The potential role of ozone in ameliorating the age-related biochemical changes in male rat cerebral cortex

Biogerontology

Volumn 13, Issue 6, 2012, Pages 565-581

  Shehata, Nagwa Ibrahim ^a   Abd Elgawad, Hanan Mohamed ^a   Mawsouf, Mohamed Nabil ^b   Shaheen, Amira Abd Elmonem ^a  

^a CAIRO UNIVERSITY   (Egypt)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

Aging; Cerebral cortex; Mitochondria; Oxidative preconditioning; Ozone therapy

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; GLUTATHIONE; MALONALDEHYDE; NEUROPROTECTIVE AGENT; NITRIC OXIDE SYNTHASE; OZONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE DISMUTASE; UBIQUINONE; ADENINE NUCLEOTIDE; LIPOFUSCIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME ASSAY; FLUORESCENCE; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; OZONE THERAPY; PRIORITY JOURNAL; RAT; SUBMITOCHONDRIAL PARTICLE; ANIMAL; DOSE RESPONSE; DRUG ADMINISTRATION; DRUG EFFECT; ENERGY METABOLISM; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN CARBONYLATION; WISTAR RAT;

ADENINE NUCLEOTIDES; AGING; ANIMALS; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; GLUTATHIONE; LIPOFUSCIN; MALE; MALONDIALDEHYDE; MITOCHONDRIAL MEMBRANES; NITRIC OXIDE SYNTHASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; OZONE; PROTEIN CARBONYLATION; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 84878249768     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-012-9400-9     Document Type: Article

References (89)

