SARS-CoV-2 Infects Human Engineered Heart Tissues and Models COVID-19 Myocarditis

Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications resu...

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Main Authors Bailey, Adam L, Dmytrenko, Oleksandr, Greenberg, Lina, Bredemeyer, Andrea L, Ma, Pan, Liu, Jing, Penna, Vinay, Lai, Lulu, Winkler, Emma S, Sviben, Sanja, Brooks, Erin, Nair, Ajith P, Heck, Kent A, Rali, Aniket S, Simpson, Leo, Saririan, Mehrdad, Hobohm, Dan, Stump, W Tom, Fitzpatrick, James A, Xie, Xuping, Shi, Pei-Yong, Hinson, J Travis, Gi, Weng-Tein, Schmidt, Constanze, Leuschner, Florian, Lin, Chieh-Yu, Diamond, Michael S, Greenberg, Michael J, Lavine, Kory J
Format Journal Article Paper
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 05.11.2020
Cold Spring Harbor Laboratory
Edition1.1
Subjects
ACE2
Angiotensin
Angiotensin-converting enzyme 2
Apoptosis
Autopsy
Biotechnology
Cardiomyocytes
Cell activation
Cell death
Coronaviruses
COVID-19
Epidemiology
Heart diseases
Immunology
Infections
Laboratories
Macrophages
Muscle contraction
Myocarditis
Pandemics
Severe acute respiratory syndrome coronavirus 2
Tropism
COVID-19
Myocarditis
SARS-CoV-2
Engineered Heart Tissue
Cardiomyocyte
Macrophage
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Abstract Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications result directly from myocardial infection. Here, we develop a human engineered heart tissue model and demonstrate that SARS-CoV-2 selectively infects cardiomyocytes. Viral infection is dependent on expression of angiotensin-I converting enzyme 2 (ACE2) and endosomal cysteine proteases, suggesting an endosomal mechanism of cell entry. After infection with SARS-CoV-2, engineered tissues display typical features of myocarditis, including cardiomyocyte cell death, impaired cardiac contractility, and innate immune cell activation. Consistent with these findings, autopsy tissue obtained from individuals with COVID-19 myocarditis demonstrated cardiomyocyte infection, cell death, and macrophage-predominate immune cell infiltrate. These findings establish human cardiomyocyte tropism for SARS-CoV-2 and provide an experimental platform for interrogating and mitigating cardiac complications of COVID-19.
AbstractList Abstract Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications result directly from myocardial infection. Here, we develop a human engineered heart tissue model and demonstrate that SARS-CoV-2 selectively infects cardiomyocytes. Viral infection is dependent on expression of angiotensin-I converting enzyme 2 (ACE2) and endosomal cysteine proteases, suggesting an endosomal mechanism of cell entry. After infection with SARS-CoV-2, engineered tissues display typical features of myocarditis, including cardiomyocyte cell death, impaired cardiac contractility, and innate immune cell activation. Consistent with these findings, autopsy tissue obtained from individuals with COVID-19 myocarditis demonstrated cardiomyocyte infection, cell death, and macrophage-predominate immune cell infiltrate. These findings establish human cardiomyocyte tropism for SARS-CoV-2 and provide an experimental platform for interrogating and mitigating cardiac complications of COVID-19. Competing Interest Statement Kory Lavine - Medtronic: DT-PAS/APOGEE trial advisory board. M.S.D. is a consultant for Inbios, Eli Lilly, Vir Biotechnology, NGM Biopharmaceuticals, and on the Scientific Advisory Board of Moderna. The Lavine laboratory has received funding and unrelated sponsored research agreements from Amgen. The Diamond laboratory has received funding and unrelated sponsored research agreements from Moderna, Vir Biotechnology, and Emergent BioSolutions. Lina Greenberg, W. Tom Stump, Michael Greenberg, Adam Bailey, Oleksandr Dmytrenko, Andrea Bredemeyer - None. Footnotes * ↵* Co-first authors * ↵# Co-senior authors
Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications result directly from myocardial infection. Here, we develop a human engineered heart tissue model and demonstrate that SARS-CoV-2 selectively infects cardiomyocytes. Viral infection is dependent on expression of angiotensin-I converting enzyme 2 (ACE2) and endosomal cysteine proteases, suggesting an endosomal mechanism of cell entry. After infection with SARS-CoV-2, engineered tissues display typical features of myocarditis, including cardiomyocyte cell death, impaired cardiac contractility, and innate immune cell activation. Consistent with these findings, autopsy tissue obtained from individuals with COVID-19 myocarditis demonstrated cardiomyocyte infection, cell death, and macrophage-predominate immune cell infiltrate. These findings establish human cardiomyocyte tropism for SARS-CoV-2 and provide an experimental platform for interrogating and mitigating cardiac complications of COVID-19.
Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications result directly from myocardial infection. Here, we develop a human engineered heart tissue model and demonstrate that SARS-CoV-2 selectively infects cardiomyocytes. Viral infection is dependent on expression of angiotensin-I converting enzyme 2 (ACE2) and endosomal cysteine proteases, suggesting an endosomal mechanism of cell entry. After infection with SARS-CoV-2, engineered tissues display typical features of myocarditis, including cardiomyocyte cell death, impaired cardiac contractility, and innate immune cell activation. Consistent with these findings, autopsy tissue obtained from individuals with COVID-19 myocarditis demonstrated cardiomyocyte infection, cell death, and macrophage-predominate immune cell infiltrate. These findings establish human cardiomyocyte tropism for SARS-CoV-2 and provide an experimental platform for interrogating and mitigating cardiac complications of COVID-19.Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are predictors of poor outcomes. Nonetheless, little is understood regarding SARS-CoV-2 tropism within the heart and whether cardiac complications result directly from myocardial infection. Here, we develop a human engineered heart tissue model and demonstrate that SARS-CoV-2 selectively infects cardiomyocytes. Viral infection is dependent on expression of angiotensin-I converting enzyme 2 (ACE2) and endosomal cysteine proteases, suggesting an endosomal mechanism of cell entry. After infection with SARS-CoV-2, engineered tissues display typical features of myocarditis, including cardiomyocyte cell death, impaired cardiac contractility, and innate immune cell activation. Consistent with these findings, autopsy tissue obtained from individuals with COVID-19 myocarditis demonstrated cardiomyocyte infection, cell death, and macrophage-predominate immune cell infiltrate. These findings establish human cardiomyocyte tropism for SARS-CoV-2 and provide an experimental platform for interrogating and mitigating cardiac complications of COVID-19.
Author Dmytrenko, Oleksandr
Saririan, Mehrdad
Greenberg, Michael J
Nair, Ajith P
Simpson, Leo
Lin, Chieh-Yu
Fitzpatrick, James A
Ma, Pan
Shi, Pei-Yong
Leuschner, Florian
Bailey, Adam L
Bredemeyer, Andrea L
Lai, Lulu
Schmidt, Constanze
Hinson, J Travis
Liu, Jing
Stump, W Tom
Rali, Aniket S
Hobohm, Dan
Sviben, Sanja
Lavine, Kory J
Xie, Xuping
Heck, Kent A
Penna, Vinay
Brooks, Erin
Greenberg, Lina
Diamond, Michael S
Winkler, Emma S
Gi, Weng-Tein
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Keywords COVID-19
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Engineered Heart Tissue
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Macrophage
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Competing Interest Statement: Kory Lavine - Medtronic: DT-PAS/APOGEE trial advisory board. M.S.D. is a consultant for Inbios, Eli Lilly, Vir Biotechnology, NGM Biopharmaceuticals, and on the Scientific Advisory Board of Moderna. The Lavine laboratory has received funding and unrelated sponsored research agreements from Amgen. The Diamond laboratory has received funding and unrelated sponsored research agreements from Moderna, Vir Biotechnology, and Emergent BioSolutions. Lina Greenberg, W. Tom Stump, Michael Greenberg, Adam Bailey, Oleksandr Dmytrenko, Andrea Bredemeyer - None.
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Snippet Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis are...
Abstract Epidemiological studies of the COVID-19 pandemic have revealed evidence of cardiac involvement and documented that myocardial injury and myocarditis...
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SubjectTerms ACE2
Angiotensin
Angiotensin-converting enzyme 2
Apoptosis
Autopsy
Biotechnology
Cardiomyocytes
Cell activation
Cell death
Coronaviruses
COVID-19
Epidemiology
Heart diseases
Immunology
Infections
Laboratories
Macrophages
Muscle contraction
Myocarditis
Pandemics
Severe acute respiratory syndrome coronavirus 2
Tropism
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Title SARS-CoV-2 Infects Human Engineered Heart Tissues and Models COVID-19 Myocarditis
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