Species- and age-dependent distribution of retinol and α-tocopherol in the Canidae family during the cold season
DOI:
https://doi.org/10.21638/spbu03.2021.304Abstract
Vitamins A and E are known as nutrients involved in metabolic processes and facilitating the adaptation of animals. The metabolism of these vitamins is closely related to lipid metabolism, which has seasonal variations in animals inhabiting northern latitudes. The aim of this study was to investigate the concentrations of retinol (vitamin A) and α-tocopherol (vitamin E) in the cold season (October to February) in tissues of Canidae species that have different ecological characteristics: the blue fox (Vulpes syn. Alopex lagopus), silver fox (Vulpes vulpes), their interspecific hybrids (Vulpes×Vulpes), raccoon dog (Nyctereutes procyonoides), and grey wolf (Canis lupus). In addition, age-related differences in the levels of these vitamins were determined. Results showed the distribution of retinol and α-tocopherol in the body of the canids was similar, with larger amounts being found in the liver and kidney cortex, which play a regulatory role in the metabolism of these nutrients. The higher retinol level in the liver of wolves and interspecific hybrids of blue fox and silver fox, as compared to the retinol level in the liver of other species, might be species-specific and could also be attributed to dietary differences. The blue fox and raccoon dog both have a higher capacity for α-tocopherol accumulation in the cold season, apparently due to their ability to store substantial fat reserves. Retinol and α-tocopherol levels were generally higher in the tissues of mature animals.
Keywords:
canids, cold season, ecological features, retinol, α-tocopherol
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References
Ahlstrom, O., Fuglei, E., and Mydland, L. T. 2003. Comparative nutrient digestibility of arctic foxes (Alopex lagopus) on Svalbard and farm-raised blue foxes (Alopex lagopus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 134(1):63–68. https://doi.org/10.1016/S1095-6433(02)00184-8
Asikainen, J., Mustonen, A. M., Nieminen, P., Pasanen, S., Araja-Matilainen, H., and Hyvärinen, H. 2002. Reproduction of the raccoon dog (Nyctereutes procyonoides) after feeding or food deprivation in winter. Journal of Animal Physiology and Animal Nutrition 86:367–375. https://doi/10.1046/j.1439-0396.2002.00389.x
Audet, A. M., Robbins, C. B., and Larivière, S. 2002. Alopex lagopus. Mammalian Species 713:1–10. https://doi.org/10.1644/1545-1410(2002)713<0001:AL>2.0.CO;2
Bechshøft, T. Ø., Jakobsen, J., Sonne, C., and Dietz, R. 2011. Distribution of vitamins A (retinol) and E (α-tocopherol) in polar bear kidney: implications for biomarker studies. Science of the Total Environment 409:3508–3511. https://doi.org/10.1016/j.scitotenv.2011.05.036
Bechshøft, T. Ø., Sonne, C., Jakobsen, J., Rigét, F. F., Born, E. W., Letcher, R. J., Jenssen, B. M., and Dietz, R. 2016. Vitamins A and E in liver, kidney, and whole blood of East Greenland polar bears sampled 1994-2008: reference values and temporal trends. Polar Biology 39:743–754. https://doi.org/10.1007/s00300-015-1830-9
Blaner, W. S., O'Byrne, S. M., Wongsiriroj, N., Kluwe, J., D'Ambrosio, D. M., Jiang, H., Schwabe, R. F., Hillman, E. M., Piantedosi, R., and Libien, J. 2009. Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage. Biochimica et Biophysica Acta 1791(6):467–473. https://doi.org/10.1016/j.bbalip.2008.11.001
Blomhoff, R., Berg, T., and Norum, K. R. 1988. Distribution of retinol in rat liver cells: effect of age, sex and nutritional status. British Journal of Nutrition 60:233–239. https://doi.org/10.1079/BJN19880095