1. Abd-Elmohsen MM, Iravani MM, Spencer JPE, Rose S, Fahim AT, Motawi TMK, Ismail NAF, Jenner P (2005) Age-associated changes in protein oxidation and proteasome activities in rat brain: modulation by antioxidants. Biochem Biophys Res Commun 336:386-391
2. Ajamieh HH, Menendez S, Martinez-Sanchez G, Candelario-Jalil E, Re L, Giuliani A, Fernandez OSL (2004) Effects of ozone oxidative preconditioning on nitric oxide generation and cellular redox balance in a rat model of hepatic ischaemia-reperfusion. Liver Int 24:55-62
3. Ajamieh HH, Berlanga J, Merino N, Sanchez GM, Carmona AM, Cepero SM, Giuliani A, Re L, Leon OS (2005) Role of protein synthesis in the protection conferred by ozone-oxidative-preconditioning in hepatic ischaemia/reperfusion. Transpl Int 18:604-612
4. Altinel O, Demirbas S, Cakir E, Yaman H, Ozerhan IH, Duran E, Cayci T, Akgul EO, Ersoz N, Uysal B, Kurt B, Yasar M, Oter S, Peker Y (2011) Comparison of hyperbaric oxygen and medical ozone therapies in a rat model of experimental distal colitis. Scand J Clin Lab Invest 71:185-192
5. Antonelli ML, Curini R, Curtis SA, Palladini G (2000) ATPase Na, K-dependent activity and water matrix interactions in cerebella of aged mice. Thermochim Acta 364:155-163
6. Arivazhagan P, Panneerselvam C (2004) Alpha-lipoic acid increases Na, K-ATPase activity and reduces lipofuscin accumulation in discrete brain regions of aged rats. Ann N Y Acad Sci 1019:350-354
7. Aureli T, Miccheli A, Ricciolini R, Di Cocco ME, Ramacci MT, Angelucci L, Ghirardi O, Conti F (1990) Aging brain: effect of acetyl-l-carnitin treatment on rat brain energy and phospholipid metabolism. A study by 31P and 1H NMR spectroscopy. Brain Res 526:108-112
8. Bala K, Tripathy BC, Sharma D (2006) Neuroprotective and anti-aging effects of curcumin in aged rat brain regions. Biogerontology 7:81-89
9. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483-495
10. Benzi C, Moretti A (1995) Age- and peroxidative stress-related modifications of the cerebral enzymic activities linked to mitochondria and the glutathione system. Free Radic Biol Med 19:77-101
11. Bocci V (1996a) Does ozone therapy normalize the cellular redox balance? Med Hypotheses 46:150-154
12. Bocci V (1996b) Ozone as a bioregulator. Pharmacology and toxicology of ozone therapy today. J Biol Regul Homeost Agents 10:31-53
13. Bocci V (2005) Ozone: A new medical drug. Springer, Dordrecht
14. Bocci V (2006) Scientific and medical aspects of ozone therapy. State of the art. Arch Med Res 37:425-435
15. Bocci V, Borrelli E, Corradeschi F, Valacchi G (2000) Systemic effects after colorectal insufflation of oxygen-ozone in rabbits. Int J Med Biol Environ 28:109-113
16. Bocci V, Aldinucci C, Mosci F, Carraro F, Valacchi G (2007) Ozonation of human blood induces a remarkable upregulation of heme oxygenase-1 and heat stress protein-70. Mediat Inflamm 2007:267-285
17. Bocci V, Borrelli E, Travagli V, Zanardi I (2009) The ozone paradox: ozone is a strong oxidant as well as a medical drug. Med Res Rev 29:646-682
18. Bocci V, Zanardi L, Travagli V (2011) Ozone acting on human blood yields a hormetic dose-response relationship. J Transl Med 9:66-76
19. Bogatskaia LN, Potapenko RI (1984) Effect of vasopressin on energy metabolism of the brain in adult and aged rats. Vopr Med Khim 30:106-110
20. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302-310
21. Bustamante J, Czerniczyniec A, Cymeryng C, Lores-Arnaiz S (2008) Age-related changes from youth to adulthood in rat brain cortex: nitric oxide synthase and mitochondrial respiratory function. Neurochem Res 33:1216-1223
22. Calabrese V, Spadaro F, Dinotta F, Ravagna A, Randazzo F, Randazzo G, Ragusa N, Rizza V (1998) Long-term ethanol administration enhances urinary ultraweak luminescence and age-dependent modulation of redox in central and peripheral organs of the rat. Int J Tissue React 20:57-62
23. Candelario-Jalil E, Al-Dalain SM, Leon OS, Menendez S, Perez-Davidson G, Merino N (2001) Oxidative preconditioning affords protection against carbon tetrachloride-induced glycogen depletion and oxidative stress in rats. J Appl Toxicol 21:297-301
24. Carrillo MC, Kanai S, Sato Y, Kitani K (1992) Age-related changes in antioxidant enzyme activities are region and organ, as well as sex, selective in the rat. Mech Ageing Dev 65:187-198
25. Chen H, Xing B, Liu X, Zhan B, Zhou J, Zhu H, Chen Z (2008) Similarities between ozone oxidative preconditioning and ischemic preconditioning in renal ischemia-reperfusion injury. Arch Med Res 39:169-178
26. Chiueh CC, Andoh T, Chock PB (2005) Induction of thioredoxin and mitochondrial survival proteins mediates preconditioning-induced cardioprotection and neuroprotection. Ann N Y Acad Sci 1042:403-418
27. Danh HC, Strolin-Benedetti M, Dostert P (1983) Differential changes in superoxide dismutase activity in brain and liver of old rats and mice. J Neurochem 40:1003-1007
28. Dubey A, Forster MJ, Lal H, Sohal RS (1996) Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Arch Biochem Biophys 333:189-197
