Abstract
This work is aimed at studying the effect of saturated stearic acid (SA) under in vitro culture conditions on the embryos of the domestic cat (Felis silvestris catus) and at estimating how a change in the composition of intracellular lipids is reflected in the results of cryopreservation. The addition of SA to the culture medium had no effect on the development of cat embryos in vitro before cryopreservation. There were also no changes by the total amount of lipids in the embryos after the effect of SA. Meanwhile, the degree of lipid unsaturation was reduced in the embryos after in vitro cultivation with SA. Moreover, the temperature of lipid phase transition onset (T*) was higher in the embryos exposed to the effect of SA as compared with the control. A decrease in the efficiency of embryo cryopreservation during the cultivation with SA was associated with a decrease in the degree of unsaturation of intracellular lipids and a increase in T *. The results can be important for the conservation of genetic resources of the species from the subfamily Felinae.
REFERENCES
Aardema, H., Bertijn, I., van Tol., H., Rijneveld, A., Vernooij, J., Gadella, B.M., and Vos, P., Fatty acid supplementation during in vitro embryo production determines cryosurvival characteristics of bovine blastocysts, Front. Cell. Dev. Biol., 2022, vol. 10, p. 837405. https://doi.org/10.3389/fcell.2022.837405
Abe, H., Yamashita, S., Satoh, T., and Hoshi, H., Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media, Mol. Reprod. Dev., 2002, vol. 61, pp. 57–66. https://doi.org/10.1002/mrd.1131
Amstislavsky, S.Ya., Mokrousova, V.I., Kozhevnikova, V.V., Kizilova, E.A., Brusentsev, E.Yu., Okotrub, K.A., Naprimerov, V.A., and Naidenko, S.V., Cryobank of feline genetic resources, Vavilov. Zh. Genet. Selekt., 2017, vol. 21, no. 5, pp. 561–568. https://doi.org/10.18699/10.18699/VJ17.27-o
Amstislavsky, S., Brusentsev, E., Kizilova, E., Mokrousova, V., Kozhevnikova, V., Abramova, T., Rozhkova, I., and Naidenko, S., Sperm cryopreservation in the far-eastern wildcat (Prionailurus bengalensis euptilurus), Reprod. Domest. Anim., 2018, vol. 53, pp. 1219–1226. https://doi.org/10.1111/rda.13230
Amstislavsky, S., Mokrousova, V., Brusentsev, E., Okotrub, K., and Comizzoli, P., Influence of cellular lipids on cryopreservation of mammalian oocytes and preimplantation embryos: a review, Biopreserv. Biobanking, 2019, vol. 17, pp. 76–83. https://doi.org/10.1089/bio.2018.0039
Barrera, N., Dos, Santos., Neto, P.C., Cuadro, F., Bosolasco, D., Mulet, A.P., Crispo, M., and Menchaca, A., Impact of delipidated estrous sheep serum supplementation on in vitro maturation, cryotolerance and endoplasmic reticulum stress gene expression of sheep oocytes, PLoS One, 2018, vol. 13, p. e0198742. https://doi.org/10.1371/journal.pone.0198742
Borges, E. and Vireque, A., Updating the impact of lipid metabolism modulation and lipidomic profiling on oocyte cryopreservation, EMJ, 2019, vol. 4, pp. 79–87. https://doi.org/10.33590/emj/10310074
Brusentsev, E., Kizilova, E., Mokrousova, V., Kozhevnikova, V., Rozhkova, I., and Amstislavsky, S., Characteristics and fertility of domestic cat epididymal spermatozoa cryopreserved with two different freezing media, Theriogenology, 2018, vol. 110, pp. 148–152. https://doi.org/10.1016/j.theriogenology.2017.12.038
Cecchele, A., Cermisoni, G., Giacomini, E., Pinna, M., and Vigano, P., Cellular and molecular nature of fragmentation of human embryos, Int. J. Mol. Sci., 2022, vol. 23, p. 1349. https://doi.org/10.3390/ijms23031349
Crichton, E., Bedows, E., Miller-Lindholm, A., Baldwin, D.M., Armstrong, D.L., Graham, L.H., Ford, J.J., Gjorret, J.O., Hyttel, P., Pope, C.E., Vajta, G., and Loskutoff, N.M., Efficacy of porcine gonadotropins for repeated stimulation of ovarian activity for oocyte retrieval and in vitro embryo production and cryopreservation in Siberian tigers (Panthera tigris altaica), Biol. Reprod., 2003, vol. 68, pp. 105–113. https://doi.org/10.1095/biolreprod.101.002204
Desmet, K.L., van Hoeck, V., Gagne, D., Fournier, E., Thakur, A., O’Doherty, A.M., Walsh, C.P., Sirard, M.A., Bols, P.E., and Leroy, J.L., Exposure of bovine oocytes and embryos to elevated non-esterified fatty acid concentrations: integration of epigenetic and transcriptomic signatures in resultant blastocysts, BMC Genomics, 2016, vol. 17, p. 1004. https://doi.org/10.1186/s12864-016-3366-y