Blomhoff, R. and Blomhoff, H. K. 2006. Overview of retinoid metabolism and function. Journal of Neurobiology 66:606–630. https://doi.org/10.1002/neu.20242
Bonet, M. L., Oliver, J., Picó, C., Felipe, F., Ribot, J., Cinti, S., and Palou, A. 2000. Opposite effects of vitamin A deficient diet-feeding and retinoic acid treatment on brown adipose tissue UCP1, UCP2 and leptin expression. Journal of Endocrinology 166:511–517. https://doi.org/10.1677/joe.0.1660511
Bonet, M. L., Ribot, J., and Palou, A. 2012. Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochimica et Biophysica Acta 1821:177–189. https://doi.org/10.1016/j.bbalip.2011.06.001
Brigelius-Flohe, R. 2009. Vitamin E: The shrew waiting to be tamed. Free Radical Biology & Medicine 46:543–554. https://doi.org/10.1016/j.freeradbiomed.2008.12.007
Careau, V., Morand-Ferron, J., and Thomas, D. 2007. Basal metabolic rate of Canidae from hot deserts to cold Arctic climates. Journal of Mammalogy 88:394–400. https://doi.org/10.1644/06-MAMM-A-111R1.1
Chow, C. K. 2001. Vitamin E regulation of mitochondrial superoxide generation. Biological Signals and Receptors 10:112–124. https://doi.org/10.1159/000046879
Czaplicki, S., Ogrodowska, D., Zadernowski, R., and Konopka, I. 2017. Effect of sea-buckthorn (Hippophaë rhamnoides L.) pulp oil consumption on fatty acids and vitamin A and E accumulation in adipose tissue and liver of rats. Plant Foods for Human Nutrition 72(2):198–204. https://doi.org/10.1007/s11130-017-0610-9
Danilov, P. I., Gursky, I. G., and Kudaktin, A. N. 1985. Reproduction. In Bibikov, D. I. (ed), The Wolf. Hystory, systematics, morphology, ecology. pp. 378–389. Izdatelstvo: Nauka, Moscow. (In Russian)
Drygala, F., Werner, U., and Zoller, H. 2013. Diet composition of the invasive raccoon dog (Nyctereutes procyonoides) and the native red fox (Vulpes vulpes) in north-east Germany. Hystrix, the Italian Journal of Mammalogy 24(2):190–194. https://doi.org/10.4404/hystrix-24.2-8867
Estornell, E., Tormo, J. R., Marín, P., Renau-Piqueras, J., Timoneda, J., and Barber, T. 2000. Effects of vitamin A deficiency on mitochondrial function in rat liver and heart. British Journal of Nutrition 84:927–934. https://doi.org/10.1017/S0007114500002567
Gieng, S. H., Raila, J., and Rosales F. J. 2005. Accumulation of retinol in the liver after prolonged hyporetinolemia in the vitamin A-sufficient rat. Journal of Lipid Research 46(4):641–649. https://doi.org/10.1194/jlr.M400415-JLR200
Ginn, B. R. 2017. The thermodynamics of protein aggregation reactions may underpin the enhanced metabolic efficiency associated with heterosis, some balancing selection, and the evolution of ploidy levels. Progress in Biophysics and Molecular Biology 126:1–21. https://doi.org/10.1016/j.pbiomolbio.2017.01.005
Gugołek, A., Strychalski, J., Konstantynowicz, M., and Zwoliñski, C. 2014. Comparative analysis of nutrient digestibility and nitrogen retention in wild and farmed canids. Annals of Animals Science 14:307–314. https://doi.org/10.2478/aoas-2014-0002
Guillen, J. 2012. FELASA guidelines and recommendations. The Journal of the American Association for Laboratory Animal Science 51(3):311–321.
Ilukha, V. A. 2003. Superoxide dismutase and catalase in organs of three Canidae species. Scientifur 26:101–104.
Ilyina, T., Baishnikova, I., Belkin, V., and Ruokolaynen, T. 2014. Vitamins A and E in physiological adaptation of mammals with different ecogenesis. Acta Biologica Universitatis Daugavpiliensis 14:45–50.
Ilyina, T. N. and Baishnikova, I. V. 2014. Vitamins A and E content in the cortical and medullary kidney layers of mammals. Transactions of Karelian Research Centre of Russian Academy of Science. Experimental biology 5:218–221.
