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Cells and gene expression programs in the adult human heart

View ORCID ProfileMonika Litviňuková, View ORCID ProfileCarlos Talavera-López, View ORCID ProfileHenrike Maatz, View ORCID ProfileDaniel Reichart, View ORCID ProfileCatherine L. Worth, Eric L. Lindberg, View ORCID ProfileMasatoshi Kanda, Krzysztof Polanski, Eirini S. Fasouli, Sara Samari, Kenny Roberts, Liz Tuck, View ORCID ProfileMatthias Heinig, Daniel M. DeLaughter, Barbara McDonough, Hiroko Wakimoto, Joshua M. Gorham, Emily R. Nadelmann, Krishnaa T. Mahbubani, View ORCID ProfileKourosh Saeb-Parsy, Giannino Patone, View ORCID ProfileJoseph J. Boyle, Hongbo Zhang, Hao Zhang, Anissa Viveiros, Gavin Y. Oudit, View ORCID ProfileOmer Bayraktar, J. G. Seidman, View ORCID ProfileChristine Seidman, View ORCID ProfileMichela Noseda, View ORCID ProfileNorbert Hübner, View ORCID ProfileSarah A. Teichmann
doi: https://doi.org/10.1101/2020.04.03.024075
Monika Litviňuková
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
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Carlos Talavera-López
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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  • ORCID record for Carlos Talavera-López
Henrike Maatz
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
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Daniel Reichart
3Department of Genetics, Harvard Medical School, Boston, MA, United States
19Department of Cardiology, University Heart&Vascular Center, University of Hamburg, Hamburg, Germany
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Catherine L. Worth
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
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Eric L. Lindberg
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
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Masatoshi Kanda
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
14Department of Rheumatology and Clinical Immunology, Sapporo Medical University, Sapporo, Japan
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Krzysztof Polanski
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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Eirini S. Fasouli
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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Sara Samari
5National Heart and Lung Institute, Imperial College London, London, United Kingdom
6British Heart Foundation Centre for Research Excellence and Centre for Regenerative Medicine, Imperial College London, United Kingdom
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Kenny Roberts
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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Liz Tuck
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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Matthias Heinig
17Institute of Computational Biology (ICB), HMGU, Neuherberg, Germany
18Department of Informatics, Technische Universitaet Muenchen (TUM), Munich, Germany
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Daniel M. DeLaughter
3Department of Genetics, Harvard Medical School, Boston, MA, United States
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Barbara McDonough
15Cardiovascular Division, Brigham and Women’s Hospital, Boston, MA, USA
16Howard Hughes Medical Institute, Chevy Chase, MD, USA
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Hiroko Wakimoto
3Department of Genetics, Harvard Medical School, Boston, MA, United States
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Joshua M. Gorham
3Department of Genetics, Harvard Medical School, Boston, MA, United States
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Emily R. Nadelmann
3Department of Genetics, Harvard Medical School, Boston, MA, United States
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Krishnaa T. Mahbubani
8Department of Surgery, University of Cambridge, NIHR Cambridge Biomedical Centre, and Cambridge Biorepository for Translational Medicine, Cambridge, United Kingdom
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Kourosh Saeb-Parsy
8Department of Surgery, University of Cambridge, NIHR Cambridge Biomedical Centre, and Cambridge Biorepository for Translational Medicine, Cambridge, United Kingdom
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Giannino Patone
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
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Joseph J. Boyle
5National Heart and Lung Institute, Imperial College London, London, United Kingdom
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Hongbo Zhang
7Department of Histology and Embryology of Zhongshan School of Medicine, Sun-Yat Sen University, Guangzhou, China
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Hao Zhang
9Division of Cardiology Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
10Mazankowski Alberta Heart Institute Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
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Anissa Viveiros
9Division of Cardiology Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
10Mazankowski Alberta Heart Institute Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
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Gavin Y. Oudit
9Division of Cardiology Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
10Mazankowski Alberta Heart Institute Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada
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Omer Bayraktar
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
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J. G. Seidman
3Department of Genetics, Harvard Medical School, Boston, MA, United States
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  • For correspondence: st9@sanger.ac.uk
Christine Seidman
3Department of Genetics, Harvard Medical School, Boston, MA, United States
15Cardiovascular Division, Brigham and Women’s Hospital, Boston, MA, USA
16Howard Hughes Medical Institute, Chevy Chase, MD, USA
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  • For correspondence: st9@sanger.ac.uk
Michela Noseda
5National Heart and Lung Institute, Imperial College London, London, United Kingdom
6British Heart Foundation Centre for Research Excellence and Centre for Regenerative Medicine, Imperial College London, United Kingdom
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  • For correspondence: st9@sanger.ac.uk
Norbert Hübner
2Cardiovascular and Metabolic Sciences, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
11DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Berlin, Germany
12Berlin Institute of Health (BIH), Berlin, Germany
13Charité-Universitätsmedizin, Berlin, Germany
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  • For correspondence: st9@sanger.ac.uk
Sarah A. Teichmann
1Cellular Genetics Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom
4Dept Physics/Cavendish Laboratory, University of Cambridge, JJ Thompson Ave, Cambridge CB3 0EH, United Kingdom
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  • For correspondence: st9@sanger.ac.uk
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Summary

