Effects of stearic acid on the cryotolerance of the domestic cat (Felis silvestris catus) embryos

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Abstract

The current work aimed to study the effect of domestic cat (Felis silvestris catus) embryos in vitro exposure to saturated stearic acid (SA) and to evaluate how the change in lipid content affects the cryopreservation results. The addition of SA to the culture medium did not affect the development of cat embryos in vitro before cryopreservation. The total lipid amount in the SA-treated embryos was not changed as well. However, the lipid unsaturation degree was lower in embryos after in vitro exposure to SA. Moreover, the lipid phase transition onset temperature (T*) was higher in SA-treated embryos as compared with controls. These changes of intracellular lipids unsaturation degree and T* were associated with the impairment of embryo cryopreservation effectiveness. The results obtained may be of importance for the applying Genome Resource Banking concept to the Felinae species.

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E. Yu. Brusentsev

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences

Author for correspondence.
Email: amstis@yandex.ru
Russian Federation, prosp. Lavrentyeva 10, Novosibirsk, 630090

S. V. Okotrub

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russian Federation, prosp. Lavrentyeva 10, Novosibirsk, 630090

D. A. Lebedeva

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Automation and Electrometry, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: amstis@yandex.ru
Russian Federation, prosp. Lavrentyeva 10, Novosibirsk, 630090; prosp. Koptyuga 1, Novosibirsk, 630090; Pirogova 2, Novosibirsk, 630090

K. A. Okotrub

Institute of Automation and Electrometry, Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russian Federation, prosp. Koptyuga 1, Novosibirsk, 630090

T. A. Rakhmanova

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Automation and Electrometry, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: amstis@yandex.ru
Russian Federation, prosp. Lavrentyeva 10, Novosibirsk, 630090; prosp. Koptyuga 1, Novosibirsk, 630090; Pirogova 2, Novosibirsk, 630090

S. Ya. Amstislavsky1

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Automation and Electrometry, Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russian Federation, prosp. Lavrentyeva 10, Novosibirsk, 630090; prosp. Koptyuga 1, Novosibirsk, 630090

