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[Preprint]. 2020 Nov 17:rs.3.rs-94634. [Version 1] doi: 10.21203/rs.3.rs-94634/v1

SARS-CoV-2 Infected Cardiomyocytes Recruit Monocytes by Secreting CCL2

Shuibing Chen, Liuliu Yang, Benjamin Nilsson-Payant, Yuling Han, Fabrice Jaffré, Jiajun Zhu, Pengfei Wang, Tuo Zhang, David Redmond, Sean Houghton, Rasmus Møller, Daisy Hoagland, Shu Horiuchi, Joshua Acklin, Jean Lim, Yaron Bram, Chanel Richardson, Vasuretha Chandar, Alain Borczuk, Yaoxing Huang, Jenny Xiang, David Ho, Robert Schwartz, Benjamin tenOever, Todd Evans
PMCID: PMC7685325  PMID: 33236003

Abstract

Heart injury has been reported in up to 20% of COVID-19 patients, yet the cause of myocardial histopathology remains unknown. In order to study the cause of myocardial pathology in COVID-19 patients, we used a hamster model to determine whether following infection SARS-CoV-2, the causative agent of COVID-19, can be detected in heart tissues. Here, we clearly demonstrate that viral RNA and nucleocapsid protein is present in cardiomyocytes in the hearts of infected hamsters. Interestingly, functional cardiomyocyte associated gene expression was decreased in infected hamster hearts, corresponding to an increase in reactive oxygen species (ROS). This data using an animal model was further validated using autopsy heart samples of COVID-19 patients. Moreover, we show that both human pluripotent stem cell-derived cardiomyocytes (hPSC-derived CMs) and adult cardiomyocytes (CMs) can be infected by SARS-CoV-2 and that CCL2 is secreted upon SARS-CoV-2 infection, leading to monocyte recruitment. Increased CCL2 expression and macrophage infiltration was also observed in the hearts of infected hamsters. Using single cell RNA-seq, we also show that macrophages are able to decrease SARS-CoV-2 infection of CMs. Overall, our study provides direct evidence that SARS-CoV-2 infects CMs in vivo and proposes a mechanism of immune-cell infiltration and pathology in heart tissue of COVID-19 patients.

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