Skip to main content
SpringerLink
Log in

Circadian Rhythms of Antioxidant Enzyme’s Activity in Young and Adult Rats under Light Deprivation Conditions

  • Published:
Advances in Gerontology Aims and scope Submit manuscript

Abstract

We have studied the age-related features of circadian rhythms of superoxide dismutase (SOD) and catalase activity in the liver of rats under conditions of light deprivation. In standard light conditions (LD), significant daily fluctuations in SOD activity with a maximum at 7:00 a.m. were detected only in young animals (1.5 months) while catalase activity was observed in both young animals (1.5 months) and adults (7.5 months) with peak at 4:00 a.m. The daily dynamics of total and specific activity of SOD and catalase in the liver of young and adult rats differed, depending on the period of ontogeny in which the impact of light deprivation had begun. When females after giving birth and their offspring were moved to darkness (group LD/DD), the circadian rhythms of SOD and catalase activities were found in the young rats and were absent in adult rats. However, circadian rhythms of the antioxidant enzymes (AOE) activities were inherent only in adult rats when light deprivation impacted on pregnant females (group DD/DD). Changes in circadian rhythms under light deprivation were characterized either by a phase shift of the enzymes activity (in LD/DD group) or by a violation of their development in ontogeny (in DD/DD group). With aging a significant decrease of catalase activity was compensated by an increase in the amplitude of circadian rhythms of this enzyme activity in animals of all groups. The presence of an ultradian rhythm in the general circadian cycle characterized by a second peak with a smaller amplitude and shorter period can be considered a distinctive feature of daily fluctuations in AOЕ activity in young rats in LD and LD/DD groups.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Anisimov, V.N., Molekulyarnye i fiziologicheskie mekhanizmy stareniya (Molecular and Physiological Mechanisms of Aging), St. Petersburg: Nauka, 2008, vol. 1.

    Google Scholar 

  2. Rukovodstvo po laboratornym zhivotnym i al’ternativnym modelyam v biomeditsinskikh issledovaniyakh (Manual on Laboratory Animals and Alternative Models in Biomedical Studies), Karkishchenko, N.N. and Grahcev, S.V., Eds., Moscow: Profil’, 2010.

    Google Scholar 

  3. Eticheskaya ekspertiza biomeditsinskikh issledovanii: prakticheskie rekomendatsii (Ethical Expertise of Biomedical Studies: Practical Manual), Belousov, Yu.B., Ed., Moscow: Ross. O-vo Klin. Issled., 2005.

    Google Scholar 

  4. Albarrán, M. T., López-Burillo, S., Pablos, M.I., et al., Endogenous rhythms of melatonin, total antioxidant status and superoxide dismutase activity in several tissues of chick and their inhibition by light, J. Pineal Res., 2001, vol. 30, no. 4, pp. 227–233.

  5. Antolín, I., Rodríguez, C., and Saínz, R.M., Neurohormone melatonin prevents cell damage: effect on gene expression for antioxidant enzymes, FASEB J., 1996, vol. 10, no. 8, pp. 882–890.

  6. Bass, J. and Takahashi, J.S., Circadian integration of metabolism and energetics, Science, 2010, vol. 330, no. 6009, pp. 1349–1354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bears, R.F. and Sizer, I.N., A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase, J. Biol. Chem., 1952, vol. 195, no. 1, pp. 133–140.

    Google Scholar 

  8. Benot, S., Molinero, P., Soutto, M., et al., Circadian variations in the rat serum total antioxidant status: correlation with melatonin levels, J. Pineal Res., 1998, vol. 25, no. 1, pp. 1–4.

    Article  CAS  PubMed  Google Scholar 

  9. Benot, S., Goberna, R., Reiter, R.J., et al., Physiological levels of melatonin contribute to the antioxidant capacity of human serum, J. Pineal Res., 1999, vol. 27, no. 1, pp. 59–64.

    Article  CAS  PubMed  Google Scholar 

  10. Berra, B. and Rizzo, A.M., Melatonin: circadian rhythm regulator, chronobiotic, antioxidant and beyond, Clin. Dermatol., 2009, vol. 27, no. 2, pp. 202–209.

