Retinol and α-Tocopherol Content in the Liver and Skeletal Muscle of Bats (Chiroptera) during Hibernation and Summer Activity

Journal of Evolutionary Biochemistry and Physiology - Tập 58 - Trang 1697-1707 - 2022
T. N. Ilyina1, I. V. Baishnikova1, V. V. Belkin1
1Institute of Biology, Karelian Research Center of the Russian Academy of Sciences, Petrozavodsk, Russia

Tóm tắt

In this work, the content of retinol and α-tocopherol in bats living and wintering in Karelia at the northern periphery of their natural habitats, was studied for the first time at different stages of hibernation and during summer activity. A characteristic feature of chiropterans of the northern area is staying most of the year in a state of hypobiosis. Torpor–arousal cycles during hibernation are associated with a rapid increase in body temperature and respiration, which leads to an increase in the production of reactive oxygen species. To study the antioxidant status in five bat species (Myotis brandtii, Myotis Mystacinus, Myotis Daubentonii, Plecotus auritus and Eptesicus nilssonii), retinol and α-tocopherol levels were determined by HPLC in their liver and skeletal muscle. It was found that the antioxidant content was higher in torpid bats during hibernation compared to active animals in the summer period. At the beginning of hibernation, a highest α-tocopherol level in the liver was found in Eptesicus nilssonii, while the retinol level was the highest in Plecotus auritus. Retinol and α-tocopherol levels in the liver and skeletal muscle of Myotis brandtii in spring were higher compared to other species. At different stages of hibernation, α-tocopherol levels in the skeletal muscle can be higher than in the liver. In spring, before exiting hibernation, females demonstrated a higher antioxidant level in tissues compared to males. In all bat species, there was a significant variability in indices, which can be explained by both species-specific and individual differences among animals living in natural conditions. High tissue tocopherol and retinol levels may play an important role in the strategy of antioxidant defense in bats of the northern area during hibernation.

