Acute stress delays brain mitochondrial permeability transition pore opening

Journal of Neurochemistry

Volumn 131, Issue 3, 2014, Pages 314-322

  Batandier, Cécile ^a,b   Poulet, Laurent ^a,b,c   Hininger, Isabelle ^a,b   Couturier, Karine ^a,b   Fontaine, Eric ^a,b   Roussel, Anne Marie ^a,b   Canini, Frédéric ^c,d  

^a UNIV GRENOBLE ALPES   (France)

^b INSERM   (France)

^c INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^d Ecole du Val de Grace   (France)

Author keywords

acute stress; AMPK; brain; complex I; mitochondria; PTP

Indexed keywords

CALCIUM ION; CYCLIC GMP DEPENDENT PROTEIN KINASE; GLUCOCORTICOID; GLYCOGEN SYNTHASE KINASE 3BETA; HEXOKINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); CALCIUM; CARRIER PROTEIN; CYCLIC GMP;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; IMMOBILIZATION STRESS; IN VITRO STUDY; MALE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; DRUG EFFECTS; MENTAL STRESS; METABOLISM; OXYGEN CONSUMPTION; PATHOLOGY; PERMEABILITY; PHYSIOLOGY; WISTAR RAT;

RATTUS;

ANIMALS; BRAIN; CALCIUM; CYCLIC GMP; GLUCOCORTICOIDS; MALE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXYGEN CONSUMPTION; PERMEABILITY; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84922243819     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12811     Document Type: Article

References (49)

