Nuclear Maturation Competence and Pronuclear Formation in Ovine Oocytes Supplemented with L-ergothioneine in Maturation Medium

Rimas Prathita Agustin, Mohamad Agus Setiadi, Iman Supriatna
 DOI  https://doi.org/10.14334/jitv.v28i1.3120

Abstract

This study aimed to determine the efficacy of supplementing maturation medium with L-ergothioneine on nuclear maturation competence and pronuclei formation of ovine oocytes in vitro.  In the first study, oocytes were divided into four groups and matured for 24 hours in a maturation medium supplemented with 0 mM (control), 10 mM, 15 mM, and 20 mM LE.  In the second study, oocytes were divided into two groups and matured for 24 hours in a maturation medium supplemented with 0 mM LE (control) and 10 mM LE (optimal dose from the first study), then co-incubated with sperm in a fertilization medium for 12 hours.  The results of the first study showed that the maturation rate of oocytes enriched with LE 10 mM (88.74±1.79%) and 15 mM (87.52±2.30%) in maturation medium was significantly different (P<0.05) compared to the control (78.55±1.78%) and LE 20 mM (77.37±1.21%).  Furthermore, the results of the second study revealed that the fertilization rate of oocytes with 10 mM LE (75.55±3.47%) supplementation in maturation medium had a significantly higher percentage of two pronuclei formation than control (63.78±3.49%).  In conclusion, supplementing 10 mM LE in a maturation medium improved oocyte nuclear maturation competence and fertilization rates.

Keywords

In Vitro Maturation; In Vitro Fertilization; L-ergothioneine; Oocyte; Ovine

Full Text:

PDF

References

Abbara A, Clarke SA, Dhillo WS. 2018. Novel concepts for inducing final oocyte maturation in vitro fertilization treatment. Endocr Rev. 39:593–628. DOI:10.1210/er. 2017-00236.

Anchordoquy JP, Lizarraga RM, Anchordoquy JM, Nikoloff N, Rosa DE, Fabra MC, Peral-García P, Furnus CC. 2019. Effect of cysteine, glutamate, and glycine supplementation to in vitro fertilization medium during bovine early embryo development. Reprod Biol. 19:349–355. DOI:10.1016/j.repbio.2019.10.002.

Anzalone DA, Palazzese L, Czernik M, Sabatucci A, Valbonetti L, Capra E, Loi P. 2021. Controlled spermatozoa–oocyte interaction improves embryo quality in sheep. Sci Rep. 11:1–9. DOI:10.1038/s41598-021-02000-z.

Bahrami M, Cottee PA. 2022. Culture conditions for in vitro maturation of oocytes – A review. Reprod Breed. 2:31–36. DOI:10.1016/j.repbre.2022.04.001.

Bahrami M, Morris MB, Day ML. 2019. Amino acid supplementation of a simple inorganic salt solution supports efficient in vitro maturation (IVM) of bovine oocytes. Sci Rep. 9:1–10. DOI:10.1038/s41598-019-480 38-y.

Batista RITP, Moro LN, Corbin E, Alminana C, Souza-Fabjan JMG, de Figueirêdo Freitas VJ, Mermillod P. 2016. Combination of oviduct fluid and heparin to improve monospermic zygote production during porcine in vitro fertilization. Theriogenology. 86:495–502. DOI:10. 1016/j.theriogenology.2016.01.031

Bazela K, Solyga-Zurek A, Debowska R, Rogiewicz K, Bartnik E, Eris I. 2014. L-ergothioneine protects skin cells against UV-induced damage-A preliminary study. Cosmetics. 1:51–60. DOI:10.3390/cosmetics1010051.

Bhakty ZW, Kaiin EM, Karja NWK, Setiadi MA. 2021. L-carnitine supplementation enhances nuclear and cytoplasmic maturation rates of sheep oocytes In vitro. Trop Anim Sci J. 44:131–137. DOI:10.5398/TASJ. 2021.44.2.131.

