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Single-cell resolution unravels spatial alterations in metabolism, transcriptome and epigenome of ageing liver

View ORCID ProfileChrysa Nikopoulou, Niklas Kleinenkuhnen, View ORCID ProfileSwati Parekh, Tonantzi Sandoval, Farina Schneider, View ORCID ProfilePatrick Giavalisco, Mihaela Bozukova, Anna Juliane Vesting, View ORCID ProfileJanine Altmüller, View ORCID ProfileThomas Wunderlich, View ORCID ProfileVangelis Kondylis, View ORCID ProfileAchim Tresch, View ORCID ProfilePeter Tessarz
doi: https://doi.org/10.1101/2021.12.14.472593
Chrysa Nikopoulou
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
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Niklas Kleinenkuhnen
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
2Institute of Medical Statistics and Computational Biology, Faculty of Medicine, University of Cologne, Bachemer Str. 86, 50931, Cologne, Germany
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Swati Parekh
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
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Tonantzi Sandoval
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
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Farina Schneider
3Institute for Pathology, University Hospital Cologne, Kerpener Str. 62, 50937 Cologne, Germany
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Patrick Giavalisco
4Metabolic Core Facility, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
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Mihaela Bozukova
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
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Anna Juliane Vesting
5Max Planck Institute for Metabolism Research, Gleueler Str. 50, 50931 Cologne, Germany
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Janine Altmüller
6Cologne Center for Genomics, University of Cologne, Cologne, Germany; Berlin Institute of Health at Charité, Core Facility Genomics, Berlin, Germany; Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.
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Thomas Wunderlich
5Max Planck Institute for Metabolism Research, Gleueler Str. 50, 50931 Cologne, Germany
7Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases (CECAD), Joseph-Stelzmann-Straße 26, 50931 Cologne, Germany
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Vangelis Kondylis
3Institute for Pathology, University Hospital Cologne, Kerpener Str. 62, 50937 Cologne, Germany
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Achim Tresch
2Institute of Medical Statistics and Computational Biology, Faculty of Medicine, University of Cologne, Bachemer Str. 86, 50931, Cologne, Germany
7Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases (CECAD), Joseph-Stelzmann-Straße 26, 50931 Cologne, Germany
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  • For correspondence: achim.tresch@uni-koeln.de ptessarz@age.mpg.de
Peter Tessarz
1Max Planck Research Group ‘Chromatin and Ageing’, Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str. 9b, 50931 Cologne, Germany
7Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases (CECAD), Joseph-Stelzmann-Straße 26, 50931 Cologne, Germany
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  • For correspondence: achim.tresch@uni-koeln.de ptessarz@age.mpg.de
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ABSTRACT

Epigenetic ageing clocks have revealed that tissues within an organism can age with different velocity. However, it has not been explored whether cells of one type experience different ageing trajectories within a tissue depending on their location. Here, we employed lipidomics, spatial transcriptomics and single-cell ATAC-seq in conjunction with available single-cell RNA-seq data to address how cells in the murine liver are affected by age-related changes of the microenvironment. Integration of the datasets revealed zonation-specific and age-related changes in metabolic states, the epigenome and transcriptome. Particularly periportal hepatocytes were characterized by decreased mitochondrial function and strong alterations in the epigenetic landscape, while pericentral hepatocytes – despite accumulation of large lipid droplets – did not show apparent functional differences. In general, chromatin alterations did not correlate well with transcriptional changes, hinting at post-transcriptional processes that shape gene expression during ageing. Together, we provide evidence that changing microenvironments within a tissue exert strong influences on their resident cells that can shape epigenetic, metabolic and phenotypic outputs.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted December 16, 2021.
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Single-cell resolution unravels spatial alterations in metabolism, transcriptome and epigenome of ageing liver
Chrysa Nikopoulou, Niklas Kleinenkuhnen, Swati Parekh, Tonantzi Sandoval, Farina Schneider, Patrick Giavalisco, Mihaela Bozukova, Anna Juliane Vesting, Janine Altmüller, Thomas Wunderlich, Vangelis Kondylis, Achim Tresch, Peter Tessarz
bioRxiv 2021.12.14.472593; doi: https://doi.org/10.1101/2021.12.14.472593
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Single-cell resolution unravels spatial alterations in metabolism, transcriptome and epigenome of ageing liver
Chrysa Nikopoulou, Niklas Kleinenkuhnen, Swati Parekh, Tonantzi Sandoval, Farina Schneider, Patrick Giavalisco, Mihaela Bozukova, Anna Juliane Vesting, Janine Altmüller, Thomas Wunderlich, Vangelis Kondylis, Achim Tresch, Peter Tessarz
bioRxiv 2021.12.14.472593; doi: https://doi.org/10.1101/2021.12.14.472593

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