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

vitamins A and E
bat
hibernation
antioxidant

Abstract

In this work the retinol and a-tocopherol content in bats that living and wintering on the northern periphery of their ranges, at different stages of hibernation and during summer activity was studied for the first time. A characteristic peculiarity of the northern zone bats is staying in hypobiosis for most of the year. The cycles of torpor–arousal during hibernation are associated with a rapid increase in body temperature and respiration, which leads to an increase in the formation of reactive oxygen species. In order to study the antioxidant status in bats of five species, the retinol and a-tocopherol content in the liver and skeletal muscle was determined by HPLC. The study objects were Myotis brandtii, Myotis Mystacinus, Myotis Daubentonii, Plecotus auritus and Eptesicus nilssonii. It was revealed that the antioxidants content was higher in torpid bats during hibernation compared with active animals in summer. At the beginning of hibernation the highest a-tocopherol content in the liver was found in Eptesicus nilssonii, and retinol content in Plecotus auritus. The retinol and a-tocopherol levels in the liver and skeletal muscle of Myotis brandtii in spring was higher than in other species. The a-tocopherol level in the skeletal muscle often exceeded the level detected in the liver at different stages of hibernation. Females showed in the spring, before the end of hibernation, higher antioxidant level in tissues than males. Significant variability of indices was observed in all bat species, which can be explained by both species and individual differences of animals living in natural conditions. High tocopherol and retinol levels in tissues may play an important role in the strategy of antioxidant protection in bats of the northern zone during hibernation.

https://doi.org/10.31857/S0044452922060031
PDF (Русский)

References

Ануфриев АИ, Ревин ЮВ (2006) Биоэнергетика зимней спячки летучих мышей (Chiroptera, Vespertilionidae) в Якутии. Plecotus et al 9:8–17. [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

Меньщикова ЕБ, Ланкин ВЗ, Зенков НК, Бондарь ИА, Круговых НФ, Труфакин ВА (2006) Окислительный стресс. Прооксиданты и антиоксиданты. М. Фирма «Слово». [Menshchikova EB, Lankin VZ, Zenkov NK, Bondar IA, Krugovykh NF, Trufakin VA (2006) Oxidative stress. Prooxidants and antioxidants. M. Firm "Slovo". (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

Калабухов НИ (1985) Спячка млекопитающих. М. Наука. [Kalabukhov NI (1985) Hibernation of mammals. M. Nauka. (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 -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

Стрелков ПП, Ильин ВЮ (1990) Рукокрылые (Chiroptera, Vespertilionidae) юга Среднего и Нижнего Поволжья. Фауна, систематика и эволюция млекопитающих. Рукокрылые, грызуны. Тр Зоол инст Л. 225:42–167. [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)]

Скурихин ВН, Двинская ЛМ 1989 Определение α-токоферола и ретинола в плазме крови сельскохозяйственных животных методом микроколоночной высокоэффективной жидкостной хроматографии. С-х биол (4):127–129. [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

Коломийцева ИК (2011) Липиды в гибернации и искусственном гипобиозе млекопитающих. Биохимия 12:1604–1614. [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

Голенко АС, Дзеверин ИИ (2007) Изменение массы тела и двигательная активность поздних кожанов (Eptesicus serotinus) в период спячки в лабораторных условиях. Plecotus et al 10:14–20. [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

Ануфриев АИ (2008) Механизмы зимней спячки мелких млекопитающих Якутии. Новосибирск. Изд-во СО РАН. [Anufriev AI (2008) Mechanisms of hibernation of small mammals of Yakutia. Novosibirsk. Publ SB RAS. (In Russ)].

Орлов ОД, Каминская ЛА, Мещанинов ВН (2012) Почему летучие мыши долго живут: предварительные анализ гипотез высокой продолжительности жизни рукокрылых. Научный диалог 2:147 – 151. [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.

Шмидт-Ниельсен К (1982) Физиология животных. Приспособление и среда. М. Мир. [Schmidt-Nielsen K (1982) Animal physiology. Adaptation and environment. M. Mir. (In Russ)].

Boyles JG, Dunbar MB, Storm JJ, Brack VJr (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

Кольтовер ВК (2009) Теория надёжности и старение: схоластическая реализация генетической программы. Проблемы старения и долголетия 1: 26-31. [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. http://dx.doi.org/10.24189/ncr.2021.002