    Article  PubMed  Google Scholar 

  11. Bonnefont-Rousselot, D. and Collin, F., Melatonin: action as antioxidant and potential applications in human disease and aging, Toxicology, 2010, vol. 278, no. 1, pp. 55–67.

    Article  CAS  PubMed  Google Scholar 

  12. Borjigin, J., Zhang, L.S., and Calinescu, A.A., Circadian regulation of pineal gland rhythmicity, Mol. Cell. Endocrinol., 2012, vol. 349, no. 1, pp. 13–19.

    Article  CAS  PubMed  Google Scholar 

  13. Brooks, E. and Canal, M.M., Development of circadian rhythms: role of postnatal light environment, Neurosci. Biobehav. Rev., 2013, vol. 37, no. 4, pp. 551–560.

    Article  PubMed  Google Scholar 

  14. Calvo, J. and Boya, J., Postnatal evolution of the rat pineal gland: light microscopy, J. Anat., 1984, vol. 138, no. 1, pp. 45–53.

    PubMed  PubMed Central  Google Scholar 

  15. Christ, E., Korf, H.-W., and von Gall, C., When does it start ticking? Ontogenetic development of the mammalian circadian system, Prog. Brain Res., 2012, vol. 199, pp. 105–118.

    Article  CAS  PubMed  Google Scholar 

  16. Davis, F.C., Melatonin: role in development, J. Biol. Rhythms, 1997, vol. 12, pp. 498–508.

    Article  CAS  PubMed  Google Scholar 

  17. Davis, F.C. and Gorski, R.A., Development of hamster circadian rhythms: role of the maternal suprachiasmatic nucleus, J. Comp. Physiol. A, 1988, vol. 162, no. 5, pp. 601–610.

    Article  CAS  PubMed  Google Scholar 

  18. Deguchi, T., Ontogenesis of a biological clock for serotonin: acetyl coenzyme A N-acetyltransferase in pineal gland of rat, Proc. Natl. Acad. Sci. U.S.A., 1975, vol. 72, no. 7, pp. 2814–2818.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Díaz-Muñoz, M., Hernández-Muñoz, R., Suárez, J., and Chagoya de Sánchez, V., Day-night cycle of lipid peroxidation in rat cerebral cortex and their relationship to the glutathione cycle and superoxide dismutase activity, Neuroscience, 1985, vol. 16, no. 4, pp. 859–863.

  20. Farajnia, S., Deboer, T., and Rohling, J.H., Aging of the suprachiasmatic clock, Neuroscientist, 2014, vol. 20, no. 1, pp. 44–55.

    Article  PubMed  Google Scholar 

  21. Froy, O., The circadian clock and metabolism, Clin. Sci., 2011, vol. 120, no. 2, pp. 65–72.

    Article  CAS  PubMed  Google Scholar 

  22. Hardeland, R., Coto-Montes, A., and Poeggeler, B., Circadian rhythms, oxidative stress, and antioxidative defense mechanisms, Chronobiol. Int., 2003, vol. 20, no. 6, pp. 921–962.

    Article  CAS  PubMed  Google Scholar 

  23. Hardeland, R., Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance, Endocrine, 2005, vol. 27, no. 2, pp. 119–130.

    Article  CAS  PubMed  Google Scholar 

  24. Husse, J., Eichele, G., and Oster, H., Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time, BioEssays, 2015, vol. 37, no. 10, pp. 1119–1128.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Ikegami, T., Maruyama, Y., Doi, H., et al., Ultradian oscillation in expression of four melatonin receptor subtype genes in the pineal gland of the grass puffer, a semilunar-synchronized spawner, under constant darkness, Front. Neurosci., 2015, vol. 30, pp. 1–10.

    Google Scholar 

  26. Jang, Y.S., Lee, M.H., Lee, S.H., and Bae, K., Cu/Zn superoxide dismutase is differentially regulated in period gene-mutant mice, Biochem. Biophys. Res. Commun., 2011, vol. 409, no. 1, pp. 22–27.

    Article  CAS  PubMed  Google Scholar 

  27. Lacoste, M.G., Ponce, I.T., Golini, R.L., et al., Aging modifies daily variation of antioxidant enzymes and oxidative status in the hippocampus, Exp. Gerontol., 2017, vol. 88, pp. 42–50.