Fayezi, S., Leroy, J., Ghaffari, NovinM., and Darabi, M., Oleic acid in the modulation of oocyte and preimplantation embryo development, Zygote, 2018, vol. 26, pp. 1–13. https://doi.org/10.1017/S0967199417000582
Galiguis, J., Gomez, M., Leibo, S., and Pope, C., Birth of a domestic cat kitten produced by vitrification of lipid polarized in vitro matured oocytes, Cryobiology, 2014, vol. 68, pp. 459–466. https://doi.org/10.1016/j.cryobiol.2014.02.012
Genicot, G., Leroy, J., van Soom, A., and Donnay, I., The use of a fluorescent dye Nile red to evaluate the lipid content of single mammalian oocytes, Theriogenology, 2005, vol. 63, pp. 1181–1194. https://doi.org/10.1111/j.1439-0531.2004.00556.x
Haggarty, P., Wood, M., Ferguson, E., Hoad, G., Srikantharajah, A., Milne, E., Hamilton, M., and Bhattacharya, S., Fatty acid metabolism in human preimplantation embryos, Hum. Reprod., 2006, vol. 21, pp. 766–773. https://doi.org/10.1093/humrep/dei385
van Hoeck, V., Sturmey, R., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H.J., Bols, P.E., and Leroy, J.L., Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology, PLoS One, 2011, vol. 6, p. e23183. https://doi.org/10.1371/journal.pone.0023183
Idrissi, S., Bourhis, D., Lefevre, A., Emond, P., Le Berre, L., Desnoes, O., Joly, T., Buff, S., Maillard, V., Schibler, L., Salvetti, P., and Elis, S., Lipid profile of bovine grade-1 blastocysts produced either in vivo or in vitro before and after slow freezing process, Sci. Rep., 2021, vol. 11, p. 11618. https://doi.org/10.1038/s41598-021-90870-8
Igonina, T., Okotrub, K., Brusentsev, E., Chuyko, E.A., Ragaeva, D.S., Ranneva, S.V., and Amstislavsky, S.Y., Alteration of the lipid phase transition during mouse embryos freezing after in vitro culture with linoleic acid, Cryobiology, 2021, vol. 99, pp. 55–63. https://doi.org/10.1016/j.cryobiol.2021.01.014
IUCN Red List of Threatened Species, IUCN, 2021. https://www.iucnredlist.org/search?taxonomies=101738& searchType=species.
Karasahin, T., The effect of oleic and linoleic acid addition to the culture media on bovine embryonic development following vitrification, Pol. J. Vet. Sci., 2019, vol. 22, pp. 661–666. https://doi.org/10.24425/pjvs.2019.129978
Kochan, J., Nowak, A., Mlodawska, W., Prochowska, S., Partyka, A., Skotnicki, J., and Nizanski, W., Comparison of the morphology and developmental potential of oocytes obtained from prepubertal and adult domestic and wild cats, Animals, 2021, vol. 11, p. 20. https://doi.org/10.3390/ani11010020
Lawson, E.F., Grupen, C.G., Baker, M.A., Aitken, R.J., Swegen, A., Pollard, C.L., and Gibb, Z., Conception and early pregnancy in the mare: lipidomics the unexplored frontier, Reprod. Fertil., 2022, vol. 3, pp. R1–R18. https://doi.org/10.1530/RAF-21-0104
Mazur, P., Equilibrium, quasiequilibrium, and nonequilibrium freezing of mammalian embryos, Cell. Biophys., 1990, vol. 17, pp. 53–92. https://doi.org/10.1007/BF02989804
Mokrousova, V., Okotrub, K., Amstislavsky, S., and Surovtsev, N., Raman spectroscopy evidence of lipid separation in domestic cat oocytes during freezing, Cryobiology, 2020a, vol. 95, pp. 177–182. https://doi.org/10.1016/j.cryobiol.2020.03.005
Mokrousova, V., Okotrub, K., Brusentsev, E., Kizilova, E.A., Surovtsev, N.V., and Amstislavsky, S.Y., Effects of slow freezing and vitrification on embryo development in domestic cat, Reprod. Dom. Anim., 2020b, vol. 55, pp. 1328–1336.https://doi.org/10.1111/rda.13776
Nagashima, H., Kashiwazaki, N., Ashman, R., Grupen, C.G., and Nottle, M.B., Cryopreservation of porcine embryos, Nature, 1995, vol. 374, p. 416. https://doi.org/10.1038/374416a0
Nonogaki, T., Noda, Y., Goto, Y., Kishi, J., and Mori, T., Developmental blockage of mouse embryos caused by fatty acids, J. Assist. Reprod. Genet., 1994, vol. 11, pp. 482–488. https://doi.org/10.1007/BF02215713
Ohata, K., Ezoe, K., Miki, T., Kouraba, S., Fujiwara, N., Yabuuchi, A., Kobayashi, T., and Kato, K., Effects of fatty acid supplementation during vitrification and warming on the developmental competence of mouse, bovine and human oocytes and embryos, Reprod. Biomed. Online, 2021, vol. 43, pp. 14–25. https://doi.org/10.1016/j.rbmo.2021.03.022
