Aging modifies daily variation of antioxidant enzymes and oxidative status in the hippocampus

Experimental Gerontology

Volumn 88, Issue , 2017, Pages 42-50

  Lacoste, María Gabriela ^a   Ponce, Ivana Tamara ^a   Golini, Rebeca Laura ^a   Delgado, Silvia Marcela ^a   Anzulovich, Ana Cecilia ^a  

^a UNIVERSIDAD NACIONAL DE SAN LUIS   (Argentina)

Author keywords

Aging; Antioxidant enzyme; Circadian rhythm; Hippocampus; Oxidative status

Indexed keywords

CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; LIPID PEROXIDASE; MESSENGER RNA; TRANSCRIPTION FACTOR ARNTL; BMAL1 PROTEIN, RAT;

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CIRCADIAN RHYTHM; COMPARATIVE STUDY; CONTROLLED STUDY; DAILY LIFE ACTIVITY; DARKNESS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME POLYMORPHISM; HEART ARRHYTHMIA; HIPPOCAMPAL TISSUE; LIPID PEROXIDATION; LOCOMOTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; YOUNG ADULT; ANIMAL; GENETICS; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; ARNTL TRANSCRIPTION FACTORS; CATALASE; CIRCADIAN RHYTHM; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HIPPOCAMPUS; LOCOMOTION; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85008873218     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2016.12.002     Document Type: Article

References (59)