    Article  CAS  PubMed  Google Scholar 

  28. Landgraf, D., Koch, C.E., and Oster, H., Embryonic development of circadian clocks in the mammalian suprachiasmatic nuclei, Front. Neuroanat., 2014, vol. 8, pp. 1–10.

    Article  Google Scholar 

  29. Liu, T. and Borjigin, J., Free-running rhythms of pineal circadian output, J. Biol. Rhythms, 2005, vol. 20, no. 5, pp. 430–440.

    Article  CAS  PubMed  Google Scholar 

  30. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., and Randall, R.J., Protein measurement with the Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, no. 1, pp. 265–275.

    CAS  PubMed  Google Scholar 

  31. Manikonda, P.K. and Jagota, A., Melatonin administration differentially affects age-induced alterations in daily rhythms of lipid peroxidation and antioxidant enzymes in male rat liver, Biogerontology, 2012, vol. 13, no. 5, pp. 511–524.

    Article  CAS  PubMed  Google Scholar 

  32. Martin, V., Sainz, R.M., Mayo, J.C., et al., Daily rhythm of gene expression in rat superoxide dismutases, Endocr. Res., 2003, vol. 29, no. 1, pp. 83–95.

    Article  CAS  PubMed  Google Scholar 

  33. Mirmiran, M., Swaab, D.F., Kok, J.H., et al., Circadian rhythms and the suprachiasmatic nucleus in perinatal development, aging and Alzheimer’s disease, Prog. Brain Res., 1992, vol. 93, pp. 151–162.

    Article  CAS  PubMed  Google Scholar 

  34. Misra, H.H. and Fridovich, I., The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase, J. Biol. Chem., 1972, vol. 247, no. 10 P. 3170–3175.

    CAS  Google Scholar 

  35. Miyata, R., Tanuma, N., Sakuma, H., and Hayashi, M., Circadian rhythms of oxidative stress markers and melatonin metabolite in patients with xeroderma pigmentosum group A, Oxid. Med. Cell. Longevity, 2016, vol. 2016. doi 10.1155/2016/5741517

  36. Pablos, M.I., Reiter, R.J., Ortiz, G.G., et al., Rhythms of glutathione peroxidase and glutathione reductase in brain of chick and their inhibition by light, Neurochem. Int., 1998, vol. 32, no. 1, pp. 69–75.

    Article  CAS  PubMed  Google Scholar 

  37. Pandi-Perumal, S.R., BaHammam, A.S., Brown, G.M., et al., Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes, Neurotoxic. Res., 2013, vol. 23, no. 3, pp. 267–300.

    Article  CAS  Google Scholar 

  38. Pereira, B., Rosa, L.F., Safi, D.A., et al., Hormonal regulation of superoxide dismutase, catalase, and glutathione peroxidase activities in rat macrophages, Biochem. Pharmacol., 1995, vol. 50, no. 12, pp. 2093–2098.

    Article  CAS  PubMed  Google Scholar 

  39. Pevet, P. and Challet, E., Melatonin: both master clock output and internal time-giver in the circadian clocks network, J. Physiol. (Paris), 2011, vol. 105, nos. 4–6, pp. 170–182.

  40. Reiter, R.J., Rosales-Corral, S., Coto-Montes, A., et al., The photoperiod, circadian regulation and chronodisruption: the requisite interplay between the suprachiasmatic nuclei and the pineal and gut melatonin, J. Physiol. Pharmacol., 2011, vol. 62, no. 3, pp. 269–274.

    CAS  PubMed  Google Scholar 

  41. Reiter, R.J., Tan, D.-X., Korkmaz, A., and Rosales-Corral, S.A., Melatonin and stable circadian rhythms optimize maternal, placental and fetal physiology, Hum. Reprod. Update, 2014, vol. 20, no. 2, pp. 293–307.

    Article  CAS  PubMed  Google Scholar 

  42. Reppert, S.M., Weaver, D.R., and Rivkees, S.A., Prenatal function and entrainment of a circadian clock, in Research in Perinatal Medicine, Vol. 9: Development of Circadian Rhythmicity and Photoperiodism in Mammals, Reppert, S.M., Ed., Ithaca, NY: Perinatology Press, 1989, ch. 2, pp. 25–44.

