Cited by 196Viral Infections and Immunology ResearchCOVID-19 Clinical Research StudiesSARS-CoV-2 and COVID-19 Research

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

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Bailey, Adam L., Dmytrenko, Oleksandr, Greenberg, Lina, Bredemeyer, Andrea L., Ma, Pan, Liu, Jing, Penna, Vinay, 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, Zhang, Xianwen, 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.·2021·JACC: Basic to Translational Science

DOI 10.1016/j.jacbts.2021.01.002PMC PMC7909907

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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.

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Additional file 4 of SARS-CoV-2 viral genes Nsp6, Nsp8, and M compromise cellular ATP levels to impair survival and function of human pluripotent stem cell-derived cardiomyocytes
Liu, J., Wu, S., Zhang, Y., Wang, C., Liu, S., Wan, J., & Yang, L. (2023) · Figshare · doi:10.6084/m9.figshare.24136215
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Additional file 3 of SARS-CoV-2 viral genes Nsp6, Nsp8, and M compromise cellular ATP levels to impair survival and function of human pluripotent stem cell-derived cardiomyocytes
Liu, J., Wu, S., Zhang, Y., Wang, C., Liu, S., Wan, J., & Yang, L. (2023) · Figshare · doi:10.6084/m9.figshare.24136212
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Additional file 5 of SARS-CoV-2 viral genes Nsp6, Nsp8, and M compromise cellular ATP levels to impair survival and function of human pluripotent stem cell-derived cardiomyocytes
Liu, J., Wu, S., Zhang, Y., Wang, C., Liu, S., Wan, J., & Yang, L. (2023) · Figshare · doi:10.6084/m9.figshare.24136218
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Additional file 2 of SARS-CoV-2 viral genes Nsp6, Nsp8, and M compromise cellular ATP levels to impair survival and function of human pluripotent stem cell-derived cardiomyocytes
Liu, J., Wu, S., Zhang, Y., Wang, C., Liu, S., Wan, J., & Yang, L. (2023) · Figshare · doi:10.6084/m9.figshare.24136209
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Heart failure and acute coronary syndrome with COVID-19
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Additional file 1 of Major adverse cardiovascular events are associated with necroptosis during severe COVID-19
Wiscovitch-Russo, R., Ibañez-Prada, E. D., Serrano-Mayorga, C. C., Sievers, B. L., Engelbride, M. A., Padmanabhan, S., Tan, G. S., Vashee, S., Bustos, I. G., Pachecho, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22671471
Additional file 6 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757205
Additional file 5 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757202
Additional file 4 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757199
Additional file 1 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757190
Additional file 7 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757208
Additional file 3 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757196
Additional file 8 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757211
Additional file 2 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757193
Additional file 2 of Major adverse cardiovascular events are associated with necroptosis during severe COVID-19
Wiscovitch-Russo, R., Ibañez-Prada, E. D., Serrano-Mayorga, C. C., Sievers, B. L., Engelbride, M. A., Padmanabhan, S., Tan, G. S., Vashee, S., Bustos, I. G., Pachecho, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22671474
Additional file 9 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757214
Additional file 1 of SARS-CoV-2 viral genes Nsp6, Nsp8, and M compromise cellular ATP levels to impair survival and function of human pluripotent stem cell-derived cardiomyocytes
Liu, J., Wu, S., Zhang, Y., Wang, C., Liu, S., Wan, J., & Yang, L. (2023) · Figshare · doi:10.6084/m9.figshare.24136206
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Additional file 10 of SARS-CoV-2 variants divergently infect and damage cardiomyocytes in vitro and in vivo
Mok, B. W.-Y., Kwok, M., Li, H. S., Ling, L., Lai, A., Yan, B., Law, C. T., Yeung, C. H., Zhang, A. J., Tam, R. C.-Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26757217
Unbiased cleavage site prediction uncovers viral antagonism of host innate immunity by SARS-CoV-2 3C-like protease
Yucel, N. D., Marchianò, S., Tchelepi, E., Paterlini, G., Kuznetsov, I. A., Li, K., Mcafee, Q. W., Nimmagadda, N., Ren, A., Shi, S., et al. (2026) · JCI Insight · doi:10.1172/jci.insight.185739
Molecular and cellular determinants of human iron overload cardiomyopathy
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Engineering Human Myocardium: Integrating the Maturation of hiPSC-Derived Cardiac Myocytes Across Genetic, Structural, Physiological and Multicellular Systems
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Obesity and Diabetes Increase SARS-CoV-2 Susceptibility Through Angiotensin-Converting Enzyme 2, Immunologic, and Gut Microbial Dysregulation
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Authors: Bailey, A. L., Dmytrenko, O., Greenberg, L., Bredemeyer, A. L., Ma, P., Liu, J., Penna, V., Winkler, E. S., Sviben, S., Brooks, E., Nair, A. P., Heck, K. A., Rali, A. S., Simpson, L., Saririan, M., Hobohm, D., Stump, W. T., Fitzpatrick, J. A., Xie, X., Zhang, X., Shi, P.-Y., Hinson, J. T., Gi, W.-T., Schmidt, C., Leuschner, F., Lin, C.-Y., Diamond, M. S., Greenberg, M. J., & Lavine, K. J.
Affiliations: Washington University in St. Louis (US)
University of Wisconsin–Madison (US)
Baylor College of Medicine (US)
Vanderbilt University (US)
Creighton University (US)
The University of Texas Medical Branch at Galveston (US)
The Jackson Laboratory for Genomic Medicine (US)
Heidelberg University (DE)
Corresponding author: Lavine, Kory J.
ORCID: Bailey, Adam L.
Dmytrenko, Oleksandr
Greenberg, Lina
Bredemeyer, Andrea L.
Ma, Pan
Liu, Jing
Penna, Vinay
Winkler, Emma S.
Sviben, Sanja
Brooks, Erin
Nair, Ajith P.
Rali, Aniket S.
Simpson, Leo
Saririan, Mehrdad
Fitzpatrick, James A.
Xie, Xuping
Zhang, Xianwen
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.
Venue: JACC: Basic to Translational Science
Publisher: Elsevier BV
Published: 2021-04
Volume: 6
Issue: 4
Pages: 331-345
ISSN: 2452-302X (ISSN-L)
DOI: 10.1016/j.jacbts.2021.01.002
PMC: PMC7909907
OpenAlex: W3134776434
Cited by: 193
References: 80
Citations by year: 2026: 8 · 2025: 13 · 2024: 37 · 2023: 50 · 2022: 42 · 2021: 43
FWCI: 29.50
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: JACC Basic to Translational Science (publishedVersion, cc-by-nc-nd)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by-nc-nd)
PubMed Central (submittedVersion)
Digital Commons-TMC (Texas Medical Center) (submittedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: Foundation for Barnes-Jewish Hospital
Center for Cellular Imaging, Washington University
National Institutes of Health (75N93019C00062, R01 AI127828, R01 HL138466, R01 HL139714, R01 HL141086)
St. Louis Children's Hospital (CDI-CORE-2015-505, CDI-CORE-2019-813)
Defense Advanced Research Projects Agency (HR001117S0019)
Burroughs Wellcome Fund (1014782)
March of Dimes Foundation (FY18-BOC-430198)
Topics: Health Sciences › Medicine › Infectious Diseases › Viral Infections and Immunology Research
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Keywords: SARS-CoV-2, COVID-19 myocarditis, engineered heart tissue, cardiac complications of COVID-19, sarcomere disassembly, cytokine production, cardiomyocyte contractile dysfunction, cell death, viral pathogenesis, myocardial pathology

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

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