PHOTOPERIOD-INDUCED ALTERATIONS IN BIOMARKERS OF OXIDATIVE STRESS IN RATS OF DIFFERENT AGES AND INDIVIDUAL PHYSIOLOGICAL REACTIVITY
DOI: 10.32999/ksu2524-0838/2022-32-7
Keywords:
rats, resistance to hypoxia, liver, seasons, lipid hydroperoxides, 2-thiobarbituric acid reactive substances (TBARS), total antioxidant capacity (TAC)
Abstract
This study was performed to investigate the photoperiod-induced changes in biomarkers of oxidative stress in rats of different ages and different physiological reactivity, as assessed by different resistance to hypoxia. The study was conducted on 96 male Wistar rats divided into 16 groups based on resistance to hypoxia (LR, low resistance, HR, high resistance) and age, i.e. 6 and 21 months. The research was conducted at four photoperiod points: winter (January), spring (March), summer (July), and autumn (October). Lower levels of oxidative stress biomarkers (p < 0.05) were observed in the younger rats when compared to older rats, as well as in HR rats compared to LR rats. The levels of lipid peroxidation end product, 2-thiobarbituric acid reactive substances (TBARS) as the major indicator of oxidative stress, were found to increase with age, and summer resulted in further elevation compared to other seasons. Also, oxidative stress biomarkers were lower (p < 0.05) in winter than in other seasons, especially in the HR rats. TAC level in the hepatic tissue of the 6-months-old rats was significantly higher (p < 0.05) when compared to the level value in older rats. A similar higher TAC level was found in the hepatic tissue of HR rats compared to the LR rats. The adult rats with HR maintained TAC with minimal fluctuations throughout the year. It should be noted that the difference in TAC was higher for the groups of the adult animals with HR to hypoxia in winter, spring, and summer, which may indicate effective mechanisms preventing the formation of reactive oxygen species and systems of elimination thereof
References
1. Altamirano FG, Castro-Pascual IC, Ferramola ML, Tula ML, Delgado SM, Anzulovich AC, Lacoste MG. Aging disrupts the temporal organization of antioxidant defenses in the heart of male rats and phase shifts circadian rhythms of systolic blood pressure. Biogerontology. 2021;22(6):603-621. doi: 10.1007/s10522-021-09938-7
2. Bartke A, Amador AG, Chandrashekar V, Klemcke HG. Seasonal differences in testicular receptors and steroidogenesis. J Steroid Biochem. 1987;27(1-3):581-7. doi: 10.1016/0022-4731(87)90357-8
3. Bartman CM, Eckle T. Circadian-Hypoxia Link and its Potential for Treatment of Cardiovascular Disease. Curr Pharm Des. 2019;25(10):1075-1090. doi: 10.2174/1381612825666190516081612
4. Bartosz G. Total antioxidant capacity. Adv Clin Chem. 2003;37:219-92. doi: 10.1016/s0065-2423(03)37010-6
5. Biondo-Simões Mde L, Matias JE, Montibeller GR, Siqueira LC, Nunes Eda S, Grassi CA. Effect of aging on liver regeneration in rats. Acta Cir Bras. 2006;21(4):197-202. doi: 10.1590/s0102-86502006000400002
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54. doi: 10.1006/abio.1976.9999
7. Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A. Organization of circadian functions: interaction with the body. Prog Brain Res. 2006;153:341-60. doi: 10.1016/S0079-6123(06)53020-1
8. Dzhalilova D, Makarova O. Differences in Tolerance to Hypoxia: Physiological, Biochemical, and Molecular-Biological Characteristics. Biomedicines. 2020;8(10):428. doi: 10.3390/biomedicines8100428
9. Dzhalilova DS, Diatroptov ME, Tsvetkov IS, Makarova OV, Kuznetsov SL. Expression of Hif-1α, Nf-κb, and Vegf Genes in the Liver and Blood Serum Levels of HIF-1α, Erythropoietin, VEGF, TGF-β, 8-Isoprostane, and Corticosterone in Wistar Rats with High and Low Resistance to Hypoxia. Bull Exp Biol Med. 2018;165(6):781-785. doi: 10.1007/s10517-018-4264-x
10. Emens JS, Burgess HJ. Effect of Light and Melatonin and Other Melatonin Receptor Agonists on Human Circadian Physiology. Sleep Med Clin. 2015;10(4):435-53. doi:10.1016/j.jsmc.2015.08.001
11. Fang YZ, Yang S, Wu G. Free radicals, antioxidants, and nutrition. Nutrition. 2002;18(10):872-9. doi:10.1016/s0899-9007(02)00916-4
12. Galaktionova LP, Molchanov AV, El'chaninova SA, Varshavskiĭ BIa. Sostoianie perekisnogo okisleniia u bol'nykh s iazvennoĭ bolezn'iu zheludka i dvenadtsatiperstnoĭ kishki [Lipid peroxidation in patients with gastric and duodenal peptic ulcers]. Klin. Lab. Diagn., 1998;(6):10-14.
