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Prolonged Light Deprivation Modulates the Age-Related Changes in α-Tocopherol Level in Rats

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Abstract

The light–dark cycle is one of the main environmental factors affecting the rhythm of biological processes in the body. A change or absence of this cyclicity leads to disruption of circadian rhythms and negatively affects the functioning of all body systems. The aim of the study was to investigate the effect of constant darkness, which began from the prenatal period (DD/DD) or from the moment of birth (LD/DD) and continued throughout life, on the content of α-tocopherol in Wistar rats in late ontogenesis (3, 6, 12, 18 and 24 months). Control animals were kept under standard light conditions (LD). The level of α-tocopherol was determined by HPLC. The modulating effect of long-term light deprivation was found in the liver, skeletal muscle and lungs, most of the changes were observed in 12-month-old rats. Thus, in the liver the level of vitamin decreased in both experimental groups, which is probably due to the regulatory role of the organ in maintaining vitamin E homeostasis in the body. In the skeletal muscle of rats from the DD/DD group, a significant increase in the content of α-tocopherol was found. This may show the accumulation of lipids in myocytes as a result of disorder of homeostasis of the main energy substrates of skeletal muscles. In 24-month-old rats of this group, the vitamin level in the tissue was significantly lower than in the control, which may indicate a decrease in the antioxidant protection of the skeletal muscle due to age-related changes. In rats, exposed to constant darkness after birth, there were differences in the direction of changes in the lungs α-tocopherol level compared with the control group at the age of 6 and 12 months. In aging and old animals, the effect of light deprivation was probably smoothed out by age-related disturbances of the circadian system thus in most of the studied tissues the vitamin content did not differ in rats of the control and both experimental groups. The results can be useful in assessing the physiological state of people working or living under poor lighting conditions.

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REFERENCES

  1. Mocchegiani E, Costarelli L, Giacconi R, Malavolta M, Basso A, Piacenza F, Ostan R, Cevenini E, Gonos ES, Franceschi C, Monti D (2014) Vitamin E—gene interactions in aging and inflammatory age-related diseases: Implications for treatment. A systematic review. Ageing Res Rev 14: 81–101. https://doi.org/10.1016/j.arr.2014.01.001

    Article  CAS  PubMed  Google Scholar 

  2. Traber MG (2013) Mechanisms for the prevention of vitamin E excess. J Lipid Res 54(9): 2295–2306. https://doi.org/10.1194/jlr.R032946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and Death: Metabolic Rate, Membrane Composition, and Life Span of Animals. Physiol Rev 87: 1175–1213. https://doi.org/10.1152/physrev.00047.2006

    Article  CAS  PubMed  Google Scholar 

  4. Mulligan AA, Hayhoe RPG, Luben RN, Welch AA (2021) Positive Associations of Dietary Intake and Plasma Concentrations of Vitamin E with Skeletal Muscle Mass, Heel Bone Ultrasound Attenuation and Fracture Risk in the EPIC-Norfolk Cohort. Antioxidants 10(2): 159. https://doi.org/10.3390/antiox10020159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hussain MM, Pan X (2015) Circadian regulation of macronutrient absorption. J Biol Rhythms 30(6): 459–469. https://doi.org/10.1177/0748730415599081

    Article  CAS  PubMed  Google Scholar 

  6. Janich P, Meng Q-J, Benitah SA (2014) Circadian control of tissue homeostasis and adult stem cells. Curr Opin Cell Biol 31: 8–15. https://doi.org/10.1016/j.ceb.2014.06.010

    Article  CAS  PubMed  Google Scholar 

  7. Reiter RJ, Rosales‑Corral S, Tan DX, Jou MJ, Galano A, Xu B (2017) Melatonin as a mitochondria‑targeted antioxidant: one of evolution’s best ideas. Cell Mol Life Sci 74: 3863–3881. https://doi.org/10.1007/s00018-017-2609-7

    Article  CAS  PubMed  Google Scholar 

  8. Anisimov VN (2008) Molecular and Physiological Mechanisms of Aging. V 1. Nauka, St-Petersburg. (In Russ).

    Google Scholar 

  9. Owino S, Buonfiglio DDC, Tchio C, Tosini G (2019) Melatonin Signaling a Key Regulator of Glucose Homeostasis and Energy Metabolism. Front Endocrinol 10: 488. https://doi.org/10.3389/fendo.2019.00488