  43. Reppert, S.M. and Schwartz, W.J., Maternal coordination of the fetal biological clock in utero, Science, 1983, vol. 220, no. 4600, pp. 969–971.

    Article  CAS  PubMed  Google Scholar 

  44. Rowe, S.A. and Kennaway, D.J., Melatonin in rat milk and the likelihood of its role in postnatal maternal entrainment of rhythms, Am. J. Physiol.-Regul., Integr. Comp. Physiol., 2002, vol. 282, no. 3, pp. R797–R804.

    Article  CAS  Google Scholar 

  45. Sancar, A., Lindsey-Boltz, L.A., Kang, T.H., et al., Circadian clock control of the cellular response to DNA damage, FEBS Lett., 2010, vol. 584, no. 12, pp. 2618–2625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sani, M., Sebaï, H., Gadacha, W., et al., Catalase activity and rhythmic patterns in mouse brain, kidney and liver, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2006, vol. 145, nos. 3–4, pp. 331–337.

  47. Sanchez, S., Paredes, S.D., Martin, M.I., et al., Effect of tryptophan administration on circulating levels of melatonin and phagocytic activity, J. Appl. Biomed., 2004, vol. 2, no. 3, pp. 169–177.

    Article  CAS  Google Scholar 

  48. Sumova, A., Sladek, M., Polidarova, L., et al., Circadian sys tem from conception till adulthood, Prog. Brain Res., 2012, vol. 199, pp. 83–103.

    Article  CAS  PubMed  Google Scholar 

  49. Tan, D.-X., Reiter, R.J., Manchester, L.C., et al., Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger, Curr. Top. Med. Chem., 2002, vol. 2, no. 2, pp. 181–197.

    Article  CAS  PubMed  Google Scholar 

  50. Tapia-Osorio, A., Salgado-Delgado, R., Angeles-Castellanos, M., and Escobar, C., Disruption of circadian rhythms due to chronic constant light leads to depressive and anxiety-like behaviors in the rat, Behav. Brain Res., 2013, vol. 252, pp. 1–9.

    Article  PubMed  Google Scholar 

  51. Tomas-Zapico, C., Coto-Montes, A., Martinez-Fraga, J., et al., Effects of continuous light exposure on antioxidant enzymes, porphyric enzymes and cellular damage in the Harderian gland of Syrian hamster, J. Pineal. Res., 2003, vol. 34, no. 1, pp. 60–68.

    Article  CAS  PubMed  Google Scholar 

  52. Wilking, M., Ndiaye, M., Mukhtar, H., and Ahmad, N., Circadian rhythm connections to oxidative stress: implications for human health, Antioxid. Redox Signaling, 2013, vol. 19, no. 2, pp. 192–208.

    Article  CAS  Google Scholar 

  53. Xu, Y.-Q., Zhang, D., Jin, T., et al., Diurnal variation of hepatic antioxidant gene expression in mice, PLoS One, 2012, vol. 7, no. 8. doi doi 10.1371/journal.pone.0044237

  54. Yamazaki, S., Yoshikawa, T., Biscoe, E.W., et al., Ontogeny of circadian organization in the rat, J. Biol. Rhythms, 2009, vol. 24, no. 1, pp. 55–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biology, Karelian Research Centre, Russian Academy of Sciences, 185910, Petrozavodsk, Russia

    E. A. Khizhkin, V. A. Ilyukha, E. P. Antonova & A. V. Morozov

  2. Petrozavodsk State University, 185910, Petrozavodsk, Russia

    E. A. Khizhkin & I. A. Vinogradova

Authors
  1. E. A. Khizhkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. A. Ilyukha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. A. Vinogradova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. P. Antonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. V. Morozov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. Khizhkin.

Additional information

Translated by E. Sherstyuk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khizhkin, E.A., Ilyukha, V.A., Vinogradova, I.A. et al. Circadian Rhythms of Antioxidant Enzyme’s Activity in Young and Adult Rats under Light Deprivation Conditions. Adv Gerontol 8, 328–338 (2018). https://doi.org/10.1134/S2079057018040069

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079057018040069

Keywords:

Search

Navigation