13. Grek OR, Pupyshev AB, Tikhonova EV. Effect of transitory ischemia on liver lysosomal apparatus in rats with different resistance to hypoxia. Bull Exp Biol Med. 2003;136(1):11-3. doi: 10.1023/a:1026016224694
14. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr. 1993;57(5 Suppl):715S-724S; discussion 724S-725S. doi: 10.1093/ajcn/57.5.715S
15. Hardeland R, Coto-Montes A, Poeggeler B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int. 2003;20(6):921-62. doi: 10.1081/cbi-120025245
16. Höller Y, Gudjónsdottir BE, Valgeirsdóttir SK, Heimisson GT. The effect of age and chronotype on seasonality, sleep problems, and mood. Psychiatry Res. 2021;297:113722. doi:10.1016/j.psychres.2021.113722
17. Jain K, Suryakumar G, Prasad R, Ganju L. Differential activation of myocardial ER stress response: a possible role in hypoxic tolerance. Int J Cardiol. 2013;168(5):4667-77. doi:10.1016/j.ijcard.2013.07.180
18. Kamyshnikov, V. 2004. A reference book on the clinic and biochemical researches and laboratory diagnostics. MEDpress-inform, Moscow. (In Russian).
19. Kurgaliuk, N.N. Oksid azota kak faktor adaptatsionnoĭ zashchity pri gipoksii [Nitric oxide as an adaptive protection factor in hypoxia]. Usp. Fiziol. Nauk, 2002;33(4), 65-79. [In Russian].
20. Kurhaluk N, Lukash O, Nosar V, Portnychenko A, Portnichenko V, Wszedybyl-Winklewska M, Winklewski PJ. Liver mitochondrial respiratory plasticity and oxygen uptake evoked by cobalt chloride in rats with low and high resistance to extreme hypobaric hypoxia. Can J Physiol Pharmacol. 2019;97(5):392-399. doi: 10.1139/cjpp-2018-0642
21. Kurhaluk N, Tkachenko H, Lukash O. Melatonin modulates oxidative phosphorylation, hepatic and kidney autophagy-caused subclinical endotoxemia and acute ethanol-induced oxidative stress. Chronobiol Int. 2020;37(12):1709-1724. doi: 10.1080/07420528.2020.1830792
22. Kurhaluk N, Tkachenko H. Melatonin and alcohol-related disorders. Chronobiol Int. 2020;37(6):781-803. doi: 10.1080/07420528.2020.1761372.
23. Kurhaluk N, Zaitseva OV, Sliuta A, Kyriienko S, Winklewski PJ. Melatonin diminishes oxidative stress in plasma, retains erythrocyte resistance and restores white blood cell count after low dose lipopolysaccharide exposure in mice. Gen Physiol Biophys. 2018;37(5):571-580. doi: 10.4149/gpb_2018010
24. Kurhalyuk N, Tkachenko H. L-arginine modulates mitochondrial function in rat liver during physical training. J Vet Res. 2007;51:641–647.