    Article  Google Scholar 

  10. 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

    Article  PubMed  PubMed Central  Google Scholar 

  11. Tapia-Osorio A, Salgado-Delgado R, Angeles-Castellanos M, Escobar C (2013) Disruption of circadian rhythms due to chronic constant light leads to depressive and anxiety-like behaviors in the rat. Behav Brain Res 252: 1–9. https://doi.org/10.1016/j.bbr.2013.05.028

    Article  PubMed  Google Scholar 

  12. Hartley S, Dauvilliers Y, Quera-Salva M-A (2018) Circadian Rhythm Disturbances in the Blind. Curr Neurol Neurosci Rep 18: 65. https://doi.org/10.1007/s11910-018-0876-9

    Article  PubMed  Google Scholar 

  13. Lockley SW, Arendt J, Skene DJ (2007) Visual impairment and circadiam rhythm disorders. Dialogues Clin Neurosci 9(3): 301–314. https://doi.org/10.31887/DCNS.2007.9.3/slockley

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li H, Zhang S, Zhang W, Chen S, Rabearivony A, Shi Y, Liu J, Corton CJ, Liu C (2020) Endogenous circadian time genes expressions in the liver of mice under constant darkness. BMC Genomics 21: 224. https://doi.org/10.1186/s12864-020-6639-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Talaei SA, Azami A, Salami M (2016) Developmental effect of light deprivation on synaptic plasticity of rats’ hippocampus: implications for melatonin. Iran J Basic Med Sci 19: 899-909.

    PubMed  PubMed Central  Google Scholar 

  16. Bishnupuri KS, Haldar C (2000) Impact of photoperiodic exposures during late gestation and lactation periods on the pineal and reproductive physiology of the Indian palm squirrel, Funambulus pennant. J Reprod Fertil 118: 295–301. https://doi.org/10.1530/jrf.0.1180295

    Article  CAS  PubMed  Google Scholar 

  17. Brooks E, Canal MM (2013) Development of circadian rhythms: Role of postnatal light environment. Neurosci Biobehav Rev 37: 551–560. https://doi.org/10.1016/j.neubiorev.2013.02.012

    Article  PubMed  Google Scholar 

  18. Baishnikova IV, Ilyina TN, Khizhkin EA, Ilyukha VA, Vinogradova IA (2021) Effect of Long-Term Light Deprivation on α-Tocopherol Content in Rats during Ontogeny. Bull Exp Biol Med 170(3): 294–298. https://doi.org/10.1007/s10517-021-05054-1

    Article  CAS  PubMed  Google Scholar 

  19. Stuetz W, Weber D, Dollé MET, Jansen E, Grubeck-Loebenstein B, Fiegl S, Toussaint O, Bernhardt J, Gonos ES, Franceschi C, Sikora E, Moreno-Villanueva M, Breusing N, Grune T, Bürkle A (2016) Plasma Carotenoids, Tocopherols, and Retinol in the Age-Stratified (35–74 Years) General Population: A Cross-Sectional Study in Six European Countries. Nutrients 8(10): 614. https://doi.org/10.3390/nu8100614

    Article  CAS  PubMed Central  Google Scholar 

  20. Grolier P, Boirie Y, Levadoux E, Brandolini M, Borel P, Azais-Braesco V, Beaufrère B, Ritz P (2000) Age-related changes in plasma lycopene concentrations, but not in vitamin E, are associated with fat mass. Br J Nutr 84: 711–716. https://doi.org/10.1017/S0007114500002063

    Article  CAS  PubMed  Google Scholar 

  21. Traber MG, Leonard SW, Bobe G, Fu X, Saltzman E, Grusak MA, Booth SL (2015) α-Tocopherol disappearance rates from plasma depend on lipid concentrations: studies using deuterium-labeled collard greens in younger and older adults. Am J Clin Nutr 101(4): 752–759. https://doi.org/10.3945/ajcn.114.100966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nesic DM, Stevanovic DM, Stankovic SD, Milosevic VL, Trajkovic V, Starcevic VP, Severs WB (2013) Age-dependent modulation of central ghrelin effects on food intake and lipid metabolism in rats. Eur J Pharmacol 710: 85–91. https://doi.org/10.1016/j.ejphar.2013.03.052

