection. These data suggest that the WAT’s abnormal response to SARS-CoV-2 infection may contribute to the greater severity of COVID-19 observed in elderly patients. |
| first_indexed | 2024-04-10T17:16:17Z |
| format | Article |
| id | doaj.art-8031905ea98f468dbf1ce46702705206 |
| institution | Directory Open Access Journal |
| issn | 2041-4889 |
| language | English |
| last_indexed | 2024-04-10T17:16:17Z |
| publishDate | 2023-02-01 |
| publisher | Nature Publishing Group |
| record_format | Article |
| series | Cell Death and Disease |
| spelling | doaj.art-8031905ea98f468dbf1ce467027052062023-02-05T12:25:30ZengNature Publishing GroupCell Death and Disease2041-48892023-02-0114211610.1038/s41419-023-05574-wSARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamstersGemma Bogard0Johanna Barthelemy1Aline Hantute-Ghesquier2Valentin Sencio3Patricia Brito-Rodrigues4Karin Séron5Cyril Robil6Anne Flourens7Florence Pinet8Delphine Eberlé9François Trottein10Martine Duterque-Coquillaud11Isabelle Wolowczuk12Univ. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, UMR9020–U1277–CANTHER–Cancer Heterogeneity Plasticity and Resistance to TherapiesUniv. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, UMR9020–U1277–CANTHER–Cancer Heterogeneity Plasticity and Resistance to TherapiesUniv. Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167–RID-AGE–Facteurs de risque et déterminants moléculaires des maladies liées au vieillissementUniv. Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1011–EGIDUniv. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, UMR9020–U1277–CANTHER–Cancer Heterogeneity Plasticity and Resistance to TherapiesUniv. Lille, Institut National de la Santé et de la Recherche Médicale (Inserm), Centre National de la Recherche Scientifique (CNRS), Centre Hospitalier Universitaire de Lille (CHU Lille), Institut Pasteur de Lille, U1019–UMR9017—Center for Infection and Immunity of Lille (CIIL)Abstract Coronavirus disease 2019 (COVID-19, caused by severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2)) is primarily a respiratory illness. However, various extrapulmonary manifestations have been reported in patients with severe forms of COVID-19. Notably, SARS-CoV-2 was shown to directly trigger white adipose tissue (WAT) dysfunction, which in turn drives insulin resistance, dyslipidemia, and other adverse outcomes in patients with COVID-19. Although advanced age is the greatest risk factor for COVID-19 severity, published data on the impact of SARS-CoV-2 infection on WAT in aged individuals are scarce. Here, we characterized the response of subcutaneous and visceral WAT depots to SARS-CoV-2 infection in young adult and aged golden hamsters. In both age groups, infection was associated with a decrease in adipocyte size in the two WAT depots; this effect was partly due to changes in tissue’s lipid metabolism and persisted for longer in aged hamsters than in young-adult hamsters. In contrast, only the subcutaneous WAT depot contained crown-like structures (CLSs) in which dead adipocytes were surrounded by SARS-CoV-2-infected macrophages, some of them forming syncytial multinucleated cells. Importantly, older age predisposed to a unique manifestation of viral disease in the subcutaneous WAT depot during SARS-CoV-2 infection; the persistence of very large CLSs was indicative of an age-associated defect in the clearance of dead adipocytes by macrophages. Moreover, we uncovered age-related differences in plasma lipid profiles during SARS-CoV-2 infection. These data suggest that the WAT’s abnormal response to SARS-CoV-2 infection may contribute to the greater severity of COVID-19 observed in elderly patients.https://doi.org/10.1038/s41419-023-05574-w |
| spellingShingle | Gemma Bogard Johanna Barthelemy Aline Hantute-Ghesquier Valentin Sencio Patricia Brito-Rodrigues Karin Séron Cyril Robil Anne Flourens Florence Pinet Delphine Eberlé François Trottein Martine Duterque-Coquillaud Isabelle Wolowczuk SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters Cell Death and Disease |
| title | SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters |
| title_full | SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters |
| title_fullStr | SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters |
| title_full_unstemmed | SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters |
| title_short | SARS-CoV-2 infection induces persistent adipose tissue damage in aged golden Syrian hamsters |
| title_sort | sars cov 2 infection induces persistent adipose tissue damage in aged golden syrian hamsters |
| url | https://doi.org/10.1038/s41419-023-05574-w |
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