25. Kurhalyuk NM, Serebrovskaya TV, Kolesnikova EE. Role of cholino- and adrenoreceptors in regulation of rat antioxidant defense system and lipid peroxidation during adaptation to intermittent hypoxia. Probl Eco. Med Genet Cell Immunol. 2001;7:126-137. [In Ukrainian].
26. Lacoste MG, Ponce IT, Golini RL, Delgado SM, Anzulovich AC. Aging modifies daily variation of antioxidant enzymes and oxidative status in the hippocampus. Exp Gerontol. 2017;88:42-50. doi: 10.1016/j.exger.2016.12.002
27. Luk'ianova LD Molekuliarnye mekhanizmy tkanevoĭ gipoksii i adaptatsii organizma [Molecular mechanisms of tissue hypoxia and organism adaptation]. Fiziol Zh, 2003;49(3):17-35. (In Russian).
28. Lukyanova LD, Kirova YI, Germanova EL. The Role of Succinate in Regulation of Immediate HIF-1α Expression in Hypoxia. Bull Exp Biol Med. 2018;164(3):298-303. doi:10.1007/s10517-018-3976-2
29. Lukyanova LD, Kirova YI. Mitochondria-controlled signaling mechanisms of brain protection in hypoxia. Front Neurosci. 2015;9:320. doi: 10.3389/fnins.2015.00320
30. Lukyanova LD, Kirova YI. Effect of hypoxic preconditioning on free radical processes in tissues of rats with different resistance to hypoxia. Bull Exp Biol Med. 2011;151(3):292-6. English, Russian. doi: 10.1007/s10517-011-1312-1
31. Mármol F, Sánchez J, López D, Martínez N, Mitjavila MT, Puig-Parellada P. Oxidative stress, nitric oxide and prostaglandin E2 levels in the gastrointestinal tract of aging rats. J Pharm Pharmacol. 2009;61(2):201-6. doi: 10.1211/jpp/61.02.0009
32. Mármol F, Sánchez J, López D, Martínez N, Xaus C, Peralta C, Roselló-Catafau J, Mitjavila MT, Puig-Parellada P. Role of oxidative stress and adenosine nucleotides in the liver of aging rats. Physiol Res. 2010;59(4):553-560. doi: 10.33549/physiolres.931768
33. McClung CA. Circadian rhythms and mood regulation: insights from pre-clinical models. Eureuropsychopharmacol. 2011;21 Suppl 4(Suppl 4):S683-93. doi:10.1016/j.euroneuro.2011.07.008
34. Miyazawa T. Lipid hydroperoxides in nutrition, health, and diseases. Proc Jpn Acad Ser B Phys Biol Sci. 2021;97(4):161-196. doi: 10.2183/pjab.97.010
35. Mortola JP. Gender and the circadian pattern of body temperature in normoxia and hypoxia. Respir Physiol Neurobiol. 2017;245:4-12. doi: 10.1016/j.resp.2016.11.002
36. Mortola JP. Hypoxia and circadian patterns. Respir Physiol Neurobiol. 2007;158(2-3):274-9. doi:10.1016/j.resp.2007.02.005
37. Niki E. Lipid peroxidation products as oxidative stress biomarkers. Biofactors. 2008;34(2):171-80. doi:10.1002/biof.5520340208
38. Padhy G, Sethy NK, Ganju L, Bhargava K. Abundance of plasma antioxidant proteins confers tolerance to acute hypobaric hypoxia exposure. High Alt Med Biol. 2013;14(3):289-97. doi:10.1089/ham.2012.1095
39. Peek CB, Levine DC, Cedernaes J, Taguchi A, Kobayashi Y, Tsai SJ, Bonar NA, McNulty MR, Ramsey KM, Bass J. Circadian Clock Interaction with HIF1α Mediates Oxygenic Metabolism and Anaerobic Glycolysis in Skeletal Muscle. Cell Metab. 2017;25(1):86-92. doi: 10.1016/j.cmet.2016.09.010
