Abstract
Phenotypic plasticity and resistance to climatic conditions allowed the wild boar Sus scrofa L. to expand its historical range and move away its Northern border. For the adaptation to living at the periphery of its range under severe conditions of the North, the status of vitamins A and E, which are natural antioxidants critical for growth, reproduction and immunity maintenance, is of vital importance. The aim of this work was to investigate the content of retinol, α-tocopherol, and the low-molecular-weight antioxidant glutathione (GSH) in the liver, kidney, heart, skeletal muscle, lungs, and spleen of the wild boars (n = 65) aged 0.5–8 years, living in the Northwest of Russia. Our results indicate that the studied animals practically did not differ in the retinol content from their counterparts living in the Central and Southern Europe, but had lower tissue α-tocopherol levels, which is probably due to the limited food resources and harsh climatic conditions of the cold season in the North. Vitamin and GSH levels in most tissues were comparable in piglets and adult animals. With age, retinol and α-tocopherol accumulated in the liver and kidney, while α-tocopherol alone accumulated in the heart, which is typical for other mammalian species. An increase in the GSH level was found in the lungs of animals over 5 years of age. The revealed vitamin status, which was formed in the wild boar under conditions of the Russia’s Northwest, as well as the peculiarities of the age-related dynamics of the above indices, may serve a compelling evidence for the successful adaptation of this species to inhabiting the northern periphery of its range, as confirmed by the growth of its population.
REFERENCES
Panchenko DV, Danilov PI, Tirronen KF, Paasivaara A, Krasovsky YuA (2019) Features of ungulates distribution in the Karelian part of the Green Belt of Fennoscandia. Transactions of the Karelian Research Centre of the Russian Academy of Sciences 4: 119–128. https://doi.org/10.17076/them997
Danilov PI, Panchenko DV (2012) Settlement and some features of the boar ecology beyond the northern limit of its historical range in the European part of Russia. Ecology 1: 48–54. (In Russ).
Castillo-Contreras R, Mentaberre G, Aguilar XF, Conejero C, Colom-Cadena A, Ráez-Bravo A, González-Crespo C, Espunyes J, Lavín S, López-Olvera JR (2021) Wild boar in the city: Phenotypic responses to urbanization. Sci Total Environ 773: 145593. https://doi.org/10.1016/j.scitotenv.2021.145593
Żmijewski T, Modzelewska-Kapituła M (2021) The influence of age and sex on carcass characteristics and chemical composition of the longissimus thoracis et lumborum muscle in wild boars (Sus scrofa). Arch Anim Breed 1: 199–210. https://doi.org/10.5194/aab-64-199-2021
Danilkin AA (2002) The Pigs (Suidae). GEOS, M. (In Russ).
Korchina TY, Korchin VI (2014) Vitamins and trace elements: features of the northern region. Ugra news, Khanty-Mansiysk. (In Russ).
Van der Loo B, Labugger R, Aebischer CP, Bachschmid M, Spitzer V, Kilo J, Altwegg L, Ullrich V, Lüscher TF (2004) Age-related changes of vitamin A status. J Cardiovasc Pharmacol 1: 26–30. https://doi.org/10.1097/00005344-200401000-00005
Debier C, Larondelle Y (2005) Vitamins A and E: metabolism, roles and transfer to offspring. Br J Nutr 2: 153–174. https://doi.org/10.1079/bjn20041308
Azzi A (2018) Many tocopherols, one vitamin E. Mol Aspects Med 61: 92–103. https://doi.org/10.1016/j.mam.2017.06.004
Brigelius-Flohé R (2002) The European perspective on vitamin E: current knowledge and future research. Am J Clin Nutr 4: 703–716. https://doi.org/10.1093/ajcn/76.4.703
Blomhoff R, Blomhoff HK (2006) Overview of retinoid metabolism and function. J Neurobiol 7: 606–630. https://doi.org/10.1002/neu.20242
Zhang Y, Zhao Y, Li C, Wang L, Tian F, Jin H (2022) Physiological, Immune Response, Antioxidant Capacity and Lipid Metabolism Changes in Grazing Sheep during the Cold Season. Animals 12: 2332. https://doi.org/10.3390/ani12182332
Kalinina EV, Chernov NN, Novichkova MD (2014) The role of glutathione, glutathione transferase and glutaredoxin in the regulation of redox-dependent processes. Uspekhi biologicheskoi khimii 54: 299–348. (In Russ).