Jurczuk, M., Brzуska, M. M., and Moniuszko-Jakoniuk, J. 2007. Hepatic and renal concentrations of vitamins E and C in lead- and ethanol-exposed rats. An assessment of their involvement in the mechanisms of peroxidative damage. Food and Chemical Toxicology 45(8):1478–1486. https://doi.org/10.1016/j.fct.2007.02.007
Käkelä, R. and Hyvärinen, H. 1996. Site-specific fatty acid composition in adipose tissues of several northern aquatic and terrestrial mammals. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 115:501–514. https://doi.org/10.1016/S0305-0491(96)00150-2
Käkelä A., Käkelä R., and Hyvärinen H. 2003. Importance of the kidneys in metabolism of vitamins A1 and A2 and their fatty acyl esters in mink feeding on fish-based diets and exposed to Aroclor 1242. Toxicology and Applied Pharmacology 187(2):118–127. https://doi.org/10.1016/s0041-008x(02)00067-4
Kalabukhov, N. I. 1985. Dormancy in mammals. 260 pp. Nauka Publ., Moscow. (In Russian)
Kirkegaard, M., Sonne, C., Dietz, R., Jenssen, B. M., and Letcher, R. J. 2010. Organohalogens in a whale blubber supplemented diet affects hepatic retinol and renal tocopherol concentrations in Greenland sled dogs (Canis familiaris). Journal of Toxicology and Environmental Health Part A 73:773–786. https://doi.org/10.1080/15287391003689192
Kreeger, T. J., DelGiudice, G. D., and Mech, L. D. 1997. Effects of fasting and refeeding on body composition of captive gray wolves (Canis lupus). Canadian Journal of Zoology 75:1549–1552. https://doi.org/10.1139/z97-781
Łapa, P., Łapiński, S., Śliwiak, W., and Barabasz, B. 2009. Genetic distances between the raccoon dog (Nyctereutes procyonoides) and some other Canidae spesies. Vavilov Journal of Genetics and Breeding 13:647–654.
Lee, Y. M., Lee, J. O., Jung, J.-H., Kim, J. H., Park, S.-H., Park, J. M., Kim, E.-K., Suh, P.-G., and Kim, H. S. 2008. Retinoic acid leads to cytoskeletal rearrangement through AMPK–Rac1 and stimulates glucose uptake through AMPK–p38 MAPK in skeletal muscle cells. The Journal of Biological Chemistry 283:33969–33974. https://doi.org/10.1074/jbc.M804469200
Lefebvre, C., Crete, M., Huot, J., and Patenaude, R. 1999. Prediction of body composition of live and post-mortem red foxes. Journal of Wildlife Diseases 35:161–170. https://doi.org/10.7589/0090-3558-35.2.161
Lewis, K. C., Green, M. H., Green, J. B., and Zech, L. A. 1990. Retinol metabolism in rats with low vitamin A status: a compartmental model. Journal of Lipid Research 31:1535–1548. https://doi.org/10.1016/S0022-2275(20)42338-7
Machlin, L. J., and Gabriel, E. 1982. Kinetics of tissue α-tocopherol uptake and depletion following administration of high levels of vitamin E. Annals of the New York Academy of Sciences 393:48–60. https://doi.org/10.1111/j.1749-6632.1982.tb31231.x
Majchrzak, D., Fabian, E., and Elmadfa, I. 2006. Vitamin A content (retinol and retinyl esters) in livers of different animals. Food Chemistry 98(4):704–710. https://doi.org/10.1016/j.foodchem.2005.06.035
Mills, J. P., Penniston, K. L., and Tanumihardjo, S. A. 2005. Extra-hepatic vitamin A concentrations in captive rhesus (Macaca mulatta) and marmoset (Callithrix jacchus) monkeys fed excess vitamin A. International Journal for Vitamin and Nutritional Research 75(2):126–132. https://doi.org/10.1024/0300-9831.74.2.126
Mustonen, A.-M., Pyykönen, T., Puukka, M., Asikainen, J., Hänninen, S., Mononen, J., and Nieminen, P. 2006. Physiological adaptations to fasting in an actively wintering Canid, the Arctic blue fox (Alopex lagopus). Journal of Experimental Zoology. Part A: Comparative Experimental Biology 305:32–46. https://doi.org/10.1002/jez.a.241
Mustonen, A.-M., Käkelä, R., Käkelä, A., Pyykönen, T., Aho, J., and Nieminen, P. 2007. Lipid metabolism in the adipose tissues of a Carnivore, the raccoon dog, during prolonged fasting. Experimental Biology and Medicine 232:58–69. https://doi.org/10.3181/00379727-207-2320058
Nagy, N. E., Holven, K. B., Roos, N., Senoo, H., Kojha, N., Norum, K. R., and Blomhoff, R. 1997. Storage of vitamin A in extrahepatic stellate cells in normal rats. Journal of Lipid Research 38:645–658. https://doi.org/10.1016/S0022-2275(20)37232-1
Nes, N. N., Einarsson, E. J., Lohi, O., Jørgensen, G., Jarosz, S. J., and Scheelje, R. 1988. Beautiful fur animals — and their colour genetics. 271 pp. Glostrup, Denmark: Scientifur.