    Article  CAS  PubMed  Google Scholar 

  23. Szewczyk K, Chojnacka A, Górnicka M (2021) Tocopherols and Tocotrienols—Bioactive Dietary Compounds; What Is Certain, What Is Doubt? Int J Mol Sci 22: 6222. https://doi.org/10.3390/ijms22126222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhao L, Zou X, Feng Z, Luo C, Liu J, Li H, Chang L, Wang H, Li Y, Long J, Gao F, Liu J (2014) Evidence for association of mitochondrial metabolism alteration with lipid accumulation in aging rats. Exp Gerontol 56: 3–12. https://doi.org/10.1016/j.exger.2014.02.001

    Article  CAS  PubMed  Google Scholar 

  25. Kim JY, Kim DH, Choi J, Park J-K, Jeong K-S, Leeuwenburgh C, Yu BP, Chung HY (2009) Changes in lipid distribution during aging and its modulation by calorie restriction. Age 31: 127–142. https://doi.org/10.1007/s11357-009-9089-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. König J, Besoke F, Stuetz W, Malarski A, Jahreis G, Grune T, Höhn A (2016) Quantification of age-related changes of α-tocopherol in lysosomal membranes in murine tissues and human fibroblasts. Biofactors 42(3): 307–315. https://doi.org/10.1002/biof.1274

    Article  CAS  PubMed  Google Scholar 

  27. van der Loo B, Labugger R, Aebischer CP, Skepper JN, Bachschmid M, Spitzer V, Kilo J, Altwegg L, Ullrich V, Lüscher TF (2002) Cardiovascular Aging Is Associated With Vitamin E Increase. Circulation 105: 1635–1638. https://doi.org/10.1161/01.CIR.0000014986.29834.71

    Article  CAS  PubMed  Google Scholar 

  28. Linard A, Macaire J-P, Christon R (2001) Phospholipid hydroperoxide glutathione peroxidase activity and vitamin E level in the liver microsomal membrane: effects of age and dietary a-linolenic acid deficiency. J Nutr Biochem 12: 481–491. https://doi.org/10.1016/s0955-2863(01)00165-6

    Article  CAS  PubMed  Google Scholar 

  29. Manikonda PK, Jagota A (2012) Melatonin administration differentially affects age-induced alterations in daily rhythms of lipid peroxidation and antioxidant enzymes in male rat liver. Biogerontology 13: 511–524. https://doi.org/10.1007/s10522-012-9396-1

    Article  CAS  PubMed  Google Scholar 

  30. Kamzalov S, Sohal RS (2004) Effect of age and caloric restriction on coenzyme Q and alpha-tocopherol levels in the rat. Exp Gerontol 39(8): 1199–1205. https://doi.org/10.1016/j.exger.2004.04.007

    Article  CAS  PubMed  Google Scholar 

  31. Takahashi K, Takisawa S, Shimokado K, Kono N, Arai H, Ishigami A (2017) Age‑related changes of vitamin E: α‑tocopherol levels in plasma and various tissues of mice and hepatic α‑tocopherol transfer protein. Eur J Nutr 56: 1317–1327. https://doi.org/10.1007/s00394-016-1182-4

    Article  CAS  PubMed  Google Scholar 

  32. Çoban J, Öztezcan S, Doğru-Abbasoğlu S, Bingül I, Yeşil-Mizrak K, Uysal M (2014) Olive leaf extract decreases age-induced oxidative stress in major organs of aged rats. Geriatr Gerontol Int 14(4): 996–1002. https://doi.org/10.1111/ggi.12192

    Article  PubMed  Google Scholar 

  33. Navarro-Hortal MD, Ramírez-Tortosa CL, Varela-López A, Romero-Márquez JM, Ochoa JJ, Ramírez-Tortosa MC, Forbes-Hernández TY, Granados-Principal S, Battino M, Quiles JL (2019) Heart Histopathology and Mitochondrial Ultrastructure in Aged Rats Fed for 24 Months on Different Unsaturated Fats (Virgin Olive Oil, Sunflower Oil or Fish Oil) and Affected by Different Longevity. Nutrients 11: 2390. https://doi.org/10.3390/nu11102390