References

  1. Амстиславский С.Я., Мокроусова В.И., Кожевникова В.В., Кизилова Е.А., Брусенцев Е.Ю., Окотруб К.А., Напримеров В.А., Найденко С.В. Криобанк генетических ресурсов кошачьих // Вавиловский журнал генетики и селекции. 2017. Т. 21. № 5. С. 561–568. https://doi.org/10.18699/10.18699/VJ17.27-o
  2. Окотруб С.В., Лебедева Д.А., Окотруб К.А., Чуйко Э.А., Брусенцев Е.Ю., Рахманова Т.А., Амстиславский С.Я. Влияние линолевой кислоты на криоконсервацию полученных путем ЭКО эмбрионов домашней кошки // Онтогенез. 2022. Т. 53. № 5. С. 345–357. https://doi.org/10.31857/S0475145022050068
  3. Aardema H., Bertijn I., van Tol H., Rijneveld A., Vernooij J., Gadella B.M., Vos P. Fatty acid supplementation during in vitro embryo production determines cryosurvival characteristics of bovine blastocysts // Front. Cell. Dev. Biol. 2022. V. 10. P. 837405. https://doi.org/10.3389/fcell.2022.837405
  4. Abe H., Yamashita S., Satoh T., 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. V. 61. P. 57–66. https://doi.org/10.1002/mrd.1131
  5. Amstislavsky S., Mokrousova V., Brusentsev E., Okotrub K., Comizzoli P. Influence of cellular lipids on cryopreservation of mammalian oocytes and preimplantation embryos: a review // Biopreserv. Biobanking. 2019. V. 17. P. 76–83. https://doi.org/10.1089/bio.2018.0039
  6. Amstislavsky S., Brusentsev E., Kizilova E., Mokrousova V., Kozhevnikova V., Abramova T., Rozhkova I., Naidenko S. Sperm cryopreservation in the Far-Eastern wildcat (Prionailurus bengalensis euptilurus) // Reprod. Domest. Anim. 2018. V. 53. P. 1219–1226. https://doi.org/10.1111/rda.13230
  7. Barrera N., Dos Santos Neto P.C., Cuadro F., Bosolasco D., Mulet A.P., Crispo M., 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. V. 13. e0198742. https://doi.org/10.1371/journal.pone.0198742
  8. Borges E., Vireque A. Updating the impact of lipid metabolism modulation and lipidomic profiling on oocyte cryopreservation // EMJ. 2019. V. 4. P. 79–87. https://doi.org/10.33590/emj/10310074
  9. Brusentsev E., Kizilova E., Mokrousova V., Kozhevnikova V., Rozhkova I., Amstislavsky S. Characteristics and fertility of domestic cat epididymal spermatozoa cryopreserved with two different freezing media // Theriogenology. 2018. V. 110. P. 148–152. https://doi.org/10.1016/j.theriogenology.2017.12.038
  10. Cecchele A., Cermisoni G., Giacomini E., Pinna M., Vigano P. Cellular and molecular nature of fragmentation of human embryos // Int. J. Mol. Sci. 2022. V. 23. P. 1349. https://doi.org/10.3390/ijms23031349
  11. 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., 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. V. 68. P. 105–113. https://doi.org/10.1095/biolreprod.101.002204
  12. 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., 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. V. 17. P. 1004. https://doi.org/10.1186/s12864-016-3366-y
  13. Fayezi S., Leroy J., Ghaffari Novin M., Darabi M. Oleic acid in the modulation of oocyte and preimplantation embryo development // Zygote. 2018. V. 26. P. 1–13. https://doi.org/10.1017/S0967199417000582
  14. Galiguis J., Gomez M., Leibo S., Pope C. Birth of a domestic cat kitten produced by vitrification of lipid polarized in vitro matured oocytes // Cryobiology. 2014. V. 68. P. 459–466. https://doi.org/10.1016/j.cryobiol.2014.02.012
  15. Genicot G., Leroy J., van Soom A., Donnay I. The use of a fluorescent dye Nile red to evaluate the lipid content of single mammalian oocytes // Theriogenology. 2005. V. 63. P. 1181–1194. https://doi.org/10.1111/j.1439-0531.2004.00556.x
  16. Haggarty P., Wood M., Ferguson E., Hoad G., Srikantharajah A., Milne E., Hamilton M., Bhattacharya S. Fatty acid metabolism in human preimplantation embryos // Hum. Reprod. 2006. V. 21. P. 766–773. https://doi.org/10.1093/humrep/dei385
  17. Idrissi S., Bourhis D., Lefevre A., Emond P., Le Berre L., Desnoes O., Joly T., Buff S., Maillard V., Schibler L., Salvetti P., 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. V. 11. P. 11618. https://doi.org/10.1038/s41598-021-90870-8
  18. Igonina T., Okotrub K., Brusentsev E., Chuyko E.A., Ragaeva D.S., Ranneva S.V., Amstislavsky S.Y. Alteration of the lipid phase transition during mouse embryos freezing after in vitro culture with linoleic acid // Cryobiology. 2021. V. 99. P. 55–63. https://doi.org/10.1016/j.cryobiol.2021.01.014
  19. IUCN Red List of Threatened Species // IUCN. 2021. [Электронный ресурс]. https://www.iucnredlist.org/search?taxonomies=101738&searchType=species
  20. Kochan J., Nowak A., Mlodawska W., Prochowska S., Partyka A., Skotnicki J., Nizanski W. Comparison of the morphology and developmental potential of oocytes obtained from prepubertal and adult domestic and wild cats // Animals. 2021. V. 11. P. 20. https://doi.org/10.3390/ani11010020
  21. 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. V. 22. P. 661–666. https://doi.org/10.24425/pjvs.2019.129978
  22. Lawson E.F., Grupen C.G., Baker M.A., Aitken R.J., Swegen A., Pollard C.L., Gibb Z. Conception and early pregnancy in the mare: lipidomics the unexplored frontier // Reprod. Fertil. 2022. V. 3. R1–R18. https://doi.org/10.1530/RAF-21-0104
  23. Mazur P. Equilibrium, quasiequilibrium, and nonequilibrium freezing of mammalian embryos // Cell. Biophys. 1990. V. 17. P. 53–92. https://doi.org/10.1007/BF02989804
  24. Mokrousova V., Okotrub K., Amstislavsky S., Surovtsev N. Raman spectroscopy evidence of lipid separation in domestic cat oocytes during freezing // Cryobiology. 2020а. V. 95. P. 177–182. https://doi.org/10.1016/j.cryobiol.2020.03.005
  25. Mokrousova V., Okotrub K., Brusentsev E., Kizilova E.A., Surovtsev N.V., Amstislavsky S.Y. Effects of slow freezing and vitrification on embryo development in domestic cat // Reprod. Dom. Anim. 2020б. V. 55. P. 1328–1336. https://doi.org/10.1111/rda.13776
  26. Nagashima H., Kashiwazaki N., Ashman R., Grupen C.G., Nottle M.B. Cryopreservation of porcine embryos // Nature. 1995. V. 374. P. 416. https://doi.org/10.1038/374416a0
  27. Nonogaki T., Noda Y., Goto Y., Kishi J., Mori T. Developmental blockage of mouse embryos caused by fatty acids // J. Assist. Reprod. Genet. 1994. V. 11. P. 482–488. https://doi.org/10.1007/BF02215713
  28. Ohata K., Ezoe K., Miki T., Kouraba S., Fujiwara N., Yabuuchi A., Kobayashi T., 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. V. 43. P. 14–25. https://doi.org/10.1016/j.rbmo.2021.03.022
  29. Okotrub K., Okotrub S., Mokrousova V., Amstislavsky S.Y., Surovtsev N.V. Lipid phase transitions in cat oocytes supplemented with deuterated fatty acids // Biophys. J. 2021. V. 120. P. 5619–5630. https://doi.org/10.1016/j.bpj.2021.11.008
  30. Okotrub K., Mokrousova V., Amstislavsky S., Surovtsev N. Lipid droplet phase transition in freezing cat embryos and oocytes probed by Raman spectroscopy // Biophys. J. 2018. V. 115. P. 577–587. https://doi.org/10.1016/j.bpj.2018.06.019
  31. Pawlak P., Malyszka N., Szczerbal I., Kolodziejski P. Fatty acid induced lipolysis influences embryo development, gene expression and lipid droplet formation in the porcine cumulus cells // Biol. Reprod. 2020. V. 103. P. 36–48. https://doi.org/10.1093/biolre/ioaa045
  32. Ranneva S., Okotrub K., Amstislavsky S., Surovtsev N. Deuterated stearic acid uptake and accumulation in lipid droplets of cat oocytes // Arch. Biochem. Biophys. 2020. V. 692. P. 108532. https://doi.org/10.1016/j.abb.2020.108532
  33. Renard J.P., 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. V. 230. P. 443–448. https://doi.org/10.1002/jez.1402300313
  34. Roth T., Swanson W., Wildt D. Developmental competence of domestic cat embryos fertilized in vivo versus in vitro // Biol. Reprod. 1994. V. 51. P. 441–451. https://doi.org/10.1095/biolreprod51.3.441
  35. Shehab-El-Deen M., Leroy J., Maes D., van Soom A. Cryotolerance of bovine blastocysts is affected by oocyte maturation in media containing palmitic or stearic acid // Reprod. Domest. Anim. 2009. V. 44. P. 140–142. https://doi.org/10.1111/j.1439-0531.2008.01084.x
  36. Swanson W.F., Roth T.L., Wildt D.E. In vivo embryogenesis, embryo migration, and embryonic mortality in the domestic cat // Biol. Reprod. 1994. V. 51. P. 452–464. https://doi.org/10.1095/biolreprod51.3.452
  37. van Hoeck V., Sturmey R., Bermejo-Alvarez P., Rizos D., Gutierrez-Adan A., Leese H.J., Bols P.E., Leroy J.L. Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology // PloS One. 2011. V. 6. e23183. https://doi.org/10.1371/journal.pone.0023183
  38. Yousif M., Calder M., Du J., Ruetz K.N., Crocker K., Urquhart B.L., Betts D.H., Rafea B.A., 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. V. 27. P. 2038–2051. https://doi.org/10.1007/s43032-020-00223-5
  39. Zahmel J., Jansch S., Jewgenow K., Sandgreen D.M., Skalborg Simonsen K., Colombo M. Maturation and fertilization of African lion (Panthera leo) oocytes after vitrification // Cryobiology. 2021. V. 98. P. 146–151. https://doi.org/10.1016/j.cryobiol.2020.11.011
  40. Zeron Y., Sklan D., Arav A. Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes // Mol. Reprod. Dev. 2002. V. 61. P. 271–278. https://doi.org/10.1002/mrd.1156