Nowicki, S., Przysiecki, P., Filistowicz, A., Potkański, A., Filistowicz, A., and Wójtowski, J. 2014. The effect of different fat sources in the diet on the composition of adipose tissue in arctic foxes (Alopex lagopus L.). Folia Biologica 62:127–133. https://doi.org/10.3409/fb62_2.127
Olivares, A., Rey, A. I., Daza, A., and Lopez-Bote, C. J. 2009. High dietary vitamin A interferes with tissue a-tocopherol concentrations in fattening pigs: a study that examines administration and withdrawal times. Animal 3(9):1264–1270. https://doi.org/10.1017/S175173110900487X
Pan, J. and Baker, K. M. 2007. Retinoic acid and the heart. Vitamins & Hormones 75:257–283. https://doi.org/10.1016/S0083-6729(06)75010-5
Patel, J. M., Sekharam, M., and Block, E. R. 1991. Vitamin E distribution and modulation of the physical state and function of pulmonary endothelial cell membranes. Experimental Lung Research 17:707–723. https://doi.org/10.3109/01902149109062874
Prestrud, P. 1991. Adaptations by the arctic fox (Alopex lagopus) to the polar winter. Arctic 44:132–138. https://doi.org/10.14430/arctic1529
Raila, J., Buchholz, I., Aupperle, H., Raila, G., Schoon, H.-A., and Schweigert, F. J. 2000. The distribution of vitamin A and retinol-binding protein in the blood plasma, urine, liver and kidneys of carnivores. Veterinary Research 31:541–551. https://doi.org/10.1051/vetres:2000138
Raila, J., Mathews, U., and Schweigert, F. J. 2001. Plasma transport and tissue distribution of b-carotene, vitamin A and retinol-binding protein in domestic cats. Comparative Biochemistry and Physiology Part A 130(4):849–856. https://doi.org/10.1016/s1095-6433(01)00443-3
Reimers, N. F. and Bibikov, D. I. 1985. Range and its modification. In Bibikov, D. I. (ed), The Wolf. Hystory, systematics, morphology, ecology. pp. 51–63. Nauka Publ., Moscow. (In Russian)
Ribaya-Mercado, J. D., Fox, J. G., Rosenblad, W. D., Blanco, M. C., and Russell, R. M. 1992. Beta-carotene, retinol and retinyl ester concentrations in serum and selected tissues of ferrets fed beta-carotene. The Journal of Nutrition 122:(9)1898–1903. https://doi.org/10.1093/jn/122.9.1898
Rogstad, T. W., Sonne, C., Villanger, G. D., Ahlstøm, Ø., Fuglei, E., Muir, D. C. G., Jørgensen, E., and Jenssen, B. M. 2017. Concentrations of vitamin A, E, thyroid and testosterone hormones in blood plasma and tissues from emaciated adult male Arctic foxes (Vulpes lagopus) dietary exposed to persistent organic pollutants (POPs). Environmental Research 154:284–290. https://doi.org/10.1016/j.envres.2017.01.017
Rouvinen, K. 1991. Dietary effects of omega-3 polyunsaturated fatty acids on body fat composition and health status of farm-raised blue and silver foxes. Acta Agriculturae Scandinavica 41:401–414. https://doi.org/10.1080/00015129109439923
Schweigert, F. J., Buchholz, I., and Bonitz, K. 1998. Effect of age on the levels of retinyl esters in blood, plasma, liver and kidney of dogs. International Journal for Vitamin and Nutrition Research 68:237–241.