40. Pré J. La lipopéroxydation [Lipid peroxidation]. Pathol Biol (Paris), 1991;39(7):716-736. [In French].
41. Reiter RJ, Tan DX, Terron MP, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol. 2007;54(1):1-9. Epub 2007 Mar 9. PMID: 17351668
42. Rubio C, Lizárraga E, Álvarez-Cilleros D, Pérez-Pardo P, Sanmartín-Salinas P, Toledo-Lobo MV, Alvarez C, Escrivá F, Fernández-Lobato M, Guijarro LG, Valverde AM, Carrascosa JM. Aging in Male Wistar Rats Associates With Changes in Intestinal Microbiota, Gut Structure, and Cholecystokinin-Mediated Gut-Brain Axis Function. J Gerontol A Biol Sci Med Sci. 2021;76(11):1915-1921. doi: 10.1093/gerona/glaa313
43. Serebrovskaya TV, Xi L. (2012). Individualized intermittent hypoxia training: principles and practices. In: Intermittent Hypoxia and Human Diseases, L. Xi and T. Serebrovskaya, Eds., Springer: London, UK.
44. Strauss E, Waliszewski K, Oszkinis G, Staniszewski R. Polymorphisms of genes involved in the hypoxia signaling pathway and the development of abdominal aortic aneurysms or largeartery atherosclerosis. J Vasc Surg. 2015;61(5):1105-13.e3. doi: 10.1016/j.jvs.2014.02.007
45. Tian L, Cai Q, Wei H. Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radic Biol Med. 1998;24(9):1477-84. doi: 10.1016/s0891-5849(98)00025-2
46. Tkachenko H, Kurhalyuk N, Khabrovska L, Kamiński P. Effect of L-arginine on lead induced oxidative stress in the blood of rats with different resistance to hypoxia. Pol J Food Nutr Sci. 2007;57(3):387-394.
47. Travaglio M, Ebling FJP. Role of hypothalamic tanycytes in nutrient sensing and energy balance. Proc Nutr Soc. 2019;78(3):272-278. doi: 10.1017/S0029665118002665
48. Ubuka T, Bentle GE. (2011). Neuroendocrine control of reproduction in birds. In: D.O. Norris, K.H. Lopez (Eds.), Hormones and Reproduction of Vertebrates. Academic Press, London, p. 1-25.
49. Urbanski HF, Sorwell KG. Age-related changes in neuroendocrine rhythmic function in the rhesus macaque. Age (Dordr). 2012;34(5):1111-21. doi: 10.1007/s11357-011-9352-z
50. van der Klein SAS, Zuidhof MJ, Bédécarrats GY. Diurnal and seasonal dynamics affecting egg production in meat chickens: A review of mechanisms associated with reproductive dysregulation. Anim Reprod Sci. 2020;213:106257. doi: 10.1016/j.anireprosci.2019.106257
51. Yan L, Lonstein JS, Nunez AA. Light as a modulator of emotion and cognition: Lessons learned from studying a diurnal rodent. Horm Behav. 2019;111:78-86. doi: 10.1016/j.yhbeh.2018.09.003
