Mitochondrial functions modulate neuroendocrine, metabolic, inflammatory, and transcriptional responses to acute psychological stress

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 48, 2015, Pages E6614-E6623

  Picard, Martin ^a,b,e   McManus, Meagan J ^a,b   Gray, Jason D ^c   Nasca, Carla ^c   Moffat, Cynthia ^d   Kopinski, Piotr K ^a,b   Seifert, Erin L ^d   McEwen, Bruce S ^c   Wallace, Douglas C ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e Columbia University Medical Center ^*  (United States)

Author keywords

Catecholamines; Hippocampus; HPA axis; Mitochondria; Stress reactivity

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADRENALIN; BIOGENIC AMINE; CELL NUCLEUS DNA; CORTICOSTERONE; CORTICOTROPIN; CYTOCHROME C OXIDASE; DOPAMINE; FATTY ACID; GLUCOCORTICOID; GLUCOSE; INTERLEUKIN 6; MITOCHONDRIAL DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; NORADRENALIN; PROTEIN C FOS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE 6; SEROTONIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CATECHOLAMINE; INTERLEUKIN-6, MOUSE; MITOCHONDRIAL PROTEIN; NADH DEHYDROGENASE SUBUNIT 6, MOUSE; NNT PROTEIN, MOUSE;

ADRENAL CORTEX; AMINO ACID BLOOD LEVEL; ANIMAL EXPERIMENT; BRAIN METABOLISM; BRAIN MITOCHONDRION; BRAIN REGION; CATECHOLAMINE BLOOD LEVEL; CELL ENERGY; CELL FUNCTION; CHRONIC STRESS; CONFERENCE PAPER; CONTROLLED STUDY; CYTOPLASM; DEAMINATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENERGY METABOLISM; ENERGY TRANSFER; ENERGY YIELD; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC CODE; GENETIC TRANSCRIPTION; GENOTYPE; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; INSULIN RELEASE; INSULIN RESISTANCE; LIPOLYSIS; MENTAL STRESS; METABOLISM; MITOCHONDRIAL DYNAMICS; MOUSE; NEGATIVE FEEDBACK; NERVOUS SYSTEM INFLAMMATION; NEUROENDOCRINE SYSTEM; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; RESPIRATORY CHAIN; STRAIN DIFFERENCE; UREA CYCLE; ALLOSTASIS; ANIMAL; BLOOD; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; INFLAMMATION; MALE; MITOCHONDRION; MUTATION; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; ADRENOCORTICOTROPIC HORMONE; ALLOSTASIS; ANIMALS; CATECHOLAMINES; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION; GENOTYPE; HIPPOCAMPUS; INFLAMMATION; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; NADH DEHYDROGENASE; NADP TRANSHYDROGENASE, AB-SPECIFIC; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84948679316     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1515733112     Document Type: Article

References (83)

