Endurance training and chronic intermittent hypoxia modulate in vitro salicylate-induced hepatic mitochondrial dysfunction

Mitochondrion

Volumn 12, Issue 6, 2012, Pages 607-616

  Ascensao A ^a   Goncalves I O ^a   Lumini Oliveira, J ^a,b   Marques Aleixo, I ^a   dos Passos, E ^a   Rocha Rodrigues, S ^a   Machado, N G ^c   Moreira, A C ^c   Oliveira, P J ^c   Torrella, J R ^d   Magalhaes J ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Fernando Pessoa   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Bioenergetics; Exercise; Intermittent hypoxia; Liver; Mitochondrial toxicity; Salicylate

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE DIPHOSPHATE; CALCIUM ION; CASPASE 3; CASPASE 8; CYCLOPHILIN D; HEAT SHOCK PROTEIN 70; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; SALICYLIC ACID; SIRTUIN 3; THIOL GROUP;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATMOSPHERIC PRESSURE; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DOWN REGULATION; ENDURANCE TRAINING; ENZYME ACTIVITY; IN VITRO STUDY; LIVER MITOCHONDRION; LIVER TOXICITY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TOXICITY; MITOCHONDRION SWELLING; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT; TREADMILL EXERCISE;

ANIMALS; ANOXIA; LIVER; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OXYGEN CONSUMPTION; PHYSICAL CONDITIONING, ANIMAL; RATS; SALICYLATES;

RATTUS;

EID: 84869082628     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.10.007     Document Type: Article

References (52)