52. Zar, J.H. (1999). Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey.
53. Zhang HJ, Xu L, Drake VJ, Xie L, Oberley LW, Kregel KC. Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. FASEB J. 2003;17(15):2293-5. doi: 10.1096/fj.03-0139fje
2. Bartke A, Amador AG, Chandrashekar V, Klemcke HG. Seasonal differences in testicular receptors and steroidogenesis. J Steroid Biochem. 1987;27(1-3):581-7. doi: 10.1016/0022-4731(87)90357-8
3. Bartman CM, Eckle T. Circadian-Hypoxia Link and its Potential for Treatment of Cardiovascular Disease. Curr Pharm Des. 2019;25(10):1075-1090. doi: 10.2174/1381612825666190516081612
4. Bartosz G. Total antioxidant capacity. Adv Clin Chem. 2003;37:219-92. doi: 10.1016/s0065-2423(03)37010-6
5. Biondo-Simões Mde L, Matias JE, Montibeller GR, Siqueira LC, Nunes Eda S, Grassi CA. Effect of aging on liver regeneration in rats. Acta Cir Bras. 2006;21(4):197-202. doi: 10.1590/s0102-86502006000400002
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54. doi: 10.1006/abio.1976.9999
7. Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A. Organization of circadian functions: interaction with the body. Prog Brain Res. 2006;153:341-60. doi: 10.1016/S0079-6123(06)53020-1
8. Dzhalilova D, Makarova O. Differences in Tolerance to Hypoxia: Physiological, Biochemical, and Molecular-Biological Characteristics. Biomedicines. 2020;8(10):428. doi: 10.3390/biomedicines8100428
9. Dzhalilova DS, Diatroptov ME, Tsvetkov IS, Makarova OV, Kuznetsov SL. Expression of Hif-1α, Nf-κb, and Vegf Genes in the Liver and Blood Serum Levels of HIF-1α, Erythropoietin, VEGF, TGF-β, 8-Isoprostane, and Corticosterone in Wistar Rats with High and Low Resistance to Hypoxia. Bull Exp Biol Med. 2018;165(6):781-785. doi: 10.1007/s10517-018-4264-x
10. Emens JS, Burgess HJ. Effect of Light and Melatonin and Other Melatonin Receptor Agonists on Human Circadian Physiology. Sleep Med Clin. 2015;10(4):435-53. doi:10.1016/j.jsmc.2015.08.001
11. Fang YZ, Yang S, Wu G. Free radicals, antioxidants, and nutrition. Nutrition. 2002;18(10):872-9. doi:10.1016/s0899-9007(02)00916-4
12. Galaktionova LP, Molchanov AV, El'chaninova SA, Varshavskiĭ BIa. Sostoianie perekisnogo okisleniia u bol'nykh s iazvennoĭ bolezn'iu zheludka i dvenadtsatiperstnoĭ kishki [Lipid peroxidation in patients with gastric and duodenal peptic ulcers]. Klin. Lab. Diagn., 1998;(6):10-14.
13. Grek OR, Pupyshev AB, Tikhonova EV. Effect of transitory ischemia on liver lysosomal apparatus in rats with different resistance to hypoxia. Bull Exp Biol Med. 2003;136(1):11-3. doi: 10.1023/a:1026016224694
14. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr. 1993;57(5 Suppl):715S-724S; discussion 724S-725S. doi: 10.1093/ajcn/57.5.715S
15. Hardeland R, Coto-Montes A, Poeggeler B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int. 2003;20(6):921-62. doi: 10.1081/cbi-120025245
16. Höller Y, Gudjónsdottir BE, Valgeirsdóttir SK, Heimisson GT. The effect of age and chronotype on seasonality, sleep problems, and mood. Psychiatry Res. 2021;297:113722. doi:10.1016/j.psychres.2021.113722
17. Jain K, Suryakumar G, Prasad R, Ganju L. Differential activation of myocardial ER stress response: a possible role in hypoxic tolerance. Int J Cardiol. 2013;168(5):4667-77. doi:10.1016/j.ijcard.2013.07.180
18. Kamyshnikov, V. 2004. A reference book on the clinic and biochemical researches and laboratory diagnostics. MEDpress-inform, Moscow. (In Russian).
19. Kurgaliuk, N.N. Oksid azota kak faktor adaptatsionnoĭ zashchity pri gipoksii [Nitric oxide as an adaptive protection factor in hypoxia]. Usp. Fiziol. Nauk, 2002;33(4), 65-79. [In Russian].
20. Kurhaluk N, Lukash O, Nosar V, Portnychenko A, Portnichenko V, Wszedybyl-Winklewska M, Winklewski PJ. Liver mitochondrial respiratory plasticity and oxygen uptake evoked by cobalt chloride in rats with low and high resistance to extreme hypobaric hypoxia. Can J Physiol Pharmacol. 2019;97(5):392-399. doi: 10.1139/cjpp-2018-0642
21. Kurhaluk N, Tkachenko H, Lukash O. Melatonin modulates oxidative phosphorylation, hepatic and kidney autophagy-caused subclinical endotoxemia and acute ethanol-induced oxidative stress. Chronobiol Int. 2020;37(12):1709-1724. doi: 10.1080/07420528.2020.1830792
22. Kurhaluk N, Tkachenko H. Melatonin and alcohol-related disorders. Chronobiol Int. 2020;37(6):781-803. doi: 10.1080/07420528.2020.1761372.