1. McEwen BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Ann N Y Acad Sci 840:33-44.
2. Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685-1687.
3. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87(3):873-904.
4. Lundberg U (2005) Stress hormones in health and illness: The roles of work and gender. Psychoneuroendocrinology 30(10):1017-1021.
5. Rohleder N (2014) Stimulation of systemic low-grade inflammation by psychosocial stress. Psychosom Med 76(3):181-189.
6. Picard M, Juster RP, McEwen BS (2014) Mitochondrial allostatic load puts the 'gluc' back in glucocorticoids. Nat Rev Endocrinol 10(5):303-310.
7. Andrews RC, Walker BR (1999) Glucocorticoids and insulin resistance: Old hormones, new targets. Clin Sci (Lond) 96(5):513-523.
8. Gray JD, Rubin TG, Hunter RG, McEwen BS (2014) Hippocampal gene expression changes underlying stress sensitization and recovery. Mol Psychiatry 19(11):1171-1178.
9. Nasca C, Bigio B, Zelli D, Nicoletti F, McEwen BS (2015) Mind the gap: Glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility. Mol Psychiatry 20(6):755-76.
10. Wallace DC, Fan W, Procaccio V (2010) Mitochondrial energetics and therapeutics. Annu Rev Path 5:297-348.
11. Lambert AJ, Brand MD (2009) Reactive oxygen species production by mitochondria. Methods Mol Biol 554:165-181.
12. Arkblad EL, Betsholtz C, Rydström J (1996) The cDNA sequence of proton-pumping nicotinamide nucleotide transhydrogenase from man and mouse. Biochim Biophys Acta 1273(3):203-205.
13. Rangaraju V, Calloway N, Ryan TA (2014) Activity-driven local ATP synthesis is required for synaptic function. Cell 156(4):825-835.
14. Manoli I, et al. (2007) Mitochondria as key components of the stress response. Trends Endocrinol Metab 18(5):190-198.
15. McFarland R, Taylor RW, Turnbull DM (2010) A neurological perspective on mitochondrial disease. Lancet Neurol 9(8):829-840.
16. Wellen KE, et al. (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324(5930):1076-1080.
17. Schroeder EA, Raimundo N, Shadel GS (2013) Epigenetic silencing mediates mitochondria stress-induced longevity. Cell Metab 17(6):954-964.
18. Picard M, et al. (2014) Progressive increase in mtDNA 3243A>G heteroplasmy causes abrupt transcriptional reprogramming. Proc Natl Acad Sci USA 111(38):E4033-E4042.
19. Gut P, Verdin E (2013) The nexus of chromatin regulation and intermediary metabolism. Nature 502(7472):489-498.
20. Hunter RG, et al. (2012) Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc Natl Acad Sci USA 109(43):17657-17662.
21. Jeppesen TD, Orngreen MC, Van Hall G, Vissing J (2013) Lactate metabolism during exercise in patients with mitochondrial myopathy. Neuromuscul Disord 23(8):629-636.
22. Szendroedi J, Phielix E, Roden M (2012) The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol 8(2):92-103.
23. Pelletier M, Lepow TS, Billingham LK, Murphy MP, Siegel RM (2012) New tricks from an old dog: Mitochondrial redox signaling in cellular inflammation. Semin Immunol 24(6):384-392.
24. Zhang Q, et al. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464(7285):104-107.
25. Lin CS, et al. (2012) Mouse mtDNA mutant model of Leber hereditary optic neuropathy. Proc Natl Acad Sci USA 109(49):20065-20070.
26. Acín-Pérez R, et al. (2003) An intragenic suppressor in the cytochrome c oxidase I gene of mouse mitochondrial DNA. Hum Mol Genet 12(3):329-339.
27. Fan W, et al. (2008) A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319(5865):958-962.
28. Graham BH, et al. (1997) A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat Genet 16(3):226-234.
29. Nicholson A, et al. (2010) Diet-induced obesity in two C57BL/6 substrains with intact or mutant nicotinamide nucleotide transhydrogenase (Nnt) gene. Obesity (Silver Spring) 18(10):1902-1905.
30. Strauss KA, et al. (2013) Severity of cardiomyopathy associated with adenine nucleotide translocator-1 deficiency correlates with mtDNA haplogroup. Proc Natl Acad Sci USA 110(9):3453-3458.