Tài liệu tham khảo

Anufriev AI, Revin YuV (2006) Bioenergetics of hibernation of bats (Chiroptera, Vespertilionidae) in Yakutia. Plecotus et al 9: 8–17. (In Russ). Brunet-Rossinni AK, Austad SN (2004) Ageing studies on bats: a review. Biogerontology 5: 211–222. https://doi.org/10.1023/B:BGEN.0000038022.65024.d8 Podlutsky AJ, Khritankov AM, Ovodov ND, Austad SN (2005) A New Field Record for Bat Longevity. J Gerontol: Biol Sci 60A 11: 1366–1368. https://doi.org/10.1093/gerona/60.11.1366 Filho DW, Althoff SL, Dafre AL, Boveris A (2007) Antioxidant defenses, longevity and ecophysiology of South American bats. Comp Biochem Physiol C 146: 214–220. https://doi.org/10.1016/J.CBPC.2006.11.015 Menshchikova EB, Lankin VZ, Zenkov NK, Bondar IA, Krugovykh NF, Trufakin VA (2006) Oxidative stress. Prooxidants and antioxidants. Firm “Slovo”, M. (In Russ). Allan ME, Storey KB (2012) Expression of NF-kB and downstream antioxidant genes in skeletal muscle of hibernating ground squirrels, Spermophilus tridecemlineatus. Cell Biochem Funct 30: 166–174. https://doi.org/10.1002/cbf.1832 Ribot J, Felipe F, Bonet ML, Palou A (2001) Changes of adiposity in response to vitamin A status correlate with changes of PPARγ2 expression. Obes Res 9: 500–509. https://doi.org/10.1038/oby.2001.65 Sprenger RJ, Tanumihardjo SA, Kurtz CC (2018) Developing a Model of Vitamin A Deficiency in a Hibernating Mammal, the 13-Lined Ground Squirrel (Ictidomys tridecemlineatus). Compar Med 3: 196–203. https://doi.org/10.30802/AALAS-CM-17-000113 Okamoto I, Kayano T, Hanaya T, Arai S, Ikeda M, Kurimoto M (2006) Up-regulation of an extracellular superoxide dismutase-like activity in hibernating hamsters subjected to oxidative stress in mid- to late arousal from torpor. Comp Biochem Physiol C 144: 47–56. https://doi.org/10.1016/j.cbpc.2006.05.003 Kalabukhov NI (1985) Hibernation of mammals. Nauka, M. (In Russ). Czeczuga B, Ruprecht AL (1982) Carotenoid Contents in Mammals. II. Carotenoids of Some Vespertilionidae from the Seasonal Variation Aspect. Acta Theriologica 6: 83–96. Müller K, Voigt CC, Raila J, Hurtienne A, Vater M, Brunnberg L, Schweigert FJ (2007) Concentration of carotenoids, retinol and α-tocopherol in plasma of six microchiroptera species. Comp Biochem Physiol B 147: 492–497. https://doi.org/10.1016/j.cbpb.2007.03.002 Dierenfeld ES, Seyjagat J (2000) Plasma fat-soluble vitamin and mineral concentrations in relation to diet in captive Pteropodid bats. J Zoo Wildl Med 3: 315–321. https://doi.org/10.1638/1042-7260(2000)031[0315:PFSVAM]2.0.CO;2 Strelkov PP, Ilyin VU (1990) Bats (Chiroptera, Vespertilionidae) of the south of the Middle and Lower Volga region. Fauna, systematics and evolution of mammals. Bats, rodents. Proceedings Zool Inst L 225: 42–167. (In Russ). Skurikhin VN, Dvinskaya LM 1989 Determination of α-tocopherol and retinol in the blood plasma of farm animals by micro-column high-performance liquid chromatography. Agricultural Biology (4):127–129. (In Russ). Lilley TM, Stauffer J, Kanerva M, Eeva T (2014) Interspecific variation in redox status regulation and immune defence in five bat species: the role of ectoparasites. Oecologia 175: 811–823. https://doi.org/10.1007/s00442-014-2959-x Anegawa D, Sugiura Y, Matsuoka Y, Sone M, Shichiri M, Otsuka R, Ishida N, Yamada KI, Suematsu M, Miura M, Yamaguchi Y (2021) Hepatic resistance to cold ferroptosis in a mammalian hibernator Syrian hamster depends on effective storage of diet-derived α-tocopherol. Commun Biol. 4(1):796. https://doi.org/10.1038/s42003-021-02297-6 Fedorov VB, Goropashnaya AV, Stewart NC, Tøien Ø, Chang C, Wang H, Yan J, Showe LC, Showe MK, Barnes BM (2014) Comparative functional genomics of adaptation to muscular disuse in hibernating mammals. Mol Ecol 23(22):5524–5537. https://doi.org/10.1111/mec.12963 Giroud S, Habold C, Nespolo RF, Mejías C, Terrien J, Logan SM, Henning RH, Storey KB (2021) The Torpid State: Recent Advances in Metabolic Adaptations and Protective Mechanisms. Front Physiol 11: 623665. https://doi.org/10.3389/fphys.2020.623665 Fuster G, Busquets S, Almendro V, Lopez-Soriano FJ, Argiles JM (2007) Antiproteolytic