29. Dufour E, Larsson NG (2004) Understanding aging: revealing order out of chaos. Biochim Biophys Acta 1658:122-132
30. El-Sawalhi MM, Darwish HA, Shaheen AA, Mausouf MN (2006) Effect of ozone oxidative preconditioning on oxidative status of adjuvant arthritic rats. Egypt J Biochem Mol Biol 24:357-372
31. Fukagawa NK (1999) Aging: is oxidative stress a marker or is it causal? Proc Soc Exp Biol Med 222:293-298
32. Genova ML, Pich MM, Bernacchia A, Bianchi C, Biondi A, Bovina C, Falasca AI, Formiggini G, Castelli GP, Lenaz G (2004) The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann N Y Acad Sci 1011:86-100
33. Ghafourifar P, Richter C (1997) Nitric oxide synthase activity in mitochondria. FEBS Lett 418:291-296
34. Gnaiger E, Lassnig B, Kuznetsov AV, Margreiter R (1998) Mitochondrial respiration in the low oxygen environment of the cell. Effect of ADP on oxygen kinetics. Biochim Biophys Acta 1365:249-254
35. Gonzalez R, Borrego A, Zamora Z, Romay C, Hernandez F, Menendez S, Montero T, Rojas E (2004) Reversion by ozone treatment of acute nephrotoxicity induced by cisplatin in rats. Mediat Inflamm 13:307-312
36. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207-212
37. Guanche D, Hernandez F, Zamora Z, Alonso Y (2010) Effect of ozone preconditioning on redox activity in a rat model of septic shock. Toxicol Mech Methods 20:466-471
38. Guevara R, Santandreu FM, Valle A, Gianotti M, Oliver J, Roca P (2009) Sex-dependent differences in aged rat brain mitochondrial function and oxidative stress. Free Radic Biol Med 46:169-175
39. Guevara R, Gianotti M, Roca P, Oliver J (2011) Age and sex-related changes in rat brain mitochondrial function. Cell Physiol Biochem 27:201-206
40. Gupta A, Hasan M, Chander R, Kapoor NK (1991) Age-related elevation of lipid peroxidation products: diminution of superoxide dismutase activity in the central nervous system of rats. Gerontology 37:305-309
41. Guven A, Gundogdu G, Sadir S, Topal T, Erdogan E, Korkmaz A, Surer I, Ozturk H (2008) The efficiency of ozone therapy in experimental caustic esophageal burn. J Pediatr Surg 43:1679-1684
42. Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18:685-716
43. Haynes V, Elfering SL, Squires RJ, Traaseth N, Solien J, Ettl A, Giulivi C (2003) Mitochondrial nitric oxide synthase: role in pathophysiology. IUBMB Life 55:599-603
44. Hiramatsu M, Kohno M, Edamatsu R, Mitsuda K, Mori A (1992) Increased superoxide dismutase activity in human cerebrospinal fluid and rat brain with age by electron spin resonance spectrometry using the spin trap method. J Neurochem 58:1160-1164
45. Huertas JR, Battino M, Lenaz G, Mataix FJ (1991) Changes in mitochondrial and microsomal rat liver coenzyme Q9 and CoQ10 content induced by dietary fat and endogenous lipid peroxidation. FEBS Lett 287:89-92
46. Iantomasi T, Favilli F, Marraccini P, Stio M, Treves C, Quattrone A, Capaccioli S, Vincenzini MT (1993) Age and GSH metabolism in rat cerebral cortex, as related to oxidative and energy parameters. Mech Ageing Dev 70:65-82
47. Iles KE, Liu RM (2005) Mechanisms of glutamate cysteine ligase (GCL) induction by 4-hydroxynonenal. Free Radic Biol Med 38:547-556
48. Jesko H, Chalimoniuk M, Strosznajder JB (2003) Activation of constitutive nitric oxide synthase(s) and absence of inducible isoform in aged rat brain. Neurochem Int 42:315-322
49. Kaur J, Sharma D, Singh R (1998) Regional effects of aging on Na,K-ATPase activity in rat brain and correlation with multiple unit action potentials and lipid peroxidation. Indian J Biochem Biophys 35:364-371
50. Keller JN, Dimayuga E, Chen Q, Thorpe J, Gee J, Ding Q (2004) Autophagy, proteasomes, lipofuscin and oxidative stress in the aging brain. Int J Biochem Cell Biol 36:2376-2391
51. Knapowski J, Wieczorowska-Tobis K, Witowski J (2002) Pathophysiology of aging. J Physiol Pharmacol 53:135-146
52. Leon OS, Menendez S, Merino N, Castillo R, Sam S, Perez L, Cruz E, Bocci V (1998) Ozone oxidative preconditioning: protection against cellular damage by free radicals. Mediators Inflamm 7:289-294
53. Liu R, Choi J (2000) Age-associated decline in gamma-glutamylcysteine synthetase gene expression in rats. Free Radic Biol Med 28:566-574
54. Liu R, Liu IY, Bi X, Thompson RF, Doctrow SR, Malfroy B (2003) Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. Proc Natl Acad Sci USA 100:8526-8531
55. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
56. Lowry OH, Passonneau JV, Hasselberger FX, Schulz DW (1964) Effect of ischemia on known substances and cofactors of the glycolytic pathways in brain. J Biol Chem 239:18-30
57. Luo J, Robinson JP, Shi R (2005) Acrolein-induced cell death in PC 12 cells. Neurochem Int 47:449-457
58. Madej P, Plewka A, Madej JA, Nowak M, Plewka D, Franik G, Golka D (2007) Ozonotherapy in an induced septic shock. I. Effect of ozonotherapy on rat organs in evaluation of free radical reactions and selected enzymatic systems. Inflammation 30:52-58
