THE CONTENT OF RETINOL, α-TOCOPHEROL AND GLUTATHIONE IN THE TISSUES OF WILD BOAR (SUS SCROFA L.), INHABITING THE NORTHWEST OF RUSSIA
- Authors: Zaitseva I.A.1,2, Baishnikova I.V.1, Panchenko D.V.1, Kalinina S.N.1,2, Ilyina T.N.1, Antonova E.P.1
-
Affiliations:
- Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences
- Petrozavodsk State University
- Issue: Vol 59, No 3 (2023)
- Pages: 232-242
- Section: EXPERIMENTAL ARTICLES
- URL: https://cijournal.ru/0044-4529/article/view/648064
- DOI: https://doi.org/10.31857/S0044452923030105
- EDN: https://elibrary.ru/YICWRG
- ID: 648064
Cite item
Abstract
Phenotypic plasticity and resistance to climatic conditions allowed the wild boar (Sus scrofa L.) to expand its historical range, pushing its Northern border. In the processes of adaptation of animals to living on the periphery of the range in the conditions of the North, the status of vitamins A and E, which are natural antioxidants, and also perform a number of other biological functions in the body and are necessary for growth, reproduction and maintenance of immunity, is of great importance. The purpose of this study was to investigate the content of retinol, α-tocopherol, and the low-molecular-weight antioxidant glutathione (GSH) in the liver, kidney, heart, skeletal muscle, lung and spleen of wild boars (n = 65) aged 0.5 to 8 years, living in the Northwest of Russia. The results obtained indicate that the studied animals practically did not differ from the wild boars living in the сentre and south of Europe in terms of retinol availability, but were characterized by a lower level of α-tocopherol in the studied tissues, which is probably due to the limited food resources and harsh climatic conditions in the cold season in the North. The levels of vitamins and GSH in most tissues were comparable in piglets and adult animals. There was an accumulation of retinol and α-tocopherol in the liver and kidney, as well as α-tocopherol in the heart of wild boars with age, which is typical for other mammalian species. An increase in the level of GSH was found in the lung of animals over 5 years of age. The revealed vitamin status, which was formed in the wild boar in the conditions of the Northwest of Russia, and the peculiarities of the age dynamics of the studied indicators, may be one of the evidences of the successful adaptation of this species to inhabit in the Northern periphery of the range, which is confirmed by the growth of its population.
About the authors
I. A. Zaitseva
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences; Petrozavodsk State University
Author for correspondence.
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk; Russia, Petrozavodsk
I. V. Baishnikova
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk
D. V. Panchenko
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk
S. N. Kalinina
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences; Petrozavodsk State University
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk; Russia, Petrozavodsk
T. N. Ilyina
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk
E. P. Antonova
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences
Email: ira.irmita@yandex.ru
Russia, Petrozavodsk
References
- Панченко ДВ, Данилов ПИ, Тирронен КФ, Пааси-ваара А, Красовский ЮА (2019) Особенности распределения копытных млекопитающих в пределах карельской части Зеленого пояса Фенноскандии. Труды Карельского научного центра РАН 4: 119–128. [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. Trans Karelian Res Centre RAS 4: 119–128. (In Russ)]. https://doi.org/10.17076/them997
- Данилов ПИ, Панченко ДВ (2012) Расселение и некоторые особенности экологии кабана за северным пределом его исторического ареала в европейской части России. Экология 1: 48–54. [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
- Данилкин АА (2002) Свиные (Suidae) М. ГЕОС [Danilkin AA (2002) Pigs (Suidae) M. GEOS. (In Russ)].
- Корчина ТЯ, Корчин ВИ (2014) Витамины и микроэлементы: особенности северного региона. Ханты-Мансийск. Новости Югры. [Korchina TY, Korchin VI (2014) Vitamins and trace elements: features of the northern region. Khanty-Mansiysk. Ugra news. (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
- Калинина ЕВ, Чернов НН, Новичкова МД (2014) Роль глутатиона, глутатионтрансферазы и глутаредоксина в регуляции редокс-зависимых процессов. Успехи биологической химии 54: 299–348. [Kalinina EV, Chernov NN, Novichkova MD (2014) The role of glutathione, glutathione transferase and glutaredoxin in the regulation of redox-dependent processes. Uspehi biologicheskoj himii 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. Intech Open. 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
- Калинина СН, Панченко ДВ, Баишникова ИВ, Антонова ЕП, Илюха ВА, Шакун ВВ, Зайцева ИА (2020) Антиоксидантный и витаминный статусы кабана Sus scrofa L. (Artiodactyla) на периферии ареала (Республика Карелия). Труды Кольского научного центра РАН 11 (2–8 (8)): 83–92. [Kalinina SN, Panchen-ko 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 (2–8 (8)): 83–92. (In Russ)]. https://doi.org/10.37614/2307-5252.2020.2.8.008
- Клевезаль ГА (2007) Принципы и методы определения возраста млекопитающих М. Т-во научных изданий КМК. [Klevezal GA (2007) Principles and methods of age determination of mammals M. KMK Sci Press Ltd. (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.
- Кульпин АА (2008) Особенности биотопического распределения и питания кабана (Sus Scrofa L.) на севере европейской части России. Вестник Нижегородского университета им. Н.И. Лобачевского 2: 82–86. [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)].
- Вапиров ВВ, Чаженгина ЕА (2019) Селеновый статус природных объектов Республики Карелия. Экологическая геология: теория, практика и региональные проблемы. Мат-лы VI Международной научно-практической конференции 16–19. [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: Nutritional Biotechnology in the Feed and Food Industries. Proc. of Alltech’s 19th Annual Symposium (Lyons TP and Jacques KA, eds.). 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
- Смирнов ЛП, Суховская ИВ (2014) Роль глутатиона в функционировании систем антиоксидантной защиты и биотрансформации (обзор). Уч запис Петрозаводск гос универ 6: 34–40. [Smirnov LP, Su-khovskaya IV (2014) Glutathione role in antioxidant protection and in functioning of biotransformation system (review). Proceed Petrozavodsk State Univ 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. https://doi.org/10.1371/journal.pone.0178487
Supplementary files
