The effects of endogenous melatonin on brain tissue oxidative stress induced by photoperiodic alterations and iron overloading in rats
Melatonin on brain tissue oxidative stress
Keywords:
Melatonin, iron dextran, photoperiod, oxidative stress, brain, rats
Abstract
Melatonin is a potent endogenously occurring antioxidant with the pleiotropic activities to neurodegenerative diseases associated with brain oxidative damage. In this study, we examined the prolonged photoperiodic alterations and iron (Fe) overload on melatonin production and brain oxidative stress in rats. The result showed that the 15 days of constant light (CL) exposure did not low the melatonin production but the 15 days of constant darkness (CD) significantly increased serum melatonin level in rats. The Fe treatment in both CL and CD conditions significantly reduced endogenous melatonin levels and increased brain tissue lipid peroxidation. Fe as a toxic transition metal can induce Fenton reaction to generated hydroxyl radical which can damage the neuronal cell membrane and impair the brain antioxidant system. In the current study, we observed the imbalanced antioxidant defense alterations upon Fe treatment in rat brain including the increased levels of alpha-tocopherol (α-T) and total thiols and the reduced melatonin level and catalase (CAT) activity. We speculated that the reduced melatonin level caused by Fe was due to its consumption since melatonin served as a metal chelator and antioxidant. Understanding these aspects enhances knowledge of brain Fe metabolism and its role in neurodegenerative disorders as well as the potential protective effects of melatonin on this metal.
References
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6. Reiter RJ, Tan DX, Fuentes-Broto L (2010) Melatonin: a multitasking molecule. Prog. Brain Res. 181: 127–151.
7. Smith JA, O’Hara J, Schiff AA (1981) Altered diurnal serum melatonin rhythm in blind men. Lancet 2: 933–938.
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9. González MMC (2018) Dim light at night and constant darkness: Two frequently used lighting conditions that jeopardize the health and well-being of laboratory rodents. Front. Neurol. 9: 609. https://doi.org/10.3389/fneur.2018.00609.
10. Cervino CO, Cogo Pagella J, Hernando MP (2023) Effects of long-term exposure to light or darkness and return to normal light-dark cycle on serum melatonin levels in rats. Melatonin Res. 6(2): 215-223. doi: 10.32794/mr112500150.
11. Tordjman, S, Chokron, S, Delorme R, Charrier A, Bellissant E, Jaafari N, Fougerou C (2017) Melatonin: Pharmacology, functions and therapeutic benefits. Cur. Neuropharmacol. 15: 434-443.
12. Arendt J, Skene DJ (2005) Melatonin as a chronobiotic. Sleep Med. Rev. 9: 25–39. doi: 10.1016/j.smrv.2004.05.002.
13. Pandi-Perumal SR, Srinivasan V, Maestroni GJM, Cardinali DP, Poeggeler B, Hardeland R (2006) Melatonin—Nature’s most versatile biological signal? FEBS J. 273: 2813–2838. DOI: 10.1111/j.1742-4658.2006.05322.x.
14. Tan DX, Hardeland R, Manchester LC, Paredes SD, Korkmaz A, Sainz RM, Mayo JC, Fuentes-Broto L, Reiter RJ (2010). The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol. Rev. Camb. Philos. Soc. 85: 607–623. doi: 10.1111/j.1469-185X.2009.00118.x.
15. Garcia JJ, Lopez-Pingarron L, Almeida-Souza P, Tres A, Escudero P, Garcia-Gil FA, Tan DX, Reiter RJ, Ramirez JM, Bernal-Perez M (2014) Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J. Pineal Res. 56: 225–237. doi: 10.1111/jpi.12128.
16. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (Pt 2): 335-344. doi: 10.1113/jphysiol.2003.049478.
17. González PM, Malanga G, Puntarulo S (2015) Cellular oxidant/antioxidant network: update on the environmental effects over marine organisms. Open Marine Biol. J. 9 (1): 1-13. http://dx.doi.org/10.2174/1874450801509010001.
18. Jones DP (2006) Redefining oxidative stress. Antioxid. Redox. Signal. 8: 1865–1879. doi: 10.1089/ars.2006.8.1865.
19. Halliwell B, Gutteridge JMC (2007). Free radicals in biology and medicine. Oxford University Press, New York. 4th Edition, pp. 936.