23. Kurhaluk N, Zaitseva OV, Sliuta A, Kyriienko S, Winklewski PJ. Melatonin diminishes oxidative stress in plasma, retains erythrocyte resistance and restores white blood cell count after low dose lipopolysaccharide exposure in mice. Gen Physiol Biophys. 2018;37(5):571-580. doi: 10.4149/gpb_2018010
24. Kurhalyuk N, Tkachenko H. L-arginine modulates mitochondrial function in rat liver during physical training. J Vet Res. 2007;51:641–647.
25. Kurhalyuk NM, Serebrovskaya TV, Kolesnikova EE. Role of cholino- and adrenoreceptors in regulation of rat antioxidant defense system and lipid peroxidation during adaptation to intermittent hypoxia. Probl Eco. Med Genet Cell Immunol. 2001;7:126-137. [In Ukrainian].
26. Lacoste MG, Ponce IT, Golini RL, Delgado SM, Anzulovich AC. Aging modifies daily variation of antioxidant enzymes and oxidative status in the hippocampus. Exp Gerontol. 2017;88:42-50. doi: 10.1016/j.exger.2016.12.002
27. Luk'ianova LD Molekuliarnye mekhanizmy tkanevoĭ gipoksii i adaptatsii organizma [Molecular mechanisms of tissue hypoxia and organism adaptation]. Fiziol Zh, 2003;49(3):17-35. (In Russian).
28. Lukyanova LD, Kirova YI, Germanova EL. The Role of Succinate in Regulation of Immediate HIF-1α Expression in Hypoxia. Bull Exp Biol Med. 2018;164(3):298-303. doi:10.1007/s10517-018-3976-2
29. Lukyanova LD, Kirova YI. Mitochondria-controlled signaling mechanisms of brain protection in hypoxia. Front Neurosci. 2015;9:320. doi: 10.3389/fnins.2015.00320
30. Lukyanova LD, Kirova YI. Effect of hypoxic preconditioning on free radical processes in tissues of rats with different resistance to hypoxia. Bull Exp Biol Med. 2011;151(3):292-6. English, Russian. doi: 10.1007/s10517-011-1312-1
31. Mármol F, Sánchez J, López D, Martínez N, Mitjavila MT, Puig-Parellada P. Oxidative stress, nitric oxide and prostaglandin E2 levels in the gastrointestinal tract of aging rats. J Pharm Pharmacol. 2009;61(2):201-6. doi: 10.1211/jpp/61.02.0009
32. Mármol F, Sánchez J, López D, Martínez N, Xaus C, Peralta C, Roselló-Catafau J, Mitjavila MT, Puig-Parellada P. Role of oxidative stress and adenosine nucleotides in the liver of aging rats. Physiol Res. 2010;59(4):553-560. doi: 10.33549/physiolres.931768
33. McClung CA. Circadian rhythms and mood regulation: insights from pre-clinical models. Eureuropsychopharmacol. 2011;21 Suppl 4(Suppl 4):S683-93. doi:10.1016/j.euroneuro.2011.07.008
34. Miyazawa T. Lipid hydroperoxides in nutrition, health, and diseases. Proc Jpn Acad Ser B Phys Biol Sci. 2021;97(4):161-196. doi: 10.2183/pjab.97.010
35. Mortola JP. Gender and the circadian pattern of body temperature in normoxia and hypoxia. Respir Physiol Neurobiol. 2017;245:4-12. doi: 10.1016/j.resp.2016.11.002
36. Mortola JP. Hypoxia and circadian patterns. Respir Physiol Neurobiol. 2007;158(2-3):274-9. doi:10.1016/j.resp.2007.02.005
37. Niki E. Lipid peroxidation products as oxidative stress biomarkers. Biofactors. 2008;34(2):171-80. doi:10.1002/biof.5520340208
38. Padhy G, Sethy NK, Ganju L, Bhargava K. Abundance of plasma antioxidant proteins confers tolerance to acute hypobaric hypoxia exposure. High Alt Med Biol. 2013;14(3):289-97. doi:10.1089/ham.2012.1095
39. Peek CB, Levine DC, Cedernaes J, Taguchi A, Kobayashi Y, Tsai SJ, Bonar NA, McNulty MR, Ramsey KM, Bass J. Circadian Clock Interaction with HIF1α Mediates Oxygenic Metabolism and Anaerobic Glycolysis in Skeletal Muscle. Cell Metab. 2017;25(1):86-92. doi: 10.1016/j.cmet.2016.09.010