Schweigert, F. J., Raila, J., and Haebel, S. 2002. Vitamin A excreted in the urine of canines is associated with a Tamm-Horsfall like protein. Veterinary Research 33:299–311. https://doi.org/10.1051/vetres:2002018
Senoo, H., Wake, K., Wold, H. L., Higashi, N., Imai, K., Moskaug, J. Ø., Kojima, N., Miura, M., Sato, T., Sato, M., Roos, N., Berg, T., Norum, K. R., and Blomhoff, R. 2004. Decreased capacity for vitamin A storage in hepatic stellate cells for arctic animals. Comparative Hepatology 3(Suppl 1):S18. https://doi.org/10.1186/1476-5926-2-S1-S18
Senoo, H., Imai, K., Mezaki, Y., Miura, M., Morii, M., Fujiwara, M., and Blomhoff, R. 2012. Accumulation of vitamin A in the hepatic stellate cell of arctic top predators. The Anatomical Record 295:1660–1668. https://doi.org/10.1002/ar.22555
Shirakami, Y., Lee, S.-A., Clugston, R. D., and Blaner, W. S. 2012. Hepatic metabolism of retinoids and disease associations. Biochimica et Biophysica Acta 1821(1):124–136. https://doi.org/10.1016/j.bbalip.2011.06.023
Stahler, D. R., Smith, D. W., and Guernsey, D. S. 2006. Foraging and feeding ecology of the gray wolf (Canis lupus): lessons from Yellowstone National Park, Wyoming, USA. The Journal of Nutrition 136:1923S–1926S. https://doi.org/10.1093/jn/136.7.1923S
Strychalski, J., Gugołek, A., Brym, P., and Antoszkiewicz, Z. 2019. Effect of the β-carotene oxygenase 2 genotype on the content of carotenoids, retinol and α-tocopherol in the liver, fat and milk of rabbit does, reproduction parameters and kitten growth. Journal of Animal Physiology and Animal Nutrition 103(5):1585–1593. https://doi.org/10.1111/jpn.13130
Sun, T., Surles, R. L., and Tanumihardjo, S. A. 2008. Vitamin A concentrations in piglet extrahepatic tissues respond differently ten days after vitamin A treatment. The Journal of Nutrition 138:1101–1106. https://doi.org/10.1093/jn/138.6.1101
Tauson, A.-H., Chwalibog, A., and Ahlstrøm, Ø. 2002. Substrate oxidation in male blue fox (Alopex lagopus) during feeding, fasting and realimentation. The Journal of Nutrition 132:1793–1795. https://doi.org/10.1093/jn/132.6.1793S
Traber, M. G., Ingold, K. U., Burton, G. W., and Kayden, H. J. 1988. Absorption and transport of deuterium-substituted 2R, 4'R, 8'R alpha-tocopherol in human lipoproteins. Lipids 23:791–797. https://doi.org/10.1007/BF02536223
Traber, M. G. 2013. Mechanisms for the prevention of vitamin E excess. The Journal of Lipid Research 54:2295–2306. https://doi.org/10.1194/jlr.R032946
Tumanov, I. L. 2003. Bioligocal characteristics of carnivores mammals of Russia. 448 pp. Nauka Publ., Saint-Petersburg. (In Russian)
Valk, E. E. J. and Hornstra, G. 2000. Relationship between vitamin E requirement and polyunsaturated fatty acid intake in man: a review. International Journal for Vitamin and Nutrition Research 70:31–42. https://doi.org/10.1024/0300-9831.70.2.31
Venditti, P., Di Stefano, L., and Di Meo, S. 2009. Vitamin E reduces cold-induced oxidative stress in rat skeletal muscle decreasing mitochondrial H2O2 release and tissue susceptibility to oxidants. Redox Report 14:165–175. https://doi.org/10.1179/135100009X466113
Villaroya, F., Giralt, M., and Iglesias, R. 1999. Retinoids and adipose tissues: metabolism, cell differentiation and gene expression. International Journal of Obesity 23:1–6. https://doi.org/10.1038/sj.ijo.0800799
Wang, F., Wang, T., Lai, J., Li, M., and Zou, C. 2006. Vitamin E inhibits hemolysis induced by hemin as a membrane stabilizer. Biochemical Pharmacology 71:799–805. https://doi.org/10.1016/j.bcp.2005.12.002
Winklhofer-Roob, B. M., van’t Hof, M. A., and Shmerling, D. H. 1997. Reference values for plasma concentrations of vitamin E and A and carotenoids in a Swiss population from infancy to adulthood, adjusted for seasonal influences. Clinical Chemistry 43:146–153. https://doi.org/10.1093/clinchem/43.1.146
Yang, T. A., Yang, Y. H., Peng, Y. H., Cong, B., Diao, Y. F., Bao, K., Hu, P. F., Song, X. C., Liu, L. L., Yang, Y. F., Xing, X. M., and Yang, F. H. 2016. Comparative studies on testicular and epididymal morphology, and serum hormone concentrations in foxes and the hybrids during the breeding season. Animal Reproduction Science 168:66–72. https://doi.org/10.1016/j.anireprosci.2016.02.027
Zrzavý, J., Duda, P., Robovský, J., Okřinová I., and Pavelková Řičánková, V. 2018. Phylogeny of the Caninae (Carnivora): Combining morphology, behaviour, genes and fossils. Zoologica Scripta 47:373–389. https://doi.org/10.1111/zsc.12293
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2021-11-12
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Baishnikova, I., Ilyina, T., Ilyukha, V., & Tirronen, K. (2021). Species- and age-dependent distribution of retinol and α-tocopherol in the Canidae family during the cold season. Biological Communications, 66(3), 225–235. https://doi.org/10.21638/spbu03.2021.304
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