    Article  CAS  PubMed Central  Google Scholar 

  34. Sadria M, Layton AT (2021) Aging affects circadian clock and metabolism and modulates timing of medication. Science 24(4): 102245. https://doi.org/10.1016/j.isci.2021.102245

    Article  CAS  Google Scholar 

  35. Koronowski KB, Kinouchi K, Welz P-S, Smith JG, Zinna VM, Shi J, Samad M, Chen S, Magnan CN, Kinchen JM, Li W, Baldi P, Benitah SA, Sassone-Corsi P (2019) Defining the Independence of the Liver Circadian Clock. Cell 177(6): 1448–1462. https://doi.org/10.1016/j.cell.2019.04.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yin H, Li W, Chatterjee S, Xiong X, Saha P, Yechoor V, Ma K (2020) Metabolic-sensing of the skeletal muscle clock coordinates fuel oxidation. FASEB J 34(5): 6613–6627. https://doi.org/10.1096/fj.201903226RR

    Article  CAS  PubMed  Google Scholar 

  37. Harfmann BD, Schroder EA, Esser KA (2015) Circadian Rhythms, the Molecular Clock, and Skeletal Muscle. J Biol Rhythms 30(2): 84–94. https://doi.org/10.1177/0748730414561638

    Article  CAS  PubMed  Google Scholar 

  38. Harfmann BD, Schroder EA, Kachman MT, Hodge BA, Zhang X, Esser KA (2016) Muscle-specific loss of Bmal1 leads to disrupted tissue glucose metabolism and systemic glucose homeostasis. Skelet Muscle 6: 12. https://doi.org/10.1186/s13395-016-0082-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Andrews JL, Zhang X, McCarthy JJ, McDearmonc EL, Hornberger TA, Russell B, Campbell KS, Arbogast S, Reid MB, Walker JR, Hogeneschg JB, Takahashi JS, Essera KA (2010) CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. PNAS 107 (44): 19090–19095. https://doi.org/10.1073/pnas.1014523107/-/DCSupplemental

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kersten S (2014) Physiological regulation of lipoprotein lipase. Biochim Biophys Acta 1841: 919–933. https://doi.org/10.1016/j.bbalip.2014.03.013

    Article  CAS  PubMed  Google Scholar 

  41. Delezie J, Dumont S, Dardente H, Oudart H, Gréchez-Cassiau A, Klosen P, Teboul M, Delaunay F, Pévet P, Challet E (2012) The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism. FASEB J 26(8): 3321–3335. https://doi.org/10.1096/fj.12-208751

    Article  CAS  PubMed  Google Scholar 

  42. Kim JK, Fillmore JJ, Chen Y, Yu C, Moore IK, Pypaert M, Lutz EP, Kako Y, Velez-Carrasco W, Goldberg IJ, Breslow JL, Shulman GI (2001) Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance. PNAS 98(13): 7522–7527. https://doi.org/10.1073/pnas.121164498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gilbert M (2021) Role of skeletal muscle lipids in the pathogenesis of insulin resistance of obesity and type 2 diabetes. J Diabetes Invest 12(11): 1934-1941. https://doi.org/10.1111/jdi.13614

    Article  CAS  Google Scholar 

  44. Park SS, Seo Y-K (2020) Excess Accumulation of Lipid Impairs Insulin Sensitivity in Skeletal Muscle. Int J Mol Sci 21(6): 1949. https://doi.org/10.3390/ijms21061949

    Article  CAS  PubMed Central  Google Scholar 

  45. Tschanz SA, Salm LA, Roth-Kleiner M, Barré SF, Burri PH, Schittny JC (2014) Rat lungs show a biphasic formation of new alveoli during postnatal development. J Appl Physiol 117: 89–95. https://doi.org/10.1152/japplphysiol.01355.2013

    Article  PubMed  Google Scholar 

  46. Wong-Riley MTT, Liu Q, Gao X (2019) Mechanisms underlying a critical period of respiratory development in the rat. Respir Physiol Neurobiol 264: 40–50. https://doi.org/10.1016/j.resp.2019.04.006