31. Meimaridou E, et al. (2012) Mutations in NNT encoding nicotinamide nucleotide transhydrogenase cause familial glucocorticoid deficiency. Nat Genet 44(7):740-742.
32. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10(6):397-409.
33. Fergusson G, et al. (2014) Defective insulin secretory response to intravenous glucose in C57Bl/6J compared to C57Bl/6N mice. Mol Metab 3(9):848-854.
34. Dimsdale JE, Herd JA (1982) Variability of plasma lipids in response to emotional arousal. Psychosom Med 44(5):413-430.
35. Dimsdale JE, Moss J (1980) Plasma catecholamines in stress and exercise. JAMA 243(4):340-342.
36. Saudubray JM, Rabier D (2007) Biomarkers identified in inborn errors for lysine, arginine, and ornithine. J Nutr 137(6, Suppl 2):1669S-1672S.
37. Esposito K, et al. (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: Role of oxidative stress. Circulation 106(16):2067-2072.
38. Kado S, Nagase T, Nagata N (1999) Circulating levels of interleukin-6, its soluble receptor and interleukin-6/interleukin-6 receptor complexes in patients with type 2 diabetes mellitus. Acta Diabetol 36(1-2):67-72.
39. Bullitt E (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol 296(4):517-530.
40. Weiner H (1992) Perturbing the Organism: The Biology of Stressful Life Experience (Univ of Chicago Press, Chicago).
41. McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338(3):171-179.
42. Gorman GS, et al. (2015) Prevalence of nuclear and mtDNA mutations related to adult mitochondrial disease. Ann Neurol 77:753-759.
43. Koopman WJ, Willems PH, Smeitink JA (2012) Monogenic mitochondrial disorders. N Engl J Med 366(12):1132-1141.
44. Taivassalo T, et al. (2003) The spectrum of exercise tolerance in mitochondrial myopathies: A study of 40 patients. Brain 126(Pt 2):413-423.
45. Singh A, Petrides JS, Gold PW, Chrousos GP, Deuster PA (1999) Differential hypothalamicpituitary-adrenal axis reactivity to psychological and physical stress. J Clin Endocrinol Metab 84(6):1944-1948.
46. Morava E, Kozicz T (2013) Mitochondria and the economy of stress (mal) adaptation. Neurosci Biobehav Rev 37(4):668-680.
47. Gimsa U, Kanitz E, Otten W, Ibrahim SM (2009) Behavior and stress reactivity in mouse strains with mitochondrial DNA variations. Ann N Y Acad Sci 1153:131-138.
48. Sharpley MS, et al. (2012) Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell 151(2):333-343.
49. Faulenbach M, et al. (2012) Effect of psychological stress on glucose control in patients with Type 2 diabetes. Diabet Med 29(1):128-131.
50. DeSantis AS, Adam EK, Hawkley LC, Kudielka BM, Cacioppo JT (2015) Racial and ethnic differences in diurnal cortisol rhythms: Are they consistent over time? Psychosom Med 77(1):6-15.
51. Gómez-Durán A, et al. (2010) Unmasking the causes of multifactorial disorders: OXPHOS differences between mitochondrial haplogroups. Hum Mol Genet 19(17):3343-3353.
52. Bornstein SR, Engeland WC, Ehrhart-Bornstein M, Herman JP (2008) Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 19(5):175-180.
53. Meimaridou E, et al. (2013) ACTH resistance: Genes and mechanisms. Endocr Dev 24:57-66.
54. Wang TJ, et al. (2011) Metabolite profiles and the risk of developing diabetes. Nat Med 17(4):448-453.
55. Mapstone M, et al. (2014) Plasma phospholipids identify antecedent memory impairment in older adults. Nat Med 20(4):415-418.
56. Wallace DC (2013) A mitochondrial bioenergetic etiology of disease. J Clin Invest 123(4):1405-1412.
57. Sindi S, Fiocco AJ, Juster RP, Pruessner J, Lupien SJ (2013) When we test, do we stress? Impact of the testing environment on cortisol secretion and memory performance in older adults. Psychoneuroendocrinology 38(8):1388-1396.
58. Juster RP, Perna A, Marin MF, Sindi S, Lupien SJ (2012) Timing is everything: Anticipatory stress dynamics among cortisol and blood pressure reactivity and recovery in healthy adults. Stress 15(6):569-577.