Bragança GM, Alcântara-Neto AS, Batista RITP, Brandão FZ, Freitas VJF, Mermillod P, Souza-Fabjan JMG. 2021. During IVF, oviduct fluid modulates polyspermy in invitro-produced goat embryos during the non-breeding season. Theriogenology. 168:59–65. DOI:10.1016/ j.theriogenology.2021.03.022.

Catalá MG, Izquierdo D, Rodríguez-Prado M, Hammami S, Paramio MT. 2012. Effect of oocyte quality on blastocyst development after in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI) in a sheep model. Fertil Steril. 97:1004–1008. DOI:10.1016/j. fertnstert.2011.12.043.

Cheah IK, Halliwell B. 2021. Ergothioneine, recent developments. Redox Biol. 42:101868. DOI:10.1016/ j.redox.2021.101868.

El-raey M, Nagai T. 2014. Different Aspects of Cattle Oocyte in vitro Maturation : Review. J Reprod Infertil. 5:1–13. DOI:10.5829/idosi.jri.2014.5.1.8397.

Evans JP. 2020. Preventing polyspermy in mammalian eggs — Contributions of the membrane block and other mechanisms. Mol Reprod Dev. 87:341–349. DOI:10. 1002/mrd.23331.

Franzoni F, Colognato R, Galetta F, Laurenza I, Barsotti M, Di Stefano R, Bocchetti R, Regoli F, Carpi A, Balbarini A, et al. 2006. An in vitro study on the free radical scavenging capacity of ergothioneine: comparison with reduced glutathione, uric acid and trolox. Biomed Pharmacother. 60:453–457. DOI:10.1016/j.biopha. 2006.07.015.

García-Martínez T, Vendrell-Flotats M, Martínez-Rodero I, Ordóñez-León EA, Ãlvarez-Rodríguez M, López-Béjar M, Yeste M, Mogas T. 2020. Glutathione ethyl ester protects in vitro-maturing bovine oocytes against oxidative stress induced by subsequent vitrification/warming. Int J Mol Sci. 21:1–26. DOI:10.3390/ijms21207547.

Gründemann D. 2012. The ergothioneine transporter controls and indicates ergothioneine activity - A review. Prev Med. 54:S71–S74. DOI:10.1016/j.ypmed.2011.12.001.

Guérin P, El Mouatassim S, Ménézo Y. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 7:175–189. DOI:10.1093/humupd/7.2.175.

Gulo FDK, Karja NWK, Setiadi MA. 2020. Cysteamine in maturation medium enhances nuclear maturation and fertilization rate of sheep oocytes in vitro. HAYATI J Biosci. 27:290–295. DOI:10.4308/hjb.27.4.290.

Van Der Heijden GW, Van Den Berg IM, Baart EB, Derijck AAHA, Martini E, De Boer P. 2009. Parental origin of chromatin in human monopronuclear zygotes revealed by asymmetric histone methylation patterns, differs between IVF and ICSI. Mol Reprod Dev. 76:101–108. DOI:10.1002/mrd.20933.

Hidaka T, Fukumoto Y, Yamamoto S, Ogata Y, Horiuchi T. 2018. Variations in bovine embryo production between individual donors for OPU-IVF are closely related to glutathione concentrations in oocytes during in vitro maturation. Theriogenology. 113:176–182. DOI:10. 1016/j.theriogenology.2018.03.002.

Hirata K, Goto S, Izumi Y, Taguchi M, Hayashi A, Fujioka M, Ishiko A. 2020. Chromosome analysis of blastocysts derived from single pronuclear zygotes by array CGH and clinical outcomes by the transfer of single pronuclear zygotes. J Assist Reprod Genet. 37:1645–1652.

Itoi F, Asano Y, Shimizu M, Honnma H, Murata Y. 2015. Birth of nine normal healthy babies following transfer of blastocysts derived from human single-pronucleate zygotes. J Assist Reprod Genet. 32:1401–1407. DOI:10.1007/s10815-015-0518-y.