40. Pré J. La lipopéroxydation [Lipid peroxidation]. Pathol Biol (Paris), 1991;39(7):716-736. [In French].
41. Reiter RJ, Tan DX, Terron MP, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol. 2007;54(1):1-9. Epub 2007 Mar 9. PMID: 17351668
42. Rubio C, Lizárraga E, Álvarez-Cilleros D, Pérez-Pardo P, Sanmartín-Salinas P, Toledo-Lobo MV, Alvarez C, Escrivá F, Fernández-Lobato M, Guijarro LG, Valverde AM, Carrascosa JM. Aging in Male Wistar Rats Associates With Changes in Intestinal Microbiota, Gut Structure, and Cholecystokinin-Mediated Gut-Brain Axis Function. J Gerontol A Biol Sci Med Sci. 2021;76(11):1915-1921. doi: 10.1093/gerona/glaa313
43. Serebrovskaya TV, Xi L. (2012). Individualized intermittent hypoxia training: principles and practices. In: Intermittent Hypoxia and Human Diseases, L. Xi and T. Serebrovskaya, Eds., Springer: London, UK.
44. Strauss E, Waliszewski K, Oszkinis G, Staniszewski R. Polymorphisms of genes involved in the hypoxia signaling pathway and the development of abdominal aortic aneurysms or largeartery atherosclerosis. J Vasc Surg. 2015;61(5):1105-13.e3. doi: 10.1016/j.jvs.2014.02.007
45. Tian L, Cai Q, Wei H. Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radic Biol Med. 1998;24(9):1477-84. doi: 10.1016/s0891-5849(98)00025-2
46. Tkachenko H, Kurhalyuk N, Khabrovska L, Kamiński P. Effect of L-arginine on lead induced oxidative stress in the blood of rats with different resistance to hypoxia. Pol J Food Nutr Sci. 2007;57(3):387-394.
47. Travaglio M, Ebling FJP. Role of hypothalamic tanycytes in nutrient sensing and energy balance. Proc Nutr Soc. 2019;78(3):272-278. doi: 10.1017/S0029665118002665
48. Ubuka T, Bentle GE. (2011). Neuroendocrine control of reproduction in birds. In: D.O. Norris, K.H. Lopez (Eds.), Hormones and Reproduction of Vertebrates. Academic Press, London, p. 1-25.
49. Urbanski HF, Sorwell KG. Age-related changes in neuroendocrine rhythmic function in the rhesus macaque. Age (Dordr). 2012;34(5):1111-21. doi: 10.1007/s11357-011-9352-z
50. van der Klein SAS, Zuidhof MJ, Bédécarrats GY. Diurnal and seasonal dynamics affecting egg production in meat chickens: A review of mechanisms associated with reproductive dysregulation. Anim Reprod Sci. 2020;213:106257. doi: 10.1016/j.anireprosci.2019.106257
51. Yan L, Lonstein JS, Nunez AA. Light as a modulator of emotion and cognition: Lessons learned from studying a diurnal rodent. Horm Behav. 2019;111:78-86. doi: 10.1016/j.yhbeh.2018.09.003
52. Zar, J.H. (1999). Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey.
53. Zhang HJ, Xu L, Drake VJ, Xie L, Oberley LW, Kregel KC. Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. FASEB J. 2003;17(15):2293-5. doi: 10.1096/fj.03-0139fje