    Article  PubMed  PubMed Central  Google Scholar 

  47. Wright RJ (2010) Perinatal stress and early life programming of lung structure and function. Biol Psychol 84: 46–56. https://doi.org/10.1016/j.biopsycho.2010.01.007

    Article  PubMed  PubMed Central  Google Scholar 

  48. Motta-Teixeira LC, Machado-Nils AV, Battagello DS, Diniz GB, Andrade-Silva J, Silva S Jr, Matos RA, do Amaral FG, Xavier GF, Bittencourt JC, Reiter RJ, Lucassen PJ, Korosi A, Cipolla-Neto J (2018) The absence of maternal pineal melatonin rhythm during pregnancy and lactation impairs offspring physical growth, neurodevelopment, and behavior. Horm Behav 105: 146–156. https://doi.org/10.1016/j.yhbeh.2018.08.006

    Article  CAS  PubMed  Google Scholar 

  49. Farhadi N, Gharghani M, Farhadi Z (2016) Effects of long-term light, darkness and oral administration of melatonin on serum levels of melatonin. Biomed J 39: 81–84. https://doi.org/10.1016/j.bj.2015.09.003

    Article  PubMed  PubMed Central  Google Scholar 

  50. Kolleck I, Sinha P, Rüstow B (2002) Vitamin E as an Antioxidant of the Lung Mechanisms of Vitamin E Delivery to Alveolar Type II Cells. Am J Respir Crit Med 166(12 Pt 2): S62-S66. https://doi.org/10.1164/rccm.2206019

    Article  Google Scholar 

  51. Matsuo M, Gomi F, Dooley MM (1992) Age-related alterations in antioxidant capacity and lipid peroxidation in brain, liver, and lung homogenates of normal and vitamin E-deficient rats. Mech Ageing Dev 64(3): 273–292. https://doi.org/10.1016/0047-6374(92)90084-q

    Article  CAS  PubMed  Google Scholar 

  52. Mori K, Blackshear PE, Lobenhofer EK, Parker JS, Orzech DP, Roycroft JH, Walker KL, Johnson KA, Marsh TA, Irwin RD, Boorman GA (2007) Hepatic Transcript Levels for Genes Coding for Enzymes Associated with Xenobiotic Metabolism are Altered with Age. Toxicol Pathol 35: 242–251. https://doi.org/10.1080/01926230601156286

    Article  CAS  PubMed  Google Scholar 

  53. Kumar D, Rizvi SI (2014) A critical period in lifespan of male rats coincides with increased oxidative stress. Arch Gerontol Geriatr 58(3): 427–433. https://doi.org/10.1016/j.archger.2013.11.006

    Article  CAS  PubMed  Google Scholar 

  54. Braidy N, Guillemin GJ, Mansour H, Chan-Ling T, Poljak A, Grant R (2011) Age Related Changes in NAD+ Metabolism Oxidative Stress and Sirt1 Activity in Wistar Rats. PLoS One 6(4): e19194. https://doi.org/10.1371/journal.pone.0019194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Nakamura TJ, Nakamura W, Tokuda IT, Ishikawa T, Kudo T, Colwell CS, Block GD (2015) Age-Related Changes in the Circadian System Unmasked by Constant Conditions. ENEURO 2(4): 0064. https://doi.org/10.1523/ENEURO.0064-15.2015

    Article  Google Scholar 

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Funding

Financial support for the research was provided from the federal budget for the state assignment of the KarRC RAS (topic FMEN-2022-0003).

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

    I. V. Baishnikova, T. N. Ilyina, E. A. Khizhkin & V. A. Ilyukha

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Contributions

Idea of work and planning of the experiment (E.A.K., V.A.I.), data collection (I.V.B., E.A.K., T.N.I.), data processing (I.V.B., T.N.I.), writing and editing the article (I.V.B., E.A.K., T.N.I., V.A.I.).

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Correspondence to I. V. Baishnikova.

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Translated by A. Dyomina

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 10, pp. 1291–1304https://doi.org/10.31857/S0869813922100028.

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Baishnikova, I.V., Ilyina, T.N., Khizhkin, E.A. et al. Prolonged Light Deprivation Modulates the Age-Related Changes in α-Tocopherol Level in Rats. J Evol Biochem Phys 58, 1592–1603 (2022). https://doi.org/10.1134/S0022093022050271

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