Kashir J, Ganesh D, Jones C, Coward K. 2022. Oocyte activation deficiency and assisted oocyte activation: mechanisms, obstacles and prospects for clinical application. Hum Reprod Open. 2022:1–29. DOI:10.1093/hropen/hoac003.

Kerley RN, McCarthy C, Kell DB, Kenny LC. 2018. The potential therapeutic effects of ergothioneine in pre-eclampsia. Free Radic Biol Med. 117:145–157. DOI:10.1016/j.freeradbiomed.2017.12.030.

Lamhonwah AM, Tein I. 2006. Novel localization of OCTN1, an organic cation/carnitine transporter, to mammalian mitochondria. Biochem Biophys Res Commun. 345:1315–1325. DOI:10.1016/j.bbrc.2006.05.026.

Landim-Alvarenga FC, Maziero RRD. 2014. Control of oocyte maturation. Anim Reprod. 11:150–158.

Lee JW, Tian XC, Yang X. 2003. Failure of male pronucleus formation is the major cause of lack of fertilization and embryo development in pig oocytes subjected to intracytoplasmic sperm injection. Biol Reprod. 68:1341–1347.DOI:10.1095/biolreprod.102.009001.

Li RWS, Yang C, Sit ASM, Kwan YW, Lee SMY, Hoi MPM, Chan SW, Hausman M, Vanhoutte PM, Leung GPH. 2014. Uptake and protective effects of ergothioneine in human endothelial cells. J Pharmacol Exp Ther. 350:691–700. DOI:10.1124/jpet.114.214049.

Luo D, Zhang JB, Li SP, Liu W, Yao XR, Guo H, Jin ZL, Jin YX, Yuan B, Jiang H, Kim NH. 2020. Imperatorin Ameliorates the aging-associated porcine oocyte meiotic spindle defects by reducing oxidative stress and protecting mitochondrial function. Front Cell Dev Biol. 8:1–12. DOI:10.3389/fcell.2020.592433.

De Matos DG, Gasparrini B, Pasqualini SR, Thompson JG. 2002. Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology. 57:1443–1451. DOI:0.1016/S0093-691X(02)00643-X.

Mishra A, Reddy IJ, Dhali A, Javvaji PK. 2018. L-Ergothioneine improves the developmental potential of in vitro sheep embryos without influencing OCTN1-mediated cross-membrane transcript expression. Zygote. 26:149–161. DOI:10.1017/S0967199418000047.

Mondal S, Mor A, Reddy IJ, Nandi S, Gupta PSP, Mishra A. 2019. In vitro embryo production in sheep. Methods Mol Biol. 2006:131–140. DOI:10.1007/978-1-4939-9566-0_9.

Mondéjar I, Martínez-Martínez I, Avilés M, Coy P. 2013. Identification of potential oviductal factors responsible for zona pellucida hardening and monospermy during fertilization in mammals. Biol Reprod. 89:1–8. DOI:10.1095/biolreprod.113.111385.

Opiela J, Kitska-Ksiizkiewicz L. 2013. The utility of Brilliant Cresyl Blue (BCB) staining of mammalian oocytes used for in vitro embryo production (IVP). Reprod Biol. 13:177–183. DOI:10.1016/j.repbio.2013.07.004.

ÖZtürkler Y, Yildiz S, Güngör Ö, Pancarci ŞM, Kaçar C, Ari UÇ. 2010. The effects of L-ergothioneine and L-ascorbic acid on the in vitro maturation (IVM) and embryonic development (IVC) of sheep oocytes. J Fac Vet Med Univ Kafkas, Kars. 16:757–763.

Paramio MT, Izquierdo D. 2014. Current status of in vitro embryo production in sheep and goats. Reprod Domest Anim. 49:37–48. DOI:10.1111/rda.12334.