1. Adzic M., Djordjevic A., Demonacos C., Krstic-Demonacos M., and, Radojcic M. B., (2009) The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats. Int. J. Biochem. Cell Biol. 41, 2181-2188.
2. Batandier C., Leverve X., and, Fontaine E., (2004) Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J. Biol. Chem. 279, 17197-17204.
3. Batandier C., Guigas B., Detaille D., El-Mir M. Y., Fontaine E., Rigoulet M., and, Leverve X. M., (2006) The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin. J. Bioenerg. Biomembr. 38, 33-42.
4. Bernardi P., (2013) The mitochondrial permeability transition pore: a mystery solved? Front. Physiol. 4, 95.
5. Bernardi P., and, von Stockum S., (2012) The permeability transition pore as a Ca(2+) release channel: new answers to an old question. Cell Calcium 52, 22-27.
6. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blachly-Dyson E., Di Lisa F., and, Forte M. A., (2006) The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 273, 2077-2099.
7. Buynitsky T., and, Mostofsky D. I., (2009) Restraint stress in biobehavioral research: recent developments. Neurosci. Biobehav. Rev. 33, 1089-1098.
8. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X., and, Fontaine E., (2001) Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J. Biol. Chem. 276, 41394-41398.
9. Chinta S. J., Rane A., Yadava N., Andersen J. K., Nicholls D. G., and, Polster B. M., (2009) Reactive oxygen species regulation by AIF- and complex I-depleted brain mitochondria. Free Radic. Biol. Med. 46, 939-947.
10. Drouet J. B., Fauvelle F., Batandier C., et al,. (2012) Metyrapone effects on systemic and cerebral energy metabolism. Eur. J. Pharmacol. 682, 92-98.
11. Du J., Wang Y., Hunter R., et al,. (2009) Dynamic regulation of mitochondrial function by glucocorticoids. Proc. Natl Acad. Sci. USA 106, 3543-3548.
12. Echeverry M. B., Guimaraes F. S., and, Del Bel E. A., (2004) Acute and delayed restraint stress-induced changes in nitric oxide producing neurons in limbic regions. Neuroscience 125, 981-993.
13. Fiskum G., Murphy A. N., and, Beal M. F., (1999) Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J. Cereb. Blood Flow Metab. 19, 351-369.
14. Fontaine E., Eriksson O., Ichas F., and, Bernardi P., (1998) Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex I. J. Biol. Chem. 273, 12662-12668.
15. Giorgio V., Soriano M. E., Basso E., Bisetto E., Lippe G., Forte M. A., and, Bernardi P., (2010) Cyclophilin D in mitochondrial pathophysiology. Biochim. Biophys. Acta 1797, 1113-1118.
16. Giorgio V., von Stockum S., Antoniel M., et al,. (2013) Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl Acad. Sci. USA 110, 5887-5892.
17. Gong Y., Chai Y., Ding J. H., Sun X. L., and, Hu G., (2011) Chronic mild stress damages mitochondrial ultrastructure and function in mouse brain. Neurosci. Lett. 488, 76-80.
18. Grimm S., and, Brdiczka D., (2007) The permeability transition pore in cell death. Apoptosis 12, 841-855.
19. Guigas B., Detaille D., Chauvin C., Batandier C., De Oliveira F., Fontaine E., and, Leverve X., (2004) Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study. Biochem. J. 382, 877-884.
20. Hatefi Y., (1978) Resolution of complex II and isolation of succinate dehydrogenase (EC 1.3.99.1). Methods Enzymol. 53, 27-35.
21. Hiramatsu R., and, Nisula B. C., (1991) Uptake of erythrocyte-associated component of blood testosterone and corticosterone to rat brain. J. Steroid Biochem. Mol. Biol. 38, 383-387.
22. Joels M., and, Karst H., (2012) Corticosteroid effects on calcium signaling in limbic neurons. Cell Calcium 51, 277-283.
23. Krolow R., Noschang C., Weis S. N., et al,. (2012) Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex. Neurochem. Res. 37, 1063-1073.
24. Kuchukashvili Z., Burjanadze G., Menabde K., Chachua M., Dachanidze N., Mikadze M., and, Koshoridze N., (2012) Long-lasting stress, quantitative changes in nitric oxide concentration and functional state of brain mitochondria. Acta Neurobiol. Exp. 72, 40-50.
25. Lablanche S., Cottet-Rousselle C., Lamarche F., Benhamou P. Y., Halimi S., Leverve X., and, Fontaine E., (2011) Protection of pancreatic INS-1 beta-cells from glucose- and fructose-induced cell death by inhibiting mitochondrial permeability transition with cyclosporin A or metformin. Cell Death Dis. 2, e134.
26. Li B., Chauvin C., De Paulis D., et al., (2012) Inhibition of complex I regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D. Biochim Biophys Acta. 1817, 1628-1634.
27. Liu Y., Fiskum G., and, Schubert D., (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787.
28. Lucca G., Comim C. M., Valvassori S. S., Reus G. Z., Vuolo F., Petronilho F., Gavioli E. C., Dal-Pizzol F., and, Quevedo J., (2009) Increased oxidative stress in submitochondrial particles into the brain of rats submitted to the chronic mild stress paradigm. J. Psychiatr. Res. 43, 864-869.
29. Manoli I., Alesci S., Blackman M. R., Su Y. A., Rennert O. M., and, Chrousos G. P., (2007) Mitochondria as key components of the stress response. Trends Endocrinol. Metab. 18, 190-198.
30. Marissal-Arvy N., Batandier C., Dallennes J., et al,. (2014) Effect of a high-fat-high-fructose diet, stress and cinnamon on central expression of genes related to immune system, hypothalamic-pituitary-adrenocortical axis function and cerebral plasticity in rats. Br. J. Nutr. 111, 1190-1201.
31. Marques M. B., Ribeiro-Oliveira A., Jr, Guimaraes J., et al,. (2012) Modifications in basal and stress-induced hypothalamic AMP-activated protein kinase (AMPK) activity in rats chronically treated with an angiotensin II receptor blocker. Stress 15, 554-561.
32. Nicholls D. G., and, Budd S. L., (2000) Mitochondria and neuronal survival. Physiol. Rev. 80, 315-360.
33. National Institutes of Health (1985) Guide of the care and use of laboratory animals-NIH publication no. 86-23.
34. Pal R., Gulati K., Chakraborti A., Banerjee B., and, Ray A., (2006) Role of free radicals in stress-induced neurobehavioural changes in rats. Indian J. Exp. Biol. 44, 816-820.
35. Pastorino J. G., and, Hoek J. B., (2008) Regulation of hexokinase binding to VDAC. J. Bioenerg. Biomembr. 40, 171-182.
36. 2+)-dependent apoptosis and necrosis. Cell Calcium 50, 222-233.
37. Rasola A., Sciacovelli M., Pantic B., and, Bernardi P., (2010) Signal transduction to the permeability transition pore. FEBS Lett. 584, 1989-1996.
38. Rezin G. T., Cardoso M. R., Goncalves C. L., Scaini G., Fraga D. B., Riegel R. E., Comim C. M., Quevedo J., and, Streck E. L., (2008) Inhibition of mitochondrial respiratory chain in brain of rats subjected to an experimental model of depression. Neurochem. Int. 53, 395-400.
39. Rezin G. T., Amboni G., Zugno A. I., Quevedo J., and, Streck E. L., (2009) Mitochondrial dysfunction and psychiatric disorders. Neurochem. Res. 34, 1021-1029.
40. Rizzuto R., De Stefani D., Raffaello A., and, Mammucari C., (2012) Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 13, 566-578.
41. Ronnett G. V., Ramamurthy S., Kleman A. M., Landree L. E., and, Aja S., (2009) AMPK in the brain: its roles in energy balance and neuroprotection. J. Neurochem. 109 (Suppl. 1), 17-23.
42. Rosenthal R. E., Hamud F., Fiskum G., Varghese P. J., and, Sharpe S., (1987) Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J. Cereb. Blood Flow Metab. 7, 752-758.
43. Sanches D. B., Carnio E. C., and, Branco L. G. S., (2003) Central nNOS is involved in restraint stress-induced fever: evidence for a cGMP pathway. Physiol. Behav. 80, 139-145.
44. Schapira A. H., (2008) Mitochondrial dysfunction in neurodegenerative diseases. Neurochem. Res. 33, 2502-2509.
45. Schapira A. H., (2010) Complex I: inhibitors, inhibition and neurodegeneration. Exp. Neurol. 224, 331-335.
46. Scheer W. D., Lehmann H. P., and, Beeler M. F., (1978) An improved assay for hexokinase activity in human tissue homogenates. Anal. Biochem. 91, 451-463.
47. Stiles B. L., (2009) PI-3-K and AKT: onto the mitochondria. Adv. Drug Deliv. Rev. 61, 1276-1282.
48. Subramaniam S., and, Unsicker K., (2010) ERK and cell death: ERK1/2 in neuronal death. FEBS J. 277, 22-29.
49. Zorov D. B., Juhaszova M., Yaniv Y., Nuss H. B., Wang S., and, Sollott S. J., (2009) Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc. Res. 83, 213-225.