1. Ascensao A., Ferreira R., Magalhaes J. Exercise-induced cardioprotection - biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int. J. Cardiol. 2007, 117:16-30.
2. Ascensao A., Lumini-Oliveira J., Oliveira P.J., Magalhaes J. Mitochondria as a target for exercise-induced cardioprotection. Curr. Drug Targets 2011, 12:860-871.
3. Ascensao A., Oliveira P.J., Magalhaes J. Exercise as a beneficial adjunct therapy during doxorubicin treatment-role of mitochondria in cardioprotection. Int. J. Cardiol. 2011, 156:4-10.
4. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
5. Battaglia V., Salvi M., Toninello A. Oxidative stress is responsible for mitochondrial permeability transition induction by salicylate in liver mitochondria. J. Biol. Chem. 2005, 280:33864-33872.
6. Begriche K., Igoudjil A., Pessayre D., Fromenty B. Mitochondrial dysfunction in NASH: causes, consequences and possible means to prevent it. Mitochondrion 2006, 6:1-28.
7. Boveris A., Navarro A. Systemic and mitochondrial adaptive responses to moderate exercise in rodents. Free Radic. Biol. Med. 2008, 44:224-229.
8. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochem. J. 2011, 435:297-312.
9. Broekemeier K.M., Pfeiffer D.R. Cyclosporin A-sensitive and insensitive mechanisms produce the permeability transition in mitochondria. Biochem. Biophys. Res. Commun. 1989, 163:561-566.
10. Brookes P.S. Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic. Biol. Med. 2005, 38:12-23.
11. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
12. Charnock J.S., Opit L.J. The effect of salicylate on adenosine-triphosphatase activity of rat-liver mitochondria. Biochem. J. 1962, 83:596-602.
13. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341(Pt 2):233-249.
14. Daussin F.N., Godin R., Ascah A., Deschenes S., Burelle Y. Cyclophilin-D is dispensable for atrophy and mitochondrial apoptotic signalling in denervated muscle. J. Physiol. 2011, 589:855-861.
15. Dong J.W., Zhu H.F., Zhu W.Z., Ding H.L., Ma T.M., Zhou Z.N. Intermittent hypoxia attenuates ischemia/reperfusion induced apoptosis in cardiac myocytes via regulating Bcl-2/Bax expression. Cell Res. 2003, 13:385-391.
16. Estabrook R. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol. 1967, 10:41-47.
17. Fontaine E., Eriksson O., Ichas F., Bernardi P. Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex i. J. Biol. Chem. 1998, 273:12662-12668.
18. Gauthier M.S., Couturier K., Latour J.G., Lavoie J.M. Concurrent exercise prevents high-fat-diet-induced macrovesicular hepatic steatosis. J. Appl. Physiol. 2003, 94:2127-2134.
19. Gauthier M.S., Couturier K., Charbonneau A., Lavoie J.M. Effects of introducing physical training in the course of a 16-week high-fat diet regimen on hepatic steatosis, adipose tissue fat accumulation, and plasma lipid profile. Int. J. Obes. Relat. Metab. Disord. 2004, 28:1064-1071.
20. Gutknecht J. Salicylates and proton transport through lipid bilayer membranes: a model for salicylate-induced uncoupling and swelling in mitochondria. J. Membr. Biol. 1990, 115:253-260.
21. Halestrap A.P., Clarke S.J., Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc. Res. 2004, 61:372-385.
22. Hochman J.S., Shah N.R. What price pain relief?. Circulation 2006, 113:2868-2870.
23. Hu M.-L. Measurement of protein thiol groups and GSH in plasma. Methods in Enzymology 1990, 380-385. Academic Press, San Diego. L. Parker (Ed.).
24. Johnson N.A., George J. Fitness versus fatness: moving beyond weight loss in nonalcoholic fatty liver disease. Hepatology 2010, 52:370-381.
25. Juby A.G., Davis P. Utility of published guidelines on the use of nonsteroidal anti-inflammatory drugs in the elderly. Clin. Rheumatol. 2008, 27:1191-1194.
26. Kamo N., Muratsugu M., Hongoh R., Kobatake Y. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 1979, 49:105-121.
27. Kolar F., Jezkova J., Balkova P., Breh J., Neckar J., Novak F., Novakova O., Tomasova H., Srbova M., Ost'adal B., Wilhelm J., Herget J. Role of oxidative stress in PKC-delta upregulation and cardioprotection induced by chronic intermittent hypoxia. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H224-H230.
28. Krebs H.A., Holzach O. The conversion of citrate into cis-aconitate and isocitrate in the presence of aconitase. Biochem. J. 1952, 52:527-528.
29. Labbe G., Pessayre D., Fromenty B. Drug-induced liver injury through mitochondrial dysfunction: mechanisms and detection during preclinical safety studies. Fundam. Clin. Pharmacol. 2008, 22:335-353.
30. Li X., Kazgan N. Mammalian sirtuins and energy metabolism. Int. J. Biol. Sci. 2011, 7:575-587.
31. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998, 94:491-501.
32. Lumini-Oliveira J., Magalhaes J., Pereira C.V., Moreira A.C., Oliveira P.J., Ascensao A. Endurance training reverts heart mitochondrial dysfunction, permeability transition and apoptotic signaling in long-term severe hyperglycemia. Mitochondrion 2011, 11:54-63.
33. Matiello R., Fukui R.T., Silva M.E., Rocha D.M., Wajchenberg B.L., Azhar S., Santos R.F. Differential regulation of PGC-1alpha expression in rat liver and skeletal muscle in response to voluntary running. Nutr. Metab. (Lond.) 2010, 7:36.
34. McCommis K.S., McGee A.M., Laughlin M.H., Bowles D.K., Baines C.P. Hypercholesterolemia increases mitochondrial oxidative stress and enhances the MPT response in the porcine myocardium: beneficial effects of chronic exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:R1250-R1258.
35. Miwa S., Brand M.D. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochem. Soc. Trans. 2003, 31:1300-1301.
36. Navarro A., Gomez C., Lopez-Cepero J.M., Boveris A. Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R505-R511.
37. Nguyen T.T., Stevens M.V., Kohr M., Steenbergen C., Sack M.N., Murphy E. Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J. Biol. Chem. 2011, 286:40184-40192.
38. Oh K.W., Qian T., Brenner D.A., Lemasters J.J. Salicylate enhances necrosis and apoptosis mediated by the mitochondrial permeability transition. Toxicol. Sci. 2003, 73:44-52.
39. Oliveira P.J. Mitochondria as a drug target in health and disease. Curr. Drug Targets 2011, 12:761.
40. Quiles J.L., Huertas J.R., Manas M., Ochoa J.J., Battino M., Mataix J. Dietary fat type and regular exercise affect mitochondrial composition and function depending on specific tissue in the rat. J. Bioenerg. Biomembr. 2001, 33:127-134.
41. Romijn J.A., Pijl H. The muscle-liver axis: does aerobic fitness induce intrahepatic protection against non-alcoholic fatty liver disease?. J. Physiol. 2009, 587:1637.
42. Singh S.N., Vats P., Kumria M.M., Ranganathan S., Shyam R., Arora M.P., Jain C.L., Sridharan K. Effect of high altitude (7,620m) exposure on glutathione and related metabolism in rats. Eur. J. Appl. Physiol. 2001, 84:233-237.
43. Sun L., Shen W., Liu Z., Guan S., Liu J., Ding S. Endurance exercise causes mitochondrial and oxidative stress in rat liver: effects of a combination of mitochondrial targeting nutrients. Life Sci. 2010, 86:39-44.
44. Terblanche S.E., Gohil K., Packer L., Henderson S., Brooks G.A. The effects of endurance training and exhaustive exercise on mitochondrial enzymes in tissues of the rat (Rattus norvegicus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 128:889-896.
45. Thyfault J.P., Rector R.S., Uptergrove G.M., Borengasser S.J., Morris E.M., Wei Y., Laye M.J., Burant C.F., Qi N.R., Ridenhour S.E., Koch L.G., Britton S.L., Ibdah J.A. Rats selectively bred for low aerobic capacity have reduced hepatic mitochondrial oxidative capacity and susceptibility to hepatic steatosis and injury. J. Physiol. 2009, 587:1805-1816.
46. Trost L.C., Lemasters J.J. The mitochondrial permeability transition: a new pathophysiological mechanism for Reye's syndrome and toxic liver injury. J. Pharmacol. Exp. Ther. 1996, 278:1000-1005.
47. Trost L.C., Lemasters J.J. Role of the mitochondrial permeability transition in salicylate toxicity to cultured rat hepatocytes: implications for the pathogenesis of Reye's syndrome. Toxicol. Appl. Pharmacol. 1997, 147:431-441.
48. Urdampilleta A., Gonzalez-Muniesa P., Portillo M.P., Martinez J.A. Usefulness of combining intermittent hypoxia and physical exercise in the treatment of obesity. J. Physiol. Biochem. 2012, 68:289-304.
49. Van Norman K.H. The Biuret reaction and the cold nitric acid test in the recognition of protein. Biochem. J. 1909, 4:127-135.
50. Verdin E., Hirschey M.D., Finley L.W., Haigis M.C. Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35:669-675.
51. Wu K.K. Biochemical pharmacology of nonsteroidal anti-inflammatory drugs. Biochem. Pharmacol. 1998, 55:543-547.
52. Xu W.Q., Yu Z., Xie Y., Huang G.Q., Shu X.H., Zhu Y., Zhou Z.N., Yang H.T. Therapeutic effect of intermittent hypobaric hypoxia on myocardial infarction in rats. Basic Res. Cardiol. 2011, 106:329-342.