van Haaften RIM, Haenen GRMM, Evelo CTA, Bast A (2003) Effect of vitamin E on glutathione-dependent enzymes. Drug Metab Rev 35(2–3): 215–253. https://doi.org/10.1081/DMR-120024086
Dannenberger D, Nuernberg G, Nuernberg K, Hagemann E (2013) The effects of gender, age and region on macro- and micronutrient contents and fatty acid profiles in the muscles of roe deer and wild boar in Mecklenburg-Western Pomerania (Germany). Meat Sci 1: 39–46. https://doi.org/10.1016/j.meatsci.2012.12.010
Quaresma MAG, Alves SP, Trigo-Rodrigues I, Pereira-Silva R, Santos N, Lemos JPC, Barreto AS, Bessa RJB (2011) Nutritional evaluation of the lipid fraction of feral wild boar (Sus scrofa scrofa) meat. Meat Sci 89: 457–461. https://doi.org/10.1016/j.meatsci.2011.05.005
Soriano A, Sánchez-García C (2021) Nutritional composition of game meat from wild species harvested in Europe. In: Ranabhat ChL (ed) Meat and Nutrition. https://doi.org/10.5772/intechopen.97763
Ortiz A, García-Torres S, González E, De Pedro-Sanz EJ, Gaspar P, Tejerina D (2020) Quality traits of fresh and dry-cured loin from Iberian x Duroc crossbred pig in the Montanera system according to slaughtering age. Meat Sci 170: 108242. https://doi.org/10.1016/j.meatsci.2020.108242
Lebret B, Lenoir H, Fonseca A, Riquet J, Mercat MJ (2021) Finishing season and feeding resources influence the quality of products from extensive-system Gascon pigs. Part 2: muscle traits and sensory quality of dry-cured ham. Animal 15(8): 100305. https://doi.org/10.1016/j.animal.2021.100305
Rodríguez-Estival J, Álvarez-Lloret P, Rodríguez-Navarro AB, Mateo R (2013) Chronic effects of lead (Pb) on bone properties in red deer and wild boar: Relationship with vitamins A and D3. Environ Pollut 174: 142–149. https://doi.org/10.1016/j.envpol.2012.11.019
Kalinina SN, Panchenko DV, Baishnikova IV, Antonova EP, Ilyukha VA, Shakun VV, Zaytseva IA (2020) Antioxidant and vitamin status in wild boar Sus Scrofa L. (Artiodactyla) on the range periphery (Republic of Karelia). Transactions Kola Science Centre 11(8): 83–92. https://doi.org/10.37614/2307-5252.2020.2.8.008
Klevezal GA (2007) Principles and methods of age determination of mammals. KMK Sci Press Ltd, M. (In Russ).
Lowry OH, Rosenbrough NJ, Farr AL, Randan RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1): 265–275.
Markov N, Economov A, Hjeljord O, Rolandsen CM, Bergqvist G, Danilov P, Dolinin V, Kambalin V, Kondratov A, Krasnoshapka N, Kunnasranta M, Mamontov V, Panchenko D, Senchik A (2022) The wild boar Sus scrofa in northern Eurasia: a review of range expansion history, current distribution, factors affecting the northern distributional limit, and management strategies. Mammal Rev 52(4): 519–537. https://doi.org/10.1111/mam.12301
Chen J, Jakovlić I, Zhong J, Jia Y, Thi TNT, Sablin M, Xia S, Yang H, Šprem N, Yang G, Jianlin H (2022) Whole-Genome Sequencing Reveals Positive Selection on Genes and Variants underlying the Climatic Adaptation of Cold-region Wild Boar. Authorea. https://doi.org/10.22541/au.165942186.69235808/v1
Landrier JF, Marcotorchino J, Tourniaire F (2012) Lipophilic Micronutrients and Adipose Tissue Biology. Nutrients 4: 1622–1649. https://doi.org/10.3390/nu4111622
Bonet ML, Ribot J, Palou A (2012) Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochim Biophys Acta 1821: 177–189. https://doi.org/10.1016/j.bbalip.2011.06.001
Raila J, Willnow TE, Schweigert FJ (2005) Megalin-Mediated Reuptake of Retinol in the Kidneys of Mice Is Essential for Vitamin A Homeostasis. J Nutr 135: 2512–2516. https://doi.org/10.1093/jn/135.11.2512
Sun T, Surles RL, Tanumihardjo SA (2008) Vitamin A concentrations in piglet extrahepatic tissues respond differently ten days after vitamin A treatment. J Nutr 138: 1101–1106. https://doi.org/10.1093/jn/138.6.1101
O’Sullivan ED, Hughes J, Ferenbach DA (2017) Renal aging: causes and consequences. J Am Soc Nephrol 28: 407–420. https://doi.org/10.1681/ASN.2015121308
Traber MG (2007) Vitamin E regulatory mechanisms. Annu Rev Nutr 27: 347–362. https://doi.org/10.1146/annurev.nutr.27.061406.093819
Rodríguez-Estival J, Taggart MA, Mateo R (2011) Alterations in vitamin A and E levels in liver and testis of wild ungulates from a lead mining area. Arch Environ Contam Toxicol 60: 361–371. https://doi.org/10.1016/j.scitotenv.2011.04.010
Niculita P, Popa EM, Ghidurus M, Turtoi M (2007) Effect of vitamin E in swine diet on animal growth performance and meat quality parameters. Polish J Food Nutr Sci 57(1): 125–130.
Kulpin AA (2008) Peculiarities of biotopic distribution and feeding of wild boar (Sus Scrofa L.) in the north of the European part of Russia. Vestnik of Lobachevsky University of Nizhni Novgorod 2: 82–86. (In Russ).
