Comparison of the antioxidant system response to melatonin implant in raccoon dog (Nyctereutes procyonoides) and silver fox (Vulpes vulpes)

Svetlana SERGINA, Irina BAISHNIKOVA, Viktor ILYUKHA, Marcin LIS, Stanislaw LAPINSKI, Piotr NIEDBALA, Bougslaw BARABASZ
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The aim of this work was to investigate whether melatonin implant may modify the response of the antioxidant systems of raccoon dog and silver fox. Animals of each species were divided into 2 equal groups: implanted with 12 mg of melatonin in late June and not implanted (control). During the standard fur production process in late November, samples of tissues (liver, kidney, spleen, and heart) were collected and specific activities of superoxide dismutase (SOD) and catalase (CAT), and the contents of reduced glutathione (GSH), retinol, α-tocopherol (TCP), and total tissue protein, were determined in tissue samples. Activity of antioxidant enzymes SOD and CAT as well as concentrations of GSH and TCP were considerably higher in organs of raccoon dogs in comparison with silver foxes at the end of autumn fattening. Melatonin implants had no significant effect on the fox antioxidant system in contrast to the raccoon dog. The SOD activity in the liver, kidney, and heart of melatonin-treated raccoon dog considerably decreased, by 25% to 70%. The CAT activity was reduced in the kidney and heart, but it increased in the liver and spleen. Simultaneously, concentrations of GSH in the examined organs of the raccoon dog showed an inverse relationship with CAT activity. In summary, raccoon dogs and silver foxes differ not only in the function of the antioxidant system but also in the response of this system to exogenous melatonin. The rapid fattening evokes oxidative stress, which stimulates the activity of the antioxidant system in this species.


Key words: Catalase, glutathione, superoxide dismutase, metabolic syndrome, Canidae

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Wang X, Tedford RH, Van Valkenburgh B, Wayne RK. Phylogeny, classification and evolutionary ecology of the Canidae. In: Sillero-Zubiri C, Hoffmann M, Macdonald DW, editors. Canids: Foxes, Wolves, Jackals and Dogs Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/ SSC Canid Specialist Group; 2004. pp. 8–20.

Lapa P, Lapinski S, Sliwiak W, Barabasz B. Genetic distances between the raccoon dog, Nyctereutes procyonoides and some other Canidae species. Herald Vavilov Soc Gen Breed Sci 2009; 133: 647–654.

Asikainen J, Mustonen A, Hyvärinen H, Nieminen P. Seasonal physiology of the wild raccoon dog (Nyctereutes procyonoides). Zool Sci 2004; 21: 385–391.

Mustonen AM, Asikainen J, Aho J, Nieminen P. Selective seasonal fatty acid accumulation and mobilization in the wild raccoon dog Nyctereutes procyonoides. Lipids 2007; 423: 1155–1167.

Sutor A, Kauhala K, Ansorge H. Diet of the raccoon dog Nyctereutes procyonoides - a canid with an opportunistic foraging strategy. Acta Theriol 2010; 553: 165–176.

Lapinski S, Bzymek J, Zon A. The influence of winter fasting on sexual activity of male finnraccoons. Sci Bull LNUVMBT SZ Gzhytsky 2008; 373: 205–209.

Mustonen AM, Nieminen P, Puukka M, Asikainen J, Saarela S, Karonen SL, Kukkonen JV, Hyvärinen H. Physiological adaptations of the raccoon dog (Nyctereutes procyonoides), to seasonal fasting-fat and nitrogen metabolism and influence of continuous melatonin treatment. J Comp Physiol B 2004; 1743: 1–

Macdonald DW, Reynolds J. Red Fox, Vulpes vulpes. In: SilleroZubiri C, Hoffmann M, Macdonald DW, editors. Canids: Foxes, Wolves, Jackals and Dogs Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/ SSC Canid Specialist Group; 2004. pp. 129–136.

Hovland AL, Bakken M. Group housing of adult silver fox (Vulpes vulpes) vixens during autumn and its consequences for body weight, injuries and later reproduction: A field study. Applied Anim Behav Sci 2010; 1273: 130–138.

Nelson RJ, Demas GE. Role of melatonin in mediating seasonal energetic and immunologic adaptations. Brain Res Bull 1997; 443: 423–430.

Fischer TW, Slominski A, Tobin DT, Paus R. Melatonin and the hair follicle. J Pineal Res 2008; 443: 1–15.