Okotrub, K., Mokrousova, V., Amstislavsky, S., and Surovtsev, N., Lipid droplet phase transition in freezing cat embryos and oocytes probed by Raman spectroscopy, Biophys. J., 2018, vol. 115, pp. 577–587. https://doi.org/10.1016/j.bpj.2018.06.019
Okotrub, K., Okotrub, S., Mokrousova, V., Amstislavsky, S.Y., and Surovtsev, N.V., Lipid phase transitions in cat oocytes supplemented with deuterated fatty acids, Biophys. J., 2021, vol. 120, pp. 5619–5630. https://doi.org/10.1016/j.bpj.2021.11.008
Okotrub, S.V., Lebedeva, D.A., Okotrub, K.A., Chuiko, E.A., Brusentsev, E.Yu., Rakhmanova, T.A., and Amstislavsky, S.Ya., Effects of linoleic acid on cryopreservation of IVF-obtained domestic cat embryos, Russ. J. Dev. Biol., 2022, vol. 53, no. 5, pp. 321–332. https://doi.org/10.1134/S106236042205006X
Pawlak, P., Malyszka, N., Szczerbal, I., and Kolodziejski, P., Fatty acid induced lipolysis influences embryo development, gene expression and lipid droplet formation in the porcine cumulus cells, Biol. Reprod., 2020, vol. 103, pp. 36–48. https://doi.org/10.1093/biolre/ioaa045
Ranneva, S., Okotrub, K., Amstislavsky, S., and Surovtsev, N., Deuterated stearic acid uptake and accumulation in lipid droplets of cat oocytes, Arch. Biochem. Biophys., 2020, vol. 692, p. 108532. https://doi.org/10.1016/j.abb.2020.108532
Renard, J.P. and Babinet, C., High survival of mouse embryos after rapid freezing and thawing inside plastic straws with 1-2 propanediol as cryoprotectant, J. Exp. Zool., 1984, vol. 230, pp. 443–448. https://doi.org/10.1002/jez.1402300313
Roth, T., Swanson, W., and Wildt, D., Developmental competence of domestic cat embryos fertilized in vivo versus in vitro, Biol. Reprod., 1994, vol. 51, pp. 441–451. https://doi.org/10.1095/biolreprod51.3.441
Shehab-El-Deen, M., Leroy, J., Maes, D., and van Soom, A., Cryotolerance of bovine blastocysts is affected by oocyte maturation in media containing palmitic or stearic acid, Reprod. Domest. Anim., 2009, vol. 44, pp. 140–142. https://doi.org/10.1111/j.1439-0531.2008.01084.x
Swanson, W.F., Roth, T.L., and Wildt, D.E., In vivo embryogenesis, embryo migration, and embryonic mortality in the domestic cat, Biol. Reprod., 1994, vol. 51, pp. 452–464. https://doi.org/10.1095/biolreprod51.3.452
Yousif, M., Calder, M., Du, J., Ruetz, K.N., Crocker, K., Urquhart, B.L., Betts, D.H., Rafea, B.A., and Watson, A.J., Oleic acid counters impaired blastocyst development induced by palmitic acid during mouse preimplantation development: understanding obesity-related declines in fertility, Reprod. Sci., 2020, vol. 27, pp. 2038–2051. https://doi.org/10.1007/s43032-020-00223-5
Zahmel, J., Jansch, S., Jewgenow, K., Sandgreen, D.M., Skalborg Simonsen, K., and Colombo, M., Maturation and fertilization of African lion (Panthera leo) oocytes after vitrification, Cryobiology, 2021, vol. 98, pp. 146–151. https://doi.org/10.1016/j.cryobiol.2020.11.011
Zeron, Y., Sklan, D., and Arav, A., Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes, Mol. Reprod. Dev., 2002, vol. 61, pp. 271–278. https://doi.org/10.1002/mrd.1156
ACKNOWLEDGMENTS
Microscopic studies were carried out at the Microscopic Analysis of Biological Objects Center for Collective Use, Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences.
Funding
This work was supported by the Russian Science Foundation (project no. 21-74-10108) using the equipment of the Center for Genetic Resources of Laboratory Animals Center for Collective Use, Federal Research Center, Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, supported by the Ministry of Science and Higher Education of Russia (Unique identifier of the project RFMEFI62119X0023).
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All studies were in accordance with the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS no. 123). The study was approved by the Bioethics Committee (protocol No. 144 dated March 29, 2023).
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Translated by A. Barkhash
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Brusentsev, E.Y., Okotrub, S.V., Lebedeva, D.A. et al. Effect of Stearic Acid on the Efficiency of Cryopreservation of Embryos of the Domestic Cat (Felis silvestris catus). Biol Bull Russ Acad Sci 51, 139–151 (2024). https://doi.org/10.1134/S1062359023602811
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DOI: https://doi.org/10.1134/S1062359023602811