effects of plasma from hibernating bears: a new approach for muscle wasting therapy? Clin Nutr 26: 658–661. https://doi.org/10.1016/j.clnu.2007.07.003 Gallagher K, Staples JF (2013) Metabolism of Brain Cortex and Cardiac Muscle Mitochondria in Hibernating 13-Lined Ground Squirrels Ictidomys tridecemlineatus. Physiol Biochem Zool 86(1): 1–8. https://doi.org/10.1086/668853 Jiang S, Gao Y, Zhang Y, Liu K, Wang H, Goswami N (2013) The research on the formation mechanism of extraordinary oxidative capacity of skeletal muscle in hibernating ground squirrels (Spermophilus dauricus). J Exp Biol 216(Pt 14): 2587–2594. https://doi.org/10.1242/jeb.080663. Hindle AG, Otis JP, Epperson LE, Hansberger TA, Goodman CA, Carey HV, Martin SL (2015) Prioritization of skeletal muscle growth for emergence from hibernation. J Exp Biol 218: 276–284. https://doi.org/10.1242/jeb.109512 Regan MD, Chiang E, Liu Y, Tonelli M, Verdoorn KM, Gugel SR, Suen G, Carey HV, Assadi-Porter FM (2022) Nitrogen recycling via gut symbionts increases in ground squirrels over the hibernation season. Science 6579: 460–463. https://doi.org/10.1126/science.abh2950 James RS, Staples JF, Brown JCL, Tessier ST, Storey KB (2013) The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, Ictidomys tridecemlineatus. J Exp Biol 216: 2587–2594. https://doi.org/10.1242/jeb.080663 Seim I, Fang X, Xiong Z, Lobanov AV, Huang Z, et al. (2013) Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii. Nat Commun 1: 2221. https://doi.org/10.1038/ncomms3212 Kolomiytseva IK (2011) Lipids in hibernation and artificial mammalian hypobiosis. Biochemistry 12: 1604–1614. (In Russ). Brown JCL, Chung DJ, Cooper AN, Staples JF (2013) Regulation of succinate-fuelled mitochondrial respiration in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. J Exp Biol 216(Pt 9): 1736–1743. https://doi.org/10.1242/jeb.078519. Epperson LE, Karimpour-Fard A, Hunter LE, Martin SL (2011) Metabolic cycles in a circannual hibernator. Physiol Genomics 13: 799–807. https://doi.org/10.1152/physiolgenomics.00028.2011 Golenko AS, Dzeverin II (2007) Body weight change and motor activity of late leather bat (Eptesicus serotinus) during hibernation in laboratory conditions. Plecotus et al 10: 14–20. (In Russ). Speakman JR, Rowland A (1999) Preparing for inactivity: how insectivorous bats deposit a fat store for hibernation. Proc Nutr Soc 58: 123–131. https://doi.org/10.1079/pns19990017 Czenze Z, Jonasson K, Willis CKR (2017) Thrifty Females, Frisky Males: Winter Energetics of Hibernating Bats from a Cold Climate. Physiol Biochem Zool 4: 502–511. https://doi.org/10.1086/692623 Anufriev AI (2008) Mechanisms of hibernation of small mammals of Yakutia. Publ SB RAS, Novosibirsk. (In Russ). Orlov OD, Kamenskaya LA, Meshchaninov VN (2012) Why bats live long: preliminary analysis of hypotheses of high life expectancy of bats. Scientific Dialogue 2: 147–151. (In Russ). Khritankov AM, Ovodov ND (2001) Longevity of Brandt’s bats (Myotis brandtii Eversmann) in central Siberia. Plecotus et al 4: 20–24. Schmidt-Nielsen K (1982) Animal physiology. Adaptation and environment. Mir, M. (In Russ). Boyles JG, Dunbar MB, Storm JJ, Brack V Jr (2007) Energy availability influences microclimate selection of hibernating bats. J Exp Biol 210: 4345–4350. https://doi.org/10.1242/jeb.007294 Blanera WS, O’Byrne SM, Wongsiriroj N, Kluwe J, D’Ambrosio DM, Jiang H, Schwabe RF, Hillman EMC, Piantedosi R, Libien J (2009) Hepatic stellate cell lipid droplets: A specialized lipid droplet for retinoid storage. Biochim Biophys Acta 1791: 467–473. https://doi.org/10.1016/j.bbalip.2008.11.001 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 3: 225–235. https://doi.org/10.21638/spbu03.2021.304 Coltover VK (2009) Reliability theory and aging: scholastic implementation of the genetic program. Problems of aging and longevity 1: 26–31. (In Russ). Belkin VV, Fyodorov FV, Ilyukha VA, Yakimova AE (2021) Characteristics of the bat (Chiroptera) population in protected areas in the northern and middle taiga subzones of European Russia. Nature Conservation Research 1: 17–31. https://doi.org/10.24189/ncr.2021.002