20. Padurariu M, Ciobica A, Lefter R, Serban IL, Stefanescu C (2013) The oxidative stress hypothesis in Alzheimer’s disease. Psychiatr. Danub. 25 (4): 401–409.
21. Imlay JA (2003) Pathways of oxidative damage. Annu. Rev. Microbiol. 57 (1): 395-418. doi: 10.1146/annurev.micro.57.030502.090938.
22. Reiter RJ, Tan DX, Manchester LC, Qi W (2001) Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem. Biophys. 34: 237–256. doi: 10.1385/CBB:34:2:237.
23. Reiter RJ, Tan DX, Mayo JC, Sainz RM, Leon J, Czarnocki Z (2003) Melatonin as an antioxidant: biochemical mechanisms and pathophysiological implications in humans. Acta Biochim. Pol. 50 (4): 1129-1146.
24. Galano A, Tan DX, Reiter RJ (2013) On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J. Pineal Res. 54 (3): 245–257.
25. Reiter R, Tang L, Garcia JJ, Munoz-Hoyos A (1997) Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci. 60: 2255–2271.
26. León J, Escames G, Rodríguez MI, López LC, Tapias V, Entrena A, Camacho E, Carrión MD, Gallo MA, Espinosa A, Tan DX, Reiter RJ, Acuña-Castroviejo D (2006) Inhibition of neuronal nitric oxide synthase activity by N1-acetyl-5-methoxykynuramine, a brain metabolite of melatonin. J. Neurochem. 98: 2023–2033. https://doi.org/10.1111/j.1471-4159.2006.04029.x.
27. Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ (2007) One molecule, many derivatives: A never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res. 42: 28–42.
28. Zhou JN, Liu RY, Kamphorst W, Hofman MA, Swaab DF (2003) Early neuropathological Alzheimer’s changes in aged individuals are accompanied by decreased cerebrospinal fluid melatonin levels. J. Pineal Res. 35: 125–130.
29. Wu YH, Swaab DF (2005) The human pineal gland and melatonin in aging and Alzheimer’s disease. J. Pineal Res. 38: 145–152.
30. Lin L, Huang QX, Yang SS, Chu J, Wang JZ, Tian Q (2013) Melatonin in Alzheimer’s disease. Int. J. Mol. Sci. 14 (7): 14575–14593. doi: 10.3390/ijms140714575.
31. Antolin I, Mayo JC, Sainz RM, del Brio ML, Herrera F, Martin V, Rodriguez C (2002) Protective effect of melatonin in a chronic experimental model of Parkinson’s disease. Brain Res. 943: 163–173.
32. Paredes SD, Reiter RJ (2010) Melatonin: Helping cells cope with oxidative disaster. Cell Memb. Free Radic. Res. 2 (3): 99-111.
33. Emerit J, Edeas M, Bricaire F (2004) Neurodegenerative diseases and oxidative stress. Biomed. Pharmacother. 58: 39–46. doi: 10.1016/j.biopha.2003.11.004.
34. Symons MCR, Gutteridge JMC (Eds). (1998). Free Radicals and Iron: Chemistry, Biology and Medicine. Oxford University Press, New York. pp. 258.
35. Gutteridge JM, Halliwell B (2000) Free radicals and antioxidants in the year 2000: A historical look to the future. Ann. N. Y. Acad. Sci. 899 (1): 136-147. doi: 10.1111/j.1749-6632.2000.tb06182.x.
36. Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P, Marsden CD (1989) Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J. Neurochem. 52 (6): 1830–1836.
37. Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic. Biol. Med. 23 (1): 134–147. doi: 10.1016/s0891-5849(96)00629-6.
38. Willmore LJ, Sypert GW, Munson JB (1978) Recurrent seizures induced by cortical iron injection: a model of posttraumatic epilepsy. Ann. Neurol. 4 (4): 329–336. doi: 10.1002/ana.410040408.
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Published
2024-04-30
How to Cite
[1]
Hernando, M., Cogo Pagella, J. and Cervino, C. 2024. The effects of endogenous melatonin on brain tissue oxidative stress induced by photoperiodic alterations and iron overloading in rats. Melatonin Research. 7, 1 (Apr. 2024), 103-119. DOI:https://doi.org/https://doi.org/10.32794/mr112500170.
Section
Research Articles
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