journal article Open Access Feb 01, 2018

Psychological Stress and Mitochondria: A Systematic Review

View at Publisher Save 10.1097/psy.0000000000000545
Abstract
ABSTRACT

Objective
Mitochondria are multifunctional life-sustaining organelles that represent a potential intersection point between psychosocial experiences and biological stress responses. This article provides a systematic review of the effects of psychological stress on mitochondrial structure and function.


Methods
A systematic review of the literature investigating the effects of psychological stress on mitochondrial function was conducted. The review focused on experimentally controlled studies allowing us to draw causal inference about the effect of induced psychological stress on mitochondria.


Results
A total of 23 studies met the inclusion criteria. All studies involved male laboratory animals, and most demonstrated that acute and chronic stressors influenced specific facets of mitochondrial function, particularly within the brain. Nineteen studies showed significant adverse effects of psychological stress on mitochondria and four found increases in function or size after stress. In humans, only six observational studies were available, none with experimental designs, and most only measured biological markers that do not directly reflect mitochondrial function, such as mitochondrial DNA copy number.


Conclusons
Overall, evidence supports the notion that acute and chronic stressors influence various aspects of mitochondrial biology, and that chronic stress exposure can lead to molecular and functional recalibrations among mitochondria. Limitations of current animal and human studies are discussed. Maladaptive mitochondrial changes that characterize this subcellular state of stress are termed mitochondrial allostatic load. Prospective studies with sensitive measures of specific mitochondrial outcomes will be needed to establish the link between psychosocial stressors, emotional states, the resulting neuroendocrine and immune processes, and mitochondrial energetics relevant to mind-body research in humans.
Topics

No keywords indexed for this article. Browse by subject →

References
116
[1]
"Mitochondria and the economy of stress (mal)adaptation" Neurosci Biobehav Rev (2013) 10.1016/j.neubiorev.2013.02.005
[2]
"Mitochondria as key components of the stress response" Trends Endocrinol Metab (2007) 10.1016/j.tem.2007.04.004
[3]
"Mitochondrial allostatic load puts the ‘gluc’ back in glucocorticoids" Nat Rev Endocrinol (2014) 10.1038/nrendo.2014.22
[4]
"The rise of mitochondria in medicine" Mitochondrion (2016) 10.1016/j.mito.2016.07.003
[5]
Mitochondrial diseases

Gráinne S. Gorman, Patrick F. Chinnery, Salvatore DiMauro et al.

Nature Reviews Disease Primers 2016 10.1038/nrdp.2016.80
[6]
"Mitochondrial energy deficiency leads to hyperproliferation of skeletal muscle mitochondria and enhanced insulin sensitivity" Proc Natl Acad Sci U S A (2017) 10.1073/pnas.1700997114
[7]
"A cannabinoid link between mitochondria and memory" Nature (2016) 10.1038/nature20127
[8]
"Fueling immunity: insights into metabolism and lymphocyte function" Science (2013) 10.1126/science.1242454
[9]
"Mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing" Nature (2016) 10.1038/nature18618
[10]
"Premature ageing in mice expressing defective mitochondrial DNA polymerase" Nature (2004) 10.1038/nature02517
[11]
"Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging" Science (2005) 10.1126/science.1112125
[12]
"Protective and damaging effects of stress mediators: central role of the brain" Dialogues Clin Neurosci (2006) 10.31887/dcns.2006.8.4/bmcewen
[13]
"Psychoneuroimmunology and psychosomatic medicine: back to the future" Psychosom Med (2002) 10.1097/00006842-200201000-00004
[14]
"Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry" Psychol Bull (2004) 10.1037/0033-2909.130.4.601
[15]
"Reciprocal regulation of the neural and innate immune systems" Nat Rev Immunol (2011) 10.1038/nri3042
[16]
"Sympathetic nervous system regulation of the tumour microenvironment" Nat Rev Cancer (2015) 10.1038/nrc3978
[17]
"The emerging field of human social genomics" Clin Psychol Sci (2013) 10.1177/2167702613478594
[18]
"Stress and telomere biology: a lifespan perspective" Psychoneuroendocrinology (2013) 10.1016/j.psyneuen.2013.03.010
[19]
"Early-life experience, epigenetics, and the developing brain" Neuropsychopharmacology (2015) 10.1038/npp.2014.140
[20]
"A healthy mix of emotions: underlying biological pathways linking emotions to physical health" Curr Opin Behav Sci (2017)
[21]
Psychological Stress and Mitochondria: A Conceptual Framework