1. Aebi, H., Catalase in vitro. Methods Enzymol. 105 (1984), 121–126.
2. Akerboom, T.P., Sies, H., Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 77 (1981), 373–382.
3. Albrecht, U., Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 74 (2012), 246–260.
4. Babu, H., Claasen, J.H., Kannan, S., Rünker, A.E., Palmer, T., Kempermann, G., A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front. Neurosci., 5, 2011, 89.
5. Balaban, R.S., Nemoto, S., Finkel, T., Mitochondria, oxidants, and aging. Cell 120 (2005), 483–495.
6. Baydas, G., Gursu, M.F., Yilmaz, S., Canpolat, S., Yasar, A., Cikim, G., Canatan, H., Daily rhythm of glutathione peroxidase activity, lipid peroxidation and glutathione levels in tissues of pinealectomized rats. Neurosci. Lett. 323 (2002), 195–198.
7. Bollinger, T., Schibler, U., Circadian rhythms - from genes to physiology and disease. Swiss Med. Wkly., 144, 2014, w13984.
8. Bonaconsa, M., Malpeli, G., Montaruli, A., Carandente, F., Grassi-Zucconi, G., Bentivoglio, M., Differential modulation of clock gene expression in the suprachiasmatic nucleus, liver and heart of aged mice. Exp. Gerontol. 55 (2014), 70–79.
9. Buhr, E.D., Takahashi, J.S., Molecular components of the mammalian circadian clock. Handb. Exp. Pharmacol. 217 (2013), 3–27.
10. Cao, L., Leers-Sucheta, S., Azhar, S., Aging alters the functional expression of enzymatic and non-enzymatic anti-oxidant defense systems in testicular rat Leydig cells. J. Steroid Biochem. Mol. Biol. 88 (2004), 61–67.
11. Casado, A., Encarnación López-Fernández, M., Concepción Casado, M., de La Torre, R., Lipid peroxidation and antioxidant enzyme activities in vascular and Alzheimer dementias. Neurochem. Res. 33 (2008), 450–458.
12. Dias, V., Junn, E., Mouradian, M.M., The role of oxidative stress in Parkinson's disease. J. Parkinsons Dis. 3 (2013), 461–491.
13. Dibner, C., Schibler, U., Albrecht, U., The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72 (2010), 517–549.
14. Draper, H.H., Hadley, M., Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186 (1990), 421–431.
15. Duncan, M.J., Prochot, J.R., Cook, D.H., Tyler Smith, J., Franklin, K.M., Influence of aging on Bmal1 and Per2 expression in extra-SCN oscillators in hamster brain. Brain Res. 1491 (2013), 44–53.
16. Farajnia, S., Deboer, T., Rohling, J.H., Meijer, J.H., Michel, S., Aging of the suprachiasmatic clock. Neuroscientist 20 (2014), 44–55.
17. Finkel, T., Holbrook, N.J., Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000), 239–247.
18. Flohé, L., Günzler, W.A., Assays of glutathione peroxidase. Methods Enzymol. 105 (1984), 114–121.
19. Fonzo, L.S., Golini, R.S., Delgado, S.M., Ponce, I.T., Bonomi, M.R., Rezza, I.G., Giménez, M.S., Anzulovich, A.C., Temporal patterns of lipoperoxidation and antioxidant enzymes are modified in the hippocampus of vitamin A-deficient rats. Hippocampus 19 (2009), 869–880.
20. Gago-Dominguez, M., Jiang, X., Castelao, J.E., Lipid peroxidation, oxidative stress genes and dietary factors in breast cancer protection: a hypothesis. Breast Cancer Res., 9, 2007, 201.
21. Gilca, M., Stoian, I., Atanasiu, V., Virgolici, B., The oxidative hypothesis of senescence. J. Postgrad. Med. 53 (2011), 207–213.
22. Golombek, D.A., Rosenstein, R.E., Physiology of circadian entrainment. Physiol. Rev. 90 (2010), 1063–1102.
23. Haddadi, M., Jahromi, S.R., Sagar, B.K., Patil, R.K., Shivanandappa, T., Ramesh, S.R., Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster. Behav. Brain Res. 259 (2014), 60–69.
24. Kolker, D.E., Fukuyama, H., Huang, D.S., Takahashi, J.S., Horton, T.H., Turek, F.W., Aging alters circadian and light-induced expression of clock genes in golden hamsters. J. Biol. Rhythm. 18 (2003), 159–169.
25. Kondratov, R.V., Kondratova, A.A., Gorbacheva, V.Y., Vykhovanets, O.V., Antoch, M.P., Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20 (2006), 1868–1873.
26. Kondratova, A.A., Kondratov, R.V., The circadian clock and pathology of the ageing brain. Nat. Rev. Neurosci. 13 (2012), 325–335.
27. Kunthavai Nachiyar, R., Subramanian, P., Tamilselvam, K., Manivasagam, T., Influence of aging on the circadian patterns of thiobarbituric acid reactive substances and antioxidants in Wistar rats. Biol. Rhythm. Res. 42 (2011), 147–154.
28. Lee, C.C., The circadian clock and tumor suppression by mammalian period genes. Methods Enzymol. 393 (2005), 852–861.
29. López-Otín, C., Blasco, M.A., Partridge, L., Serrano, M., Kroemer, G., The hallmarks of aging. Cell 153 (2013), 1194–1217.
30. Lu, S.C., Regulation of glutathione synthesis. Mol. Asp. Med. 30 (2009), 42–59.
31. Manikonda, P.K., Jagota, A., Melatonin administration differentially affects age-induced alterations in daily rhythms of lipid peroxidation and antioxidant enzymes in male rat liver. Biogerontology 13 (2012), 511–524.
32. Mendoza, J., Challet, E., Brain clocks: from the suprachiasmatic nuclei to a cerebral network. Neuroscientist 15 (2009), 477–488.
