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Mitochondrial phenotypes in purified human immune cell subtypes and cell mixtures

View ORCID ProfileShannon Rausser, Caroline Trumpff, Marlon A McGill, Alex Junker, Wei Wang, Siu-hong Ho, Anika Mitchell, View ORCID ProfileKalpita R Karan, Catherine Monk, View ORCID ProfileSuzanne C. Segerstrom, View ORCID ProfileRebecca G. Reed, View ORCID ProfileMartin Picard
doi: https://doi.org/10.1101/2020.10.16.342923
Shannon Rausser
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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  • ORCID record for Shannon Rausser
Caroline Trumpff
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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Marlon A McGill
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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Alex Junker
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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Wei Wang
2Columbia Center for Translational Immunology, Columbia University Irving Medical Center, New York, NY 10032, USA
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Siu-hong Ho
2Columbia Center for Translational Immunology, Columbia University Irving Medical Center, New York, NY 10032, USA
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Anika Mitchell
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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Kalpita R Karan
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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Catherine Monk
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
5Department of Neurology, Merritt Center, Columbia University Irving Medical Center, New York, NY 10032, USA
6Department of Obstetrics & Gynecology, Columbia University Irving Medical Center, New York, NY 10032, USA
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Suzanne C. Segerstrom
3Department of Psychology, University of Kentucky, Lexington, KY, 40506, USA
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Rebecca G. Reed
4Department of Psychology, University of Pittsburgh, Pittsburgh, PA, 15260, USA
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Martin Picard
1Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
6Department of Obstetrics & Gynecology, Columbia University Irving Medical Center, New York, NY 10032, USA
7New York State Psychiatric Institute, New York, NY 10032, USA
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  • For correspondence: martin.picard@columbia.edu
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Abstract

Mitochondrial function studies in human leukocytes have mainly focused on peripheral blood mononuclear cells (PBMCs), with the assumption that the immunometabolic properties of different immune cells have a negligible effect on PBMCs. Using a high-throughput mitochondrial phenotyping platform to quantify multiple mitochondrial features among both PBMCs and immunologically-defined immune cell subtypes from the same individuals, we show how mitochondrial activity in PBMCs is confounded by both cell type distributions and contaminating platelets. Then, applying this cell-specific approach in women and men spanning 4 decades of life, we find that mitochondria exhibit specific age- and sex-related differences, including an age-related elevation in mitochondrial DNA copy number (mtDNAcn), which are masked or blunted in PBMCs. Our purified cell subtypes data also define in humans the variation in mtDNAcn, mitochondrial content (citrate synthase), and respiratory chain enzymatic activities among neutrophils, monocytes, B and T lymphocyte subtypes. Moreover, we validate these cell type differences and define the natural intra-individual variation in mitochondrial function using an intensive repeated-measures study in a single individual, revealing substantial natural variation over time among cell subtypes and PBMCs. Finally, we introduce multivariate mitochondrial phenotypes – mitotypes – that distinguish lymphoid from myeloid cell types, naïve-to-memory lymphocyte states, and moderately differ between women and men, which we propose as potential cell-specific biomarkers for future studies. Together, these findings identify dynamic cell-type specific variation in mitochondrial biology in circulating human leukocytes, providing foundational knowledge to develop interpretable blood-based assays of mitochondrial health.

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-NC-ND 4.0 International license.
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Posted February 22, 2021.
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Mitochondrial phenotypes in purified human immune cell subtypes and cell mixtures
Shannon Rausser, Caroline Trumpff, Marlon A McGill, Alex Junker, Wei Wang, Siu-hong Ho, Anika Mitchell, Kalpita R Karan, Catherine Monk, Suzanne C. Segerstrom, Rebecca G. Reed, Martin Picard
bioRxiv 2020.10.16.342923; doi: https://doi.org/10.1101/2020.10.16.342923
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Mitochondrial phenotypes in purified human immune cell subtypes and cell mixtures
Shannon Rausser, Caroline Trumpff, Marlon A McGill, Alex Junker, Wei Wang, Siu-hong Ho, Anika Mitchell, Kalpita R Karan, Catherine Monk, Suzanne C. Segerstrom, Rebecca G. Reed, Martin Picard
bioRxiv 2020.10.16.342923; doi: https://doi.org/10.1101/2020.10.16.342923

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