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Psychoneuroendocrinology. 2019 Aug;106:268-276. doi: 10.1016/j.psyneuen.2019.03.026. Epub 2019 Mar 28.

Acute psychological stress increases serum circulating cell-free mitochondrial DNA.

Author information

1
Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA; New York State Psychiatric Institute, New York, NY, 10032, USA.
2
Department of Psychology, University of Pittsburgh, Pittsburgh, PA, 15260, USA. Electronic address: marsland@pitt.edu.
3
Universidad de Aysén, Coyhaique, Chile; Anatomy and Legal Medicine Department, Faculty of Medicine, Universidad de Chile, Santiago, Chile.
4
Department of Medicine, Division of Cardiology, Vascular Medicine Institute, Center for Metabolism and Mitochondrial Medicine, University of Pittsburgh Medical School, Pittsburgh, PA, 15261, USA.
5
Cousins Center for Psychoneuroimmunology, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA, 90095, USA.
6
Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA.
7
Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA; Wellcome Trust Centre for Mitochondrial Research, Institute of Neurosciences, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK.
8
Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA; New York State Psychiatric Institute, New York, NY, 10032, USA; Department of Neurology, H. Houston Merritt Center, Columbia Translational Neuroscience Initiative, Columbia University Irving Medical Center, New York, NY, 10032, USA.
9
Division of Nutritional Sciences, Cornell University, Ithaca, New York, NY, 14850, USA.
10
Department of Medicine, Division of Cardiology, Vascular Medicine Institute, Center for Metabolism and Mitochondrial Medicine, University of Pittsburgh Medical School, Pittsburgh, PA, 15261, USA. Electronic address: bkauf@pitt.edu.
11
Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA; New York State Psychiatric Institute, New York, NY, 10032, USA; Department of Neurology, H. Houston Merritt Center, Columbia Translational Neuroscience Initiative, Columbia University Irving Medical Center, New York, NY, 10032, USA; Columbia Aging Center, Columbia University Mailman School of Public Health, New York, NY, 10032, USA. Electronic address: martin.picard@columbia.edu.

Abstract

Intrinsic biological mechanisms transduce psychological stress into physiological adaptation that requires energy, but the role of mitochondria and mitochondrial DNA (mtDNA) in this process has not been defined in humans. Here, we show that similar to physical injury, exposure to psychological stress increases serum circulating cell-free mtDNA (ccf-mtDNA) levels. Healthy midlife adults exposed on two separate occasions to a brief psychological challenge exhibited a 2-3-fold increase in ccf-mtDNA, with no change in ccf-nuclear DNA levels, establishing the magnitude and specificity for ccf-mtDNA reactivity. In cell-based studies, we show that glucocorticoid signaling - a consequence of psychological stress in humans - is sufficient to induce mtDNA extrusion in a time frame consistent with stress-induced ccf-mtDNA increase. Collectively, these findings provide evidence that acute psychological stress induces ccf-mtDNA and implicate neuroendocrine signaling as a potential trigger for ccf-mtDNA release. Further controlled work is needed to confirm that observed increases in ccf-mtDNA result from stress exposure and to determine the functional significance of this effect.

KEYWORDS:

Cell-free DNA; Mitochondria; Mitokine; Neuroendocrine; Psychobiology; Psychosocial stress

PMID:
31029929
PMCID:
PMC6589121
[Available on 2020-08-01]
DOI:
10.1016/j.psyneuen.2019.03.026

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