In vitro salicylate does not further impair aging-induced brain mitochondrial dysfunction

Toxicology

Volumn 302, Issue 1, 2012, Pages 51-59

  Marques Aleixo, I ^a   Rocha Rodrigues, S ^a   Santos Alves, E ^a   Coxito, P M ^b   Passos, E ^c   Oliveira, P J ^b   Magalhaes J ^a   Ascensao A ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c University of Porto   (Portugal)

Author keywords

Apoptosis; Brain mitochondria; Elderly; Oxidative damage; Salicylate toxicity

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE DIPHOSPHATE; BCL2 RELATED PROTEIN A1; CALCIUM; CYCLOPHILIN D; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEIN BAX; SALICYLIC ACID; THIOL DERIVATIVE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOENERGY; BRAIN MITOCHONDRION; BREATHING; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRIC POTENTIAL; IN VITRO STUDY; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING;

AGING; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BLOTTING, WESTERN; BRAIN; CALCIUM; ENERGY METABOLISM; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; RATS; RATS, WISTAR; SALICYLATES;

ANIMALIA; RATTUS NORVEGICUS;

EID: 84866002199     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.07.018     Document Type: Article

References (64)

1. Ascensao A., Magalhaes J., Soares J.M., Ferreira R., Neuparth M.J., Marques F., Oliveira P.J., Duarte J.A. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H722-H731.
2. Ascensao A., Lumini-Oliveira J., Machado N.G., Ferreira R.M., Goncalves I.O., Moreira A.C., Marques F., Sardao V.A., Oliveira P.J., Magalhaes J. Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats. Clin. Sci. (Lond) 2011, 120:37-49.
3. 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.
4. 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.
5. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005, 58:495-505.
6. Boveris A., Navarro A. Brain mitochondrial dysfunction in aging. IUBMB Life 2008, 60:308-314.
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. Brookes P.S. Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic. Biol. Med. 2005, 38:12-23.
10. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
11. Carreira R.S., Lee Y., Ghochani M., Gustafsson A.B., Gottlieb R.A. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 2010, 6.
12. Chabi B., Ljubicic V., Menzies K.J., Huang J.H., Saleem A., Hood D.A. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2008, 7:2-12.
13. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006, 125:1241-1252.
14. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341(Pt 2):233-249.
15. Csukly K., Ascah A., Matas J., Gardiner P.F., Fontaine E., Burelle Y. Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J. Physiol. 2006, 574:319-327.
16. De Cristobal J., Cardenas A., Lizasoain I., Leza J.C., Fernandez-Tome P., Lorenzo P., Moro M.A. Inhibition of glutamate release via recovery of ATP levels accounts for a neuroprotective effect of aspirin in rat cortical neurons exposed to oxygen-glucose deprivation. Stroke 2002, 33:261-267.
17. Dickstein D.L., Kabaso D., Rocher A.B., Luebke J.I., Wearne S.L., Hof P.R. Changes in the structural complexity of the aged brain. Aging Cell 2007, 6:275-284.
18. Dikshit P., Chatterjee M., Goswami A., Mishra A., Jana N.R. Aspirin induces apoptosis through the inhibition of proteasome function. J. Biol. Chem. 2006, 281:29228-29235.
19. Duncan G.W. The aging brain and neurodegenerative diseases. Clin. Geriatr. Med. 2011, 27:629-644.
20. Eliseev R.A., Filippov G., Velos J., VanWinkle B., Goldman A., Rosier R.N., Gunter T.E. Role of cyclophilin D in the resistance of brain mitochondria to the permeability transition. Neurobiol. Aging 2007, 28:1532-1542.
21. Estabrook R.W. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol. 1967, 10:41-57.
22. Fuster V., Sweeny J.M. Aspirin: a historical and contemporary therapeutic overview. Circulation 2011, 123:768-778.
23. Gilmer L.K., Ansari M.A., Roberts K.N., Scheff S.W. Age-related changes in mitochondrial respiration and oxidative damage in the cerebral cortex of the Fischer 344 rat. Mech. Ageing Dev. 2010, 131:133-143.
24. Giorgio V., Soriano M.E., Basso E., Bisetto E., Lippe G., Forte M.A., Bernardi P. Cyclophilin D in mitochondrial pathophysiology. Biochim. Biophys. Acta 2010, 1797:1113-1118.
25. Gornall A.G., Bardawill C.J., David M.M. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 1949, 177:751-766.
26. Head E., Nukala V.N., Fenoglio K.A., Muggenburg B.A., Cotman C.W., Sullivan P.G. Effects of age, dietary, and behavioral enrichment on brain mitochondria in a canine model of human aging. Exp. Neurol. 2009, 220:171-176.
27. Hoppins S., Lackner L., Nunnari J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 2007, 76:751-780.
28. Hu M.L. Measurement of protein thiol groups and GSH in plasma. Methods in Enzymology 1990, 380-385. Academic, San Diego, CA. L. Parker (Ed.).
29. Jastreboff P.J., Hansen R., Sasaki P.G., Sasaki C.T. Differential uptake of salicylate in serum, cerebrospinal fluid, and perilymph. Arch. Otolaryngol. Head Neck Surg. 1986, 112:1050-1053.