Cardiovascular disease is the leading cause of death worldwide. Advanced insights into disease mechanisms and strategies to improve therapeutic opportunities require deeper understanding of the molecular processes of the normal heart. Knowledge of the full repertoire of cardiac cells and their gene expression profiles is a fundamental first step in this endeavor. Here, using large-scale single cell and nuclei transcriptomic profiling together with state-of-the-art analytical techniques, we characterise the adult human heart cellular landscape covering six anatomical cardiac regions (left and right atria and ventricles, apex and interventricular septum). Our results highlight the cellular heterogeneity of cardiomyocytes, pericytes and fibroblasts, revealing distinct subsets in the atria and ventricles indicative of diverse developmental origins and specialized properties. Further we define the complexity of the cardiac vascular network which includes clusters of arterial, capillary, venous, lymphatic endothelial cells and an atrial-enriched population. By comparing cardiac cells to skeletal muscle and kidney, we identify cardiac tissue resident macrophage subsets with transcriptional signatures indicative of both inflammatory and reparative phenotypes. Further, inference of cell-cell interactions highlight a macrophage-fibroblast-cardiomyocyte network that differs between atria and ventricles, and compared to skeletal muscle. We expect this reference human cardiac cell atlas to advance mechanistic studies of heart homeostasis and disease.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.heartcellatlas.org/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Cells and gene expression programs in the adult human heart
Monika Litviňuková, Carlos Talavera-López, Henrike Maatz, Daniel Reichart, Catherine L. Worth, Eric L. Lindberg, Masatoshi Kanda, Krzysztof Polanski, Eirini S. Fasouli, Sara Samari, Kenny Roberts, Liz Tuck, Matthias Heinig, Daniel M. DeLaughter, Barbara McDonough, Hiroko Wakimoto, Joshua M. Gorham, Emily R. Nadelmann, Krishnaa T. Mahbubani, Kourosh Saeb-Parsy, Giannino Patone, Joseph J. Boyle, Hongbo Zhang, Hao Zhang, Anissa Viveiros, Gavin Y. Oudit, Omer Bayraktar, J. G. Seidman, Christine Seidman, Michela Noseda, Norbert Hübner, Sarah A. Teichmann
bioRxiv 2020.04.03.024075; doi: https://doi.org/10.1101/2020.04.03.024075
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Cells and gene expression programs in the adult human heart
Monika Litviňuková, Carlos Talavera-López, Henrike Maatz, Daniel Reichart, Catherine L. Worth, Eric L. Lindberg, Masatoshi Kanda, Krzysztof Polanski, Eirini S. Fasouli, Sara Samari, Kenny Roberts, Liz Tuck, Matthias Heinig, Daniel M. DeLaughter, Barbara McDonough, Hiroko Wakimoto, Joshua M. Gorham, Emily R. Nadelmann, Krishnaa T. Mahbubani, Kourosh Saeb-Parsy, Giannino Patone, Joseph J. Boyle, Hongbo Zhang, Hao Zhang, Anissa Viveiros, Gavin Y. Oudit, Omer Bayraktar, J. G. Seidman, Christine Seidman, Michela Noseda, Norbert Hübner, Sarah A. Teichmann
bioRxiv 2020.04.03.024075; doi: https://doi.org/10.1101/2020.04.03.024075

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