Supplementary files

Supplementary Files
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1. JATS XML
2. Fig. 1. Experimental design. IVF – in vitro fertilization; LPL – lipid phase transition

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3. Fig. 2. Developmental stages of domestic cat (Felis silvestris catus) embryos after 66 hours of in vitro cultivation without (a, c) or with stearic acid –SA (d, e): early morulae (a, b) and late morulae (d, e) ); DAPI staining and fluorescence microscopy. White arrows – fragmentation, dotted arrows – spermatozoa. Scale – 50 µm

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4. Fig. 3. Effect of stearic acid (SA) on the degree of lipid unsaturation (top) and T* (bottom) in the cells of preimplantation embryos of the domestic cat (Felis silvestris catus). Data are presented as M ± SEM. Each point corresponds to one embryo. *p < 0.05; ***p < 0.001 compared to control

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5. Fig. 4. Fluorescence intensity of domestic cat (Felis silvestris catus) embryos stained with Nile red after 66 hours of in vitro cultivation without and with stearic acid (SA). a – number of photons (Me [Q1; Q3]), each point corresponds to one embryo; b, c-representative CLSM optical sections of domestic cat embryos stained with Nile red. b – without SC; with SK. Scale – 50 µm

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6. Fig. 5. Late morulae of the domestic cat (Felis silvestris catus) after freezing-thawing and subsequent cultivation in vitro for 30 hours (total time – 96 hours): control (a) and SC (b) groups; DAPI staining. Arrows indicate fragmented nuclei. Scale – 50 µm

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