30. Knott A.B., Bossy-Wetzel E. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Ann. N.Y. Acad. Sci. 2008, 1147:283-292.
31. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
32. LaFrance R., Brustovetsky N., Sherburne C., Delong D., Dubinsky J.M. Age-related changes in regional brain mitochondria from Fischer 344 rats. Aging Cell 2005, 4:139-145.
33. Lemasters J.J., Nieminen A.L., Qian T., Trost L.C., Herman B. The mitochondrial permeability transition in toxic, hypoxic and reperfusion injury. Mol. Cell. Biochem. 1997, 174:159-165.
34. Lemasters J.J., Theruvath T.P., Zhong Z., Nieminen A.L. Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta 2009, 1787:1395-1401.
35. Locke M., Noble E.G., Atkinson B.G. Exercising mammals synthesize stress proteins. Am. J. Physiol. 1990, 258:C723-C729.
36. Matas J., Young N.T., Bourcier-Lucas C., Ascah A., Marcil M., Deschepper C.F., Burelle Y. Increased expression and intramitochondrial translocation of cyclophilin-d associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy. J. Mol. Cell. Cardiol. 2009, 46:420-430.
37. 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.
38. Melov S., Coskun P., Patel M., Tuinstra R., Cottrell B., Jun A.S., Zastawny T.H., Dizdaroglu M., Goodman S.I., Huang T.T., Miziorko H., Epstein C.J., Wallace D.C. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:846-851.
39. Mendelsohn A.R., Larrick J.W. Reversing age-related decline in working memory. Rejuvenation Res. 2011, 14:557-559.
40. Miwa S., Brand M.D. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochem. Soc. Trans. 2003, 31:1300-1301.
41. Miyahara J.T., Karler R. Effect of salicylate on oxidative phosphorylation and respiration of mitochondrial fragments. Biochem. J. 1965, 97:194-198.
42. Moreira P.I., Santos M.S., Moreno A., Oliveira C. Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci. Rep. 2001, 21:789-800.
43. Moreira P.I., Santos M.S., Moreno A.M., Seica R., Oliveira C.R. Increased vulnerability of brain mitochondria in diabetic (Goto-Kakizaki) rats with aging and amyloid-beta exposure. Diabetes 2003, 52:1449-1456.
44. Moreira P.I., Santos M.S., Sena C., Seica R., Oliveira C.R. Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol. Dis. 2005, 18:628-637.
45. Nadanaciva S., Will Y. Investigating mitochondrial dysfunction to increase drug safety in the pharmaceutical industry. Curr. Drug Targets 2011, 12:774-782.
46. Nadanaciva S., Will Y. New insights in drug-induced mitochondrial toxicity. Curr. Pharm. Des. 2011, 17:2100-2112.
47. Navarro A., Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol. 2007, 292:C670-C686.
48. Nulton-Persson A.C., Szweda L.I., Sadek H.A. Inhibition of cardiac mitochondrial respiration by salicylic acid and acetylsalicylate. J. Cardiovasc. Pharmacol. 2004, 44:591-595.
49. Oliveira P.J. Mitochondria as a drug target in health and disease. Curr. Drug Targets 2011, 12:761.
50. Oliveira A.M., Bading H. Calcium signaling in cognition and aging-dependent cognitive decline. Biofactors 2011, 37:168-174.
51. Pereira C.V., Moreira A.C., Pereira S.P., Machado N.G., Carvalho F.S., Sardao V.A., Oliveira P.J. Investigating drug-induced mitochondrial toxicity: a biosensor to increase drug safety?. Curr. Drug Saf. 2009, 4:34-54.
52. Pereira C.V., Nadanaciva S., Oliveira P.J., Will Y. The contribution of oxidative stress to drug-induced organ toxicity and its detection in vitro and in vivo. Expert. Opin. Drug Metab. Toxicol. 2012, 8:219-237.
53. Petrosillo G., Matera M., Casanova G., Ruggiero F.M., Paradies G. Mitochondrial dysfunction in rat brain with aging Involvement of complex I, reactive oxygen species and cardiolipin. Neurochem. Int. 2008, 53:126-131.
54. 2+-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R659-R668.
55. 2+ overload underlies Abeta oligomers neurotoxicity providing an unexpected mechanism of neuroprotection by NSAIDs. PLoS One 2008, 3:e2718.
56. Sardao V.A., Pereira S.L., Oliveira P.J. Drug-induced mitochondrial dysfunction in cardiac and skeletal muscle injury. Expert Opin. Drug Saf. 2008, 7:129-146.
57. Sen T., Sen N., Jana S., Khan F.H., Chatterjee U., Chakrabarti S. Depolarization and cardiolipin depletion in aged rat brain mitochondria: relationship with oxidative stress and electron transport chain activity. Neurochem. Int. 2007, 50:719-725.
58. Swerdlow R.H. Brain aging, Alzheimer's disease, and mitochondria. Biochim. Biophys. Acta 2011, 1812:1630-1639.
59. Toescu E.C. Normal brain ageing: models and mechanisms. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2005, 360:2347-2354.
60. Toman J., Fiskum G. Influence of aging on membrane permeability transition in brain mitochondria. J. Bioenerg. Biomembr. 2011, 43:3-10.
61. 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.
62. Tsaioun K., Bottlaender M., Mabondzo A. ADDME - avoiding drug development mistakes early: central nervous system drug discovery perspective. BMC Neurol. 2009, 9(Suppl. 1):S1.
63. Vainio H., Morgan G., Elwood P. The public health potential of aspirin. Pharmacol. Toxicol. 2002, 91:49-50.
64. Zoratti M., Szabo I., De Marchi U. Mitochondrial permeability transitions: how many doors to the house?. Biochim. Biophys. Acta 2005, 1706:40-52.