Vapirov VV, Chazhengina EA (2019) Selenium status of environmental sites the Republic of Karelia. Ecological geology: theory, practice and regional problems. Materials of the VI International Scientific and Practical Conference 16–19. (In Russ).
Surai PF (2003) Selenium-vitamin E interactions: does 1+1 equal more than 2? In: Lyons TP, Jacques KA (eds) Nutritional Biotechnology in the Feed and Food Industries. Proc. of Alltech’s 19th Annual Symposium. Nottingham University Press, Nottingham; UK, 59–76.
Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Funct Ecol 23: 57–69. https://doi.org/10.1111/j.1365-2435.2008.01528.x
Babicz M, Kasprzyk A (2019) Comparative analysis of the mineral composition in the meat of wild boar and domestic pig. Ital J Anim Sci 18(1): 1013–1020. https://doi.org/10.1080/1828051X.2019.1610337
Raederstorff D, Wyss A, Calder PC, Weber P, Eggersdorfer M (2015) Vitamin E function and requirements in relation to PUFA. Br J Nutr 114(8): 1113–1122. https://doi.org/10.1017/S000711451500272X
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
Kaushik S, Kaur J (2003) Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clin Chim Acta 333(1): 69–77. https://doi.org/10.1016/S0009-8981(03)00171-2
Smirnov LP, Sukhovskaya IV (2014) Glutathione role in antioxidant protection and in functioning of biotransformation system (review). Proceedings of Petrozavodsk State University 6: 34–40. (In Russ).
Kulinsky VI, Kolesnichenko LS (2009) The glutathione system. I. Synthesis, transport, glutathione transferases, glutathione peroxidases. Biochem (Moscow) Supplement Series B: Biomed Chem 3(2): 129–144. https://doi.org/10.1134/s1990750809020036
Esposito L, Tafuri S, Cocchia N, Fasanelli R, Piscopo N, Lamagna B, Eguren V, Amici A, Iorio EL, Ciani F (2021) Assessment of living conditions in wild boars by analysis of oxidative stress markers. J Appl Anim Welf Sci 1: 64–71. https://doi.org/10.1080/10888705.2020.1790365
Elsayed NM (2001) Antioxidant mobilization in response to oxidative stress: a dynamic environmental-nutritional interaction. Nutrition 17: 828–834. https://doi.org/10.1016/S0899-9007(01)00646-3
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): S62–S66. https://doi.org/10.1164/rccm.2206019
Yudin NS, Larkin DM, Ignatieva EV (2017) A compendium and functional characterization of mammalian genes involved in adaptation to Arctic or Antarctic environments. BMC Genetics 18: 33–43. https://doi.org/10.1186/s12863-017-0580-9
Rasch I, Görs S, Tuchscherer A, Viergutz T, Metges C, Kuhla B (2020) Substitution of Dietary Sulfur Amino Acids by DL-2-Hydroxy-4-Methylthiobutyric Acid Reduces Fractional Glutathione Synthesis in Weaned Piglets. J Nutr 150(4): 722–729. https://doi.org/10.1093/jn/nxz272
Moreira I, Mahan DC (2002) Effect of dietary levels of vitamin E (all-rac-αtocopheryl acetate) with and without added fat on weanling pig performance and tissue α-tocopherol concentration. J Anim Sci 80: 663–669. https://doi.org/10.2527/2002.803663x
Berg F, Gustafson U, Andersson L (2006) The uncoupling protein 1 gene (UCP1) is disrupted in the pig lineage: a genetic explanation for poor thermoregulation in piglets. PLoS Genet 2(8): e129. https://doi.org/10.1371/journal.pgen.0020129
Buchet A, Belloc C, Leblanc-Maridor M, Merlot E (2017) Effects of age and weaning conditions on blood indicators of oxidative status in pigs. PLoS ONE 12(5): e0178487.
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This work was state budget funded for the implementation of governmental assignment to KarRC RAS (FMEN-2022-003).
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Conceptualization (D.V.P., S.N.K.), material sampling (D.V.P.), data collection and processing (I.A.Z., I.V.B., T.N.I., E.P.A.), manuscript writing (I.A.Z., I.V.B.), manuscript editing (all authors).
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The biological material was obtained from the wild boars hunted legally on the permission issued by the Hunting Department of the Ministry of Agriculture, Fisheries and Hunting of the Republic of Karelia and the Committee for the Protection, Control and Regulation of the Use of Wildlife Objects of the Leningrad Region, so that the study required no approval by the Bioethics Committee of the Karelian Research Institute of the Russian Academy of Sciences (KarRC RAS).
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Translated by A. Polyanovsky
Russian Text © The Author(s), 2023, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2023, Vol. 59, No. 3, pp. 232–242https://doi.org/10.31857/S0044452923030105.
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Zaitseva, I.A., Baishnikova, I.V., Panchenko, D.V. et al. The Content of Retinol, α-Tocopherol and Glutathione in Tissues of the Wild Boar (Sus scrofa L.) Inhabiting the Northwest of Russia. J Evol Biochem Phys 59, 744–755 (2023). https://doi.org/10.1134/S0022093023030092
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DOI: https://doi.org/10.1134/S0022093023030092