Nieminen P, Kakela R, Mustonen AM, Hyvarinen H, Asikainen J. Exogenous melatonin affects lipids and enzyme activities in mink Mustela vison liver. Comp Biochem Physiol B Toxicol Pharmacol 2001; 1283: 203–211.

Reiter RJ, Paredes SD, Korkmaz A, Manchester LC, Tan DX. Melatonin in relation to the strong and weak versions of the free radical theory of aging. Adv Med Sci 2008; 533: 119–129.

Vinogradova IA, Anisimov VN, Bukalev AV, Ilyukha VA. Khizhkin EA, Lotosh TA, Semenchenko AV, Zabezhinski MA. Circadian disruption induced by light-at-night accelerates aging and promotes tumorigenesis in young but not in old rats. Aging 2010; 23: 82–92.

Vinogradova IA, Ilyukha VA, Ilina TN, Uzenbayeva LB, Fedorova AV. Effects of melatonin and epithalone on antioxidant system of rats depend on light conditions. Patol Fiziol Eksp Ter 2006; 33: 22–26.

Khizhkin EA, Ilukha VA, Ilyina TN, Unzhakov AR, Vinogradova IA, Anisimov VN. Antioxidant system and energy provision of the rat heart during aging depend on illumination regimen and are resistant to exogenous melatonin. Bull Exp Biol Med 2010; 1493: 354–358.

Skurihin VN, Dvinskaya LM. Determination of α-tocopherol and retinol in plasma of farming animals by the method of high performance liquid chromatography. Selskohozyaistvennaya Biol 1989; 43: 127–129.

Illison VK, Rondo PH, de Oliveira AM, D’Abronzo FH, Campos KF. The relationship between plasma alpha-tocopherol concentration and vitamin E intake in patients with type 2 diabetes mellitus. Int J Vitamin Nutr Res 2011; 813: 12–20.

Roberts CK, Sindhu KK. Oxidative stress and metabolic syndrome. Life Science 2009; 843: 705–712.

Roberts CK, Barnard RJ. Effects of exercise and diet on chronic disease. J Appl Physiol 2005; 983: 3–30.

Grattagliano I, Palmieri VO, Portincasa P, Moschetta A, Palasciano G. Oxidative stress-induced risk factors associated with the metabolic syndrome, a unifying hypothesis. J Nutr Biochem 2008; 193: 491–504.

Kozirog M, Poliwczak AR, Duchnowicz P, Koter-Michalak M, Sikora J, Broncel M. Melatonin treatment improves blood pressure, lipid profile, and parameters of oxidative stress in patients with metabolic syndrome. J Pineal Res 2011; 503: 261–266.

Anisimov VN. Effects of exogenous melatonin. A review. Toxicol Pathol 2003; 31: 589–603.

Ohta Y, Kongo M, Kishikawa T. Effect of melatonin on changes in hepatic antioxidant enzyme activities in rats treated with alpha-naphthylisothiocyanate. J Pineal Res 2001; 313: 370–377.

Rodriguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Reiter RJ. Regulation of antioxidant enzymes, a significant role for melatonin. J Pineal Res 2004; 363: 1–9.

Milczarek R, Hallmann A, Sokołowska E, Kaletha K, Klimek J. Melatonin enhances antioxidant action of α-tocopherol and ascorbate against NADPH- and iron-dependent lipid peroxidation in human placental mitochondria. J Pineal Res 2010; 493: 149–155.

Forsberg M, Madej A. Effects of melatonin implants on plasma concentrations of testosterone, thyroxine and prolactin in the male silver fox (Vulpes vulpes). J Reprod Fertil 1990; 893: 351– 3

Balkan J, Sener G, Cevikbaş U, Keyer-Uysal M, Uysal M. Melatonin improved the disturbances in hepatic prooxidant and antioxidant balance and hepatotoxicity induced by a high cholesterol diet in C57BL/6J mice. Int J Vitam Nutr Res 2004; 74: 349–354.

Szaroma W, Dziubek K. Changes in the amount of reduced glutathione and activity of antioxidant enzymes in chosen mouse organs influenced by zymosan and melatonin administration. Acta Biol Hung 2011; 623: 133–141.

Tan DX, Manchester LC, Fuentes-Broto L, Paredes SD, Reiter RJ. Significance and application of melatonin in the regulation of brown adipose tissue metabolism, Relation to human obesity. Obesity Rev 2011; 123: 167–188.