33. Mirmiran, M., Swaab, D.F., Kok, J.H., Hofman, M.A., Witting, W., Van Gool, W.A., Circadian rhythms and the suprachiasmatic nucleus in perinatal development, aging and Alzheimer's disease. Prog. Brain Res. 93 (1992), 151–162.
34. Nakamura, T.J., Nakamura, W., Yamazaki, S., Kudo, T., Cutler, T., Colwell, C.S., Block, G.D., Age-related decline in circadian output. J. Neurosci. 31 (2011), 10201–10205.
35. Navigatore-Fonzo, L.S., Delgado, S.M., Golini, R.S., Anzulovich, A.C., Circadian rhythms of locomotor activity and hippocampal clock genes expression are dampened in vitamin A-deficient rats. Nutr. Res. 34 (2014), 326–335.
36. Pablos, M.I., Reiter, R.J., Ortiz, G.G., Guerrero, J.M., Agapito, M.T., Chuang, J.I., Sewerynek, E., Rhythms of glutathione peroxidase and glutathione reductase in brain of chick and their inhibition by light. Neurochem. Int. 32 (1998), 69–75.
37. Ponce, I.T., Rezza, I.G., Delgado, S.M., Navigatore, L.S., Bonomi, M.R., Golini, R.L., Giménez, M.S., Anzulovich, A.C., Daily oscillation of glutathione redox cycle is dampened in the nutritional vitamin A deficiency. Biol. Rhythm. Res. 43 (2012), 351–372.
38. Radak, Z., Zhao, Z., Goto, S., Koltai, E., Age-associated neurodegeneration and oxidative damage to lipids, proteins and DNA. Mol. Asp. Med. 32 (2011), 305–315.
39. Refinetti, R., Lissen, G.C., Halberg, F., Procedures for numerical analysis of circadian rhythms. Biol. Rhythm. Res. 38 (2007), 275–325.
40. Reppert, S.M., Weaver, D.R., Coordination of circadian timing in mammals. Nature 418 (2002), 935–941.
41. Ristow, M., Schmeisser, S., Extending life span by increasing oxidative stress. Free Radic. Biol. Med. 51 (2011), 327–336.
42. Rodrigues Siqueira, I., Fochesatto, C., da Silva Torres, I.L., Dalmaz, C., Alexandre Netto, C., Aging affects oxidative state in hippocampus, hypothalamus and adrenal glands of Wistar rats. Life Sci. 78 (2005), 271–278.
43. Rutter, J., Reick, M., Wu, L.C., McKnight, S.L., Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293 (2001), 510–514.
44. S.E.P.T.M.R, Physiology software editor. http://www.septmr.com, 2000.
45. Sani, M., Ghanem-Boughanmi, N., Gadacha, W., Sebai, H., Boughattas, N.A., Reinberg, A., Ben-Attia, M., Malondialdehyde content and circadian variations in brain, kidney, liver, and plasma of mice. Chronobiol. Int. 24 (2007), 671–685.
46. Schibler, U., Sassone-Corsi, P., A web of circadian pacemakers. Cell 111 (2002), 919–922.
47. Shankar, S.K., Biology of aging brain. Indian J. Pathol. Microbiol. 53 (2010), 595–604.
48. Siqueira, I.R., Fochesatto, C., de Andrade, A., Santos, M., Hagen, M., Bello-Klein, A., Netto, C.A., Total antioxidant capacity is impaired in different structures from aged rat brain. Int. J. Dev. Neurosci. 23 (2005), 663–671.
49. Suh, J.H., Moreau, R., Heath, S.H., Hagen, T.M., Dietary supplementation with (R)-alpha-lipoic acid reverses the age-related accumulation of iron and depletion of antioxidants in the rat cerebral cortex. Redox Rep. 10 (2005), 52–60.
50. Suh, J.H., Wang, H., Liu, R.M., Liu, J., Hagen, T.M., (R)-alpha-lipoic acid reverses the age-related loss in GSH redox status in post-mitotic tissues: evidence for increased cysteine requirement for GSH synthesis. Arch. Biochem. Biophys. 423 (2004), 126–135.
51. Thaela, M.J., Jensen, M.S., Cornélissen, G., Halberg, F., Nöddegaard, F., Jakobsen, K., Pierzynowski, S.G., Circadian and ultradian variation in pancreatic secretion of meal-fed pigs after weaning. J. Anim. Sci. 76 (1998), 1131–1139.
52. Tsay, H.J., Wang, P., Wang, S.L., Ku, H.H., Age-associated changes of superoxide dismutase and catalase activities in the rat brain. J. Biomed. Sci. 7 (2000), 466–474.
53. Valentinuzzi, V.S., Scarbrough, K., Takahashi, J.S., Turek, F.W., Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am. J. Phys. 273 (1997), R1957–R1964.
54. Wang, Q., Zhao, X., He, S., Liu, Y., An, M., Ji, J., Differential proteomics analysis of specific carbonylated proteins in the temporal cortex of aged rats: the deterioration of antioxidant system. Neurochem. Res. 35 (2010), 13–21.
55. Wollnik, F., Physiology and regulation of biological rhythms in laboratory animals: an overview. Lab. Anim. 23 (1989), 107–125.
56. Wu, G., Fang, Y.Z., Yang, S., Lupton, J.R., Turner, N.D., Glutathione metabolism and its implications for health. J. Nutr. 134 (2004), 489–492.
57. Zhang, C., Pan, T., Salesse, C., Zhang, D., Miao, L., Wang, L., Gao, Y., Xu, J., Dong, Z., Luo, Q., Liu, J., Reversible Ca(2 +) switch of an engineered allosteric antioxidant selenoenzyme. Angew. Chem. Int. Ed. Eng. 53 (2014), 13536–13539.
58. Zhao, Y., Zhao, B., Oxidative stress and the pathogenesis of Alzheimer's disease. Oxidative Med. Cell. Longev., 2013, 2013, 316523.
59. Zuther, P., Gorbey, S., Lemmer, B., Chronos-Fit 1.06. http://www.ma.uni-heidelberg.de/inst/phar/lehre/chrono.html, 2009.