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SARS-CoV-2 infects human adipose tissue and elicits an inflammatory response consistent with severe COVID-19

Giovanny J. Martínez-Colón, Kalani Ratnasiri, Heping Chen, Sizun Jiang, Elizabeth Zanley, View ORCID ProfileArjun Rustagi, Renu Verma, Han Chen, Jason R. Andrews, Kirsten D. Mertz, View ORCID ProfileAlexandar Tzankov, Dan Azagury, Jack Boyd, Garry P. Nolan, Christian M. Schürch, Matthias S. Matter, View ORCID ProfileCatherine A. Blish, Tracey L. McLaughlin
doi: https://doi.org/10.1101/2021.10.24.465626
Giovanny J. Martínez-Colón
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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Kalani Ratnasiri
2Program in Immunology, Stanford University School of Medicine, Stanford, CA, USA
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Heping Chen
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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Sizun Jiang
5Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA
9Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA
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Elizabeth Zanley
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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Arjun Rustagi
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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  • ORCID record for Arjun Rustagi
Renu Verma
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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Han Chen
5Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA
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Jason R. Andrews
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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Kirsten D. Mertz
10Institute of Pathology, Cantonal Hospital Baselland, Liestal, Switzerland
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Alexandar Tzankov
8Institute of Medical Genetics and Pathology, University Hospital of Basel, University of Basel, Basel, Switzerland
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Dan Azagury
3Department of Surgery, Stanford University School of Medicine, Stanford, CA, USA
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Jack Boyd
4Department of Cardiothoracic Surgery, Stanford University School of Medicine, Stanford, CA, USA
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Garry P. Nolan
5Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA
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Christian M. Schürch
7Department of Pathology and Neuropathology, University Hospital and Comprehensive Cancer Center Tübingen, Tübingen, Germany
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Matthias S. Matter
8Institute of Medical Genetics and Pathology, University Hospital of Basel, University of Basel, Basel, Switzerland
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Catherine A. Blish
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
2Program in Immunology, Stanford University School of Medicine, Stanford, CA, USA
6Chan Zuckerberg Biohub, San Francisco, CA USA
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  • For correspondence: tmclaugh@stanford.edu cblish@stanford.edu
Tracey L. McLaughlin
1Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
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  • For correspondence: tmclaugh@stanford.edu cblish@stanford.edu
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Abstract

The COVID-19 pandemic, caused by the viral pathogen SARS-CoV-2, has taken the lives of millions of individuals around the world. Obesity is associated with adverse COVID-19 outcomes, but the underlying mechanism is unknown. In this report, we demonstrate that human adipose tissue from multiple depots is permissive to SARS-CoV-2 infection and that infection elicits an inflammatory response, including the secretion of known inflammatory mediators of severe COVID-19. We identify two cellular targets of SARS-CoV-2 infection in adipose tissue: mature adipocytes and adipose tissue macrophages. Adipose tissue macrophage infection is largely restricted to a highly inflammatory subpopulation of macrophages, present at baseline, that is further activated in response to SARS-CoV-2 infection. Preadipocytes, while not infected, adopt a proinflammatory phenotype. We further demonstrate that SARS-CoV-2 RNA is detectable in adipocytes in COVID-19 autopsy cases and is associated with an inflammatory infiltrate. Collectively, our findings indicate that adipose tissue supports SARS-CoV-2 infection and pathogenic inflammation and may explain the link between obesity and severe COVID-19.

One sentence summary Our work provides the first in vivo evidence of SARS-CoV-2 infection in human adipose tissue and describes the associated inflammation.

Competing Interest Statement

CAB is on the Scientific Advisory Boards of Catamaran Bio and DeepCell. CMS is on the Scientific Advisory Board of and has received research funding from Enable Medicine, Inc., both outside the current work. MSM has served as a consultant for Novartis and Glaxo Smith Kline and received speaker's honoraria from ThermoFisher and Merck, all outside the current work.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 25, 2021.
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SARS-CoV-2 infects human adipose tissue and elicits an inflammatory response consistent with severe COVID-19
Giovanny J. Martínez-Colón, Kalani Ratnasiri, Heping Chen, Sizun Jiang, Elizabeth Zanley, Arjun Rustagi, Renu Verma, Han Chen, Jason R. Andrews, Kirsten D. Mertz, Alexandar Tzankov, Dan Azagury, Jack Boyd, Garry P. Nolan, Christian M. Schürch, Matthias S. Matter, Catherine A. Blish, Tracey L. McLaughlin
bioRxiv 2021.10.24.465626; doi: https://doi.org/10.1101/2021.10.24.465626
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SARS-CoV-2 infects human adipose tissue and elicits an inflammatory response consistent with severe COVID-19
Giovanny J. Martínez-Colón, Kalani Ratnasiri, Heping Chen, Sizun Jiang, Elizabeth Zanley, Arjun Rustagi, Renu Verma, Han Chen, Jason R. Andrews, Kirsten D. Mertz, Alexandar Tzankov, Dan Azagury, Jack Boyd, Garry P. Nolan, Christian M. Schürch, Matthias S. Matter, Catherine A. Blish, Tracey L. McLaughlin
bioRxiv 2021.10.24.465626; doi: https://doi.org/10.1101/2021.10.24.465626

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