Martin Picard, Bruce S. McEwen

Psychosomatic Medicine 2018 10.1097/psy.0000000000000544
[22]
"Mitochondrial synapses: intracellular communication and signal integration" Trends Neurosci (2015) 10.1016/j.tins.2015.06.001
[23]
"Mitochondrial Nanotunnels" Trends Cell Biol (2017) 10.1016/j.tcb.2017.08.009
[24]
"The nexus of chromatin regulation and intermediary metabolism" Nature (2013) 10.1038/nature12752
[25]
"Progressive increase in mtDNA 3243A > G heteroplasmy causes abrupt transcriptional reprogramming" Proc Natl Acad Sci U S A (2014)
[26]
"Mitochondria, energetics, epigenetics, and cellular responses to stress" Environ Health Perspect (2014) 10.1289/ehp.1408418
[27]
"MOTS-c: a novel mitochondrial-derived peptide regulating muscle and fat metabolism" Free Radic Biol Med (2016) 10.1016/j.freeradbiomed.2016.05.015
[28]
"Glucocorticoids induce mitochondrial gene transcription in HepG2 cells: role of the mitochondrial glucocorticoid receptor" Biochim Biophys Acta (2011) 10.1016/j.bbamcr.2011.05.014
[29]
"Maternal inheritance of human mitochondrial DNA" Proc Natl Acad Sci U S A (1980) 10.1073/pnas.77.11.6715
[30]
"Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease" Cold Spring Harb Perspect Med (2013)
[31]
"Molecular and bioenergetic differences between cells with African versus European inherited mitochondrial DNA haplogroups: implications for population susceptibility to diseases" Biochim Biophys Acta (2014) 10.1016/j.bbadis.2013.10.016
[32]
Telomeres and telomerase

Simon R. W. L. Chan, Elizabeth H. Blackburn

Philosophical Transactions of the Royal Society B:... 2004 10.1098/rstb.2003.1370
[33]
"Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress" Proc Natl Acad Sci U S A (1997) 10.1073/pnas.94.2.514
[34]
"Reactive oxygen species production by mitochondria" Methods Mol Biol (2009) 10.1007/978-1-59745-521-3_11
[35]
"Mitochondria, oxidants, and aging" Cell (2005) 10.1016/j.cell.2005.02.001
[36]
"The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer's disease" J Neurosci (2011) 10.1523/jneurosci.0552-11.2011
[37]
"Chemiosmotic hypothesis of oxidative phosphorylation" Nature (1967) 10.1038/213137a0
[38]
"Mitochondrial metabolic function assessed in vivo and in vitro" Curr Opin Clin Nutr Metab Care (2010) 10.1097/mco.0b013e32833cc93d
[39]
"Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells" Nat Protoc (2008) 10.1038/nprot.2008.61
[40]
"Bioenergetics and the oxidative burst: protocols for the isolation and evaluation of human leukocytes and platelets" J Vis Exp (2014)
[41]
"Development and implementation of standardized respiratory chain spectrophotometric assays for clinical diagnosis" Mitochondrion (2009) 10.1016/j.mito.2009.05.001
[42]
"Mitochondrial dysfunction and the pathophysiology of myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS)" Int J Clin Exp Med (2012)
[43]
"Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function" Am J Physiol Cell Physiol (2012) 10.1152/ajpcell.00368.2011
[44]
"Protein composition and function of red and white skeletal muscle mitochondria" Am J Physiol Cell Physiol (2011) 10.1152/ajpcell.00496.2010
[45]
"Quantitative proteomics of synaptic and nonsynaptic mitochondria: insights for synaptic mitochondrial vulnerability" J Proteome Res (2014) 10.1021/pr500295n
[46]
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement

David Moher, Alessandro Liberati, Jennifer Tetzlaff et al.

PLoS Medicine 2009 10.1371/journal.pmed.1000097
[47]
"Social isolation in rats inhibits oxidative metabolism, decreases the content of mitochondrial K-Ras and activates mitochondrial hexokinase" Behav Brain Res (2009) 10.1016/j.bbr.2009.07.009
[48]
"Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex" Neurochem Res (2012) 10.1007/s11064-012-0709-1
[49]
"The opposite roles of glucocorticoid and α1-adrenergic receptors in stress triggered apoptosis of rat Leydig cells" Am J Physiol Endocrinol Metab (2013) 10.1152/ajpendo.00443.2012
[50]
"Acute stress delays brain mitochondrial permeability transition pore opening" J Neurochem (2014) 10.1111/jnc.12811

Showing 50 of 116 references

Metrics
286
Citations
116
References
Details
Published
Feb 01, 2018
Vol/Issue
80(2)
Pages
141-153
License
View
Cite This Article
Martin Picard, Bruce S. McEwen (2018). Psychological Stress and Mitochondria: A Systematic Review. Psychosomatic Medicine, 80(2), 141-153. https://doi.org/10.1097/psy.0000000000000545
Related

You May Also Like

Impact of Event Scale: A Measure of Subjective Stress

Mardi Horowitz, Nancy Wilner · 1979

6,058 citations

Associations of Depression With C-Reactive Protein, IL-1, and IL-6: A Meta-Analysis

M Bryant Howren, Donald M. Lamkin · 2009

2,357 citations

Assessing Quality of Life in Older Adults With Cognitive Impairment

Rebecca G. Logsdon, Laura E. Gibbons · 2002

1,099 citations