59. Maines MD (1997) The heme oxygenase system: a regulator of second messenger genes. Annu Rev Pharmacol Toxicol 37:517-554
60. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autooxidation of pyrogallol and convenient assay for superoxide dismutase. Eur J Biochem 47:469-474
61. Martin H, Mcllwain H (1959) Glutathione, oxidized and reduced, in the brain and in isolated cerebral tissue. Biochem J 71:275-280
62. Martinez M, Hernandez AI, Martinez N (2000) N-acetylcysteine delays age-associated memory impairment in mice: role in synaptic mitochondria. Brain Res 855:100-106
63. Martinez-Sanchez G, Perez-Davison G, Re L, Giuliani A (2011) Ozone as U-shaped dose responses molecules (hormetins). Dose Response 9:32-49
64. Matchett GA, Martin RD, Zhang JH (2009) Hyperbaric oxygen therapy and cerebral ischemia: neuroprotective mechanisms. Neurol Res 31:114-121
65. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 34:609-616
66. Mrsic-Pelcic J, Pelcic G, Vitezic D, Antoncic I, Filipovic T, Simonic A, Zupan G (2004) Hyperbaric oxygen treatment: the influence on the hippocampal superoxide dismutase and Na,K-ATPase activities in global cerebral ischemia-exposed rats. Neurochem Int 44:585-594
67. Navarro A, Boveris A (2004) Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am J Physiol 287:R1244-R1249
68. Navarro A, Boveris A (2010) Brain mitochondrial dysfunction in aging, neurodegeneration and Parkinson's disease. Front Aging Neurosci 2:1-11
69. Navarro A, Gomez C, Sanchez-Pino MJ, Gonzalez H, Bandez MJ, Boveris AD, Boveris A (2005) Vitamin E at high doses improves survival, neurological performance, and brain mitochondrial function in aging male mice. Am J Physiol 289:R1392-R1399
70. Niu KC, Lin MT, Chang CP (2007) Hyperbaric oxygen improves survival in heatstroke rats by reducing multiorgan dysfunction and brain oxidative stress. Eur J Pharmacol 569:94-102
71. Oenzil F, Kishikawa M, Mizuno T, Nakano M (1994) Age-related accumulation of lipofuscin in three different regions of rat brain. Mech Ageing Dev 76:157-163
72. Ojaimi J, Masters CL, Opeskin K, Mckelvie P, Byrne E (1999) Mitochondrial respiratory chain activity in the human brain as a function of age. Mech Ageing Dev 111:39-47
73. Ostrowski RP, Tang J, Zhang JH (2006) Hyperbaric oxygen suppresses NADPH oxidase in a rat subarachnoid hemorrhage model. Stroke 47:1314-1318
74. Post RL, Sen AK (1967) Sodium and potassium-stimulated ATPase. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 10. Academic Press, New York, pp 762-768
75. Rangaraj N, Kalant H (1978) Effects of ethanol withdrawal, stress and amphetamine on rat brain Na,K-ATPase. Biochem Pharmacol 27:1139-1144
76. Rattan SIS, Fernandes RA, Demirovic D, Dymek B, Lima CF (2009) Heat stress and hormetin-induced hormesis in human cells: effects on aging, wound healing, angiogenesis and differentiation. Dose Response 7:90-103
77. Re L, Mawsouf MN, Menendez S, Leon OS, Sanchez GM, Hernandez F (2008) Ozone therapy: clinical and basic evidence of its therapeutic potential. Arch Med Res 39:17-26
78. Rebrin I, Kamzalov S, Sohal RS (2003) Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med 35:626-635
79. Sen T, Sen N, Jana S, Khan FH, Chatterjee U, Chakrabarti S (2007) Depolarization and cardiolipin depletion in aged rat brain mitochondria: relationship with oxidative stress and electron transport chain activity. Neurochem Int 50:719-725
80. Sharman EH, Bondy SC (2001) Effects of age and dietary antioxidants on cerebral electron transport chain activity. Neurobiol Aging 22:629-634
81. Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, Markesbery WR (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci USA 88:10540-10543
82. Subathra M, Shila S, Devi MA, Panneerselvam C (2005) Emerging role of Centella asiatica in improving age-related neurological antioxidant status. Exp Gerontol 40:707-715
83. Tang X, Liu KJ, Ramu J, Chen Q, Li T, Liu W (2010) Inhibition of gp91 (Phox) contributes towards normobaric hyperoxia-afforded neuroprotection in focal cerebral ischemia. Brain Res 1348:174-180
84. Tappel A, Fletcher B, Deamer D (1973) Effect of antioxidants and nutrients on lipid peroxidation fluorescent products and aging parameters in the mouse. J Gerontol 28:415-424
85. Teerlink T, Hennekes M, Bussemaker J, Groeneveld J (1993) Simultaneous determination of creatine compounds and adenine nucleotides in myocardial tissue by high-performance liquid chromatography. Anal Biochem 214:278-283
86. Tian L, Cai Q, Wei H (1998) Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radic Biol Med 24:1477-1484
87. Weidman SV (1980) Lipids and lipoproteins. In: Sonnenwirth AC, Jarett L (eds) Gradwohl's clinical laboratory methods and diagnosis, vol 1, 8th edn. Mosby Company, St. Louis, pp 272-304
88. Zhang T, Yang QW, Wang SN, Wang JZ, Wang Q, Wang Y, Luo YJ (2010) Hyperbaric oxygen therapy improves neurogenesis and brain blood supply in piriform cortex in rats with vascular dementia. Brain Inj 24:1350-1357
89. Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res 1090:35-44