59. Bandura A, Taylor CB, Williams SL, Mefford IN, Barchas JD (1985) Catecholamine secretion as a function of perceived coping self-efficacy. J Consult Clin Psychol 53(3):406-414.
60. Gonzalez-Bono E, Rohleder N, Hellhammer DH, Salvador A, Kirschbaum C (2002) Glucose but not protein or fat load amplifies the cortisol response to psychosocial stress. Horm Behav 41(3):328-333.
61. Armbruster D, et al. (2011) Predicting cortisol stress responses in older individuals: Influence of serotonin receptor 1A gene (HTR1A) and stressful life events. Horm Behav 60(1):105-111.
62. Hara Y, et al. (2014) Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc Natl Acad Sci USA 111(1):486-491.
63. Vos M, Lauwers E, Verstreken P (2010) Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease. Front Synaptic Neurosci 2(139):1-10.
64. Picard M, McEwen BS (2014) Mitochondria impact brain function and cognition. Proc Natl Acad Sci USA 111(1):7-8.
65. Courchet J, et al. (2013) Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 153(7):1510-1525.
66. Sun T, Qiao H, Pan PY, Chen Y, Sheng ZH (2013) Motile axonal mitochondria contribute to the variability of presynaptic strength. Cell Reports 4(3):413-419.
67. Olsen RH, Johnson LA, Zuloaga DG, Limoli CL, Raber J (2013) Enhanced hippocampusdependent memory and reduced anxiety in mice over-expressing human catalase in mitochondria. J Neurochem 125(2):303-313.
68. Knapman A, et al. (2012) Increased stress reactivity is associated with reduced hippocampal activity and neuronal integrity along with changes in energy metabolism. Eur J Neurosci 35(3):412-422.
69. Ye K, Lu J, Ma F, Keinan A, Gu Z (2014) Extensive pathogenicity of mitochondrial heteroplasmy in healthy human individuals. Proc Natl Acad Sci USA 111(29):10654-10659.
70. Booth FW, Laye MJ, Lees SJ, Rector RS, Thyfault JP (2008) Reduced physical activity and risk of chronic disease: The biology behind the consequences. Eur J Appl Physiol 102(4):381-390.
71. Picard M, Turnbull DM (2013) Linking the metabolic state and mitochondrial DNA in chronic disease, health, and aging. Diabetes 62(3):672-678.
72. Tyrka AR, et al. (2015) Alterations of mitochondrial DNA copy number and telomere length with early adversity and psychopathology. Biol Psychiatry, 10.1016/j.biopsych. 2014.12.025.
73. Cai N, et al. (2015) Molecular signatures of major depression. Curr Biol 25(9):1146-1156.
74. Su YA, et al.; Traumatic Stress Brain Study Group (2008) Dysregulated mitochondrial genes and networks with drug targets in postmortem brain of patients with posttraumatic stress disorder (PTSD) revealed by human mitochondria-focused cDNA microarrays. Int J Biol Sci 4(4):223-235.
75. Nasca C, et al. (2013) L-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc Natl Acad Sci USA 110(12):4804-4809.
76. Fisher-Wellman KH, et al. (2015) Pyruvate dehydrogenase complex and nicotinamide nucleotide transhydrogenase constitute an energy-consuming redox circuit. Biochem J 467(2):271-280.
77. Sorge RE, et al. (2014) Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat Methods 11(6):629-632.
78. Jones BN, Gilligan JP (1983) o-Phthaldialdehyde precolumn derivatization and reversed-phase high-performance liquid chromatography of polypeptide hydrolysates and physiological fluids. J Chromatogr A 266:471-482.
79. Nissim I, et al. (2012) Effects of a glucokinase activator on hepatic intermediary metabolism: Study with 13C-isotopomer-based metabolomics. Biochem J 444(3):537-551.
80. Huang ZH, et al. (1993) Characterization of N-ethoxycarbonyl ethyl esters of amino acids by mass spectrometry. J Chromatogr A 635(2):271-281.
81. Van De Merbel NC, et al. (2011) Quantitative determination of free and total dopamine in human plasma by LC-MS/MS: The importance of sample preparation. Bioanalysis 3(17):1949-1961.
82. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25(4):402-408.
83. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40 (Web Server issue):W127-133.