Paramio MT, Izquierdo D. 2016. Recent advances in in-vitro embryo production in small ruminants. Theriogenology. 86:152–159. DOI:10.1016/j.theriogenology.2016.04.027.

Paul BD, Snyder SH. 2010. The unusual amino acid L-ergothioneine is a physiologic cytoprotectant. Cell Death Differ. 17:1134–1140. DOI:10.1038/cdd.2009.163.

Quan GB, Ma Y, Ni YN, Wu GQ, Lv CR, Hong QH. 2017. Effects of synthetic polymers on in vitro maturation of sheep oocytes and subsequent developmental capacity after parthenogenetic activation or fertilization. Small Rumin Res. 153:153–157. DOI:10.1016/j.smallrumres. 2017.06.008.

Rakha SI, Elmetwally MA, El-Sheikh Ali H, Balboula A, Mahmoud AM, Zaabel SM. 2022. Importance of Antioxidant Supplementation during in vitro Maturation of Mammalian Oocytes. Vet Sci. 9. DOI:10.3390 /vetsci9080439.

Ramadan WM, Kashir J, Jones C, Coward K. 2012. Oocyte activation and phospholipase C zeta ( PLC ζ ): diagnostic and therapeutic implications for assisted reproductive technology. Cell Commun Signal. 10:12–32. DOI:10.1186/1478-811X-10-12.

Rao BS, Naidu KS, Amarnath D, Vagdevi R, Rao AS, Brahmaiah K V., Rao VH. 2002. In vitro maturation of sheep oocytes in different media during breeding and non-breeding seasons. Small Rumin Res. 43:31–36. DOI:10.1016/S0921-4488(01)00254-1.

Rizos D, Clemente M, Bermejo-Alvarez P, De La Fuente J, Lonergan P, Gutiérrez-Adán A. 2008. Consequences of in vitro culture conditions on embryo development and quality. Reprod Domest Anim. 43:44–50. DOI:10. 1111/j.1439-0531.2008.01230.x.

Rocha-Frigoni NAS, Leão BCS, Dall'Acqua PC, Mingoti GZ. 2016. Improving the cytoplasmic maturation of bovine oocytes matured in vitro with intracellular and/or extracellular antioxidants is not associated with increased rates of embryo development. Theriogenology. 86:1897–1905. DOI:10.1016/j.theriogenology.2016.0 6.009.

Rodríguez-Gonzáles E, López-Bejar M, Izquierdo D, Paramio MT. 2003. Developmental competence of prepubertal goat oocytes selected with brilliant cresyl blue and matured with cysteamine supplementation. Reprod Nutr Dev. 43:179–187. DOI:10.1051/rnd:2003012.

Rojas J, Hinostroza F, Vergara S, Pinto-Borguero I, Aguilera F, Fuentes R, Carvacho I. 2021. Knockin' on Egg's Door: Maternal Control of Egg Activation That Influences Cortical Granule Exocytosis in Animal Species. Front Cell Dev Biol. 9:1–20. DOI:10.3389/fcell.2021.704867.

Shirazi A, Golestanfar A, Bashiri M, Ahmadi E. 2018. Male Pronuclear Formation and Embryo Development Following Intracytoplasmic Injection of Ovine Pretreated Sperm. Avicenna J Med Biothechnology. 10:41–48.

Shirazi A, Shams-Esfandabadi N, Ahmadi E, Heidari B. 2010. Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development. Reprod Domest Anim. 45:530–536. DOI:10.11 11/j.1439-0531.2008.01290.x.

Simon H, Haj-Yehia A, Levi-Schaffer F. 2000. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 5:415–418.

Slavík T, Libik M, Wierzchos E, Fulka J. 2005. An attempt to reduce polyspermic penetration in lamb oocytes. Folia Biol. 51:34–39.

Songsasen N. 2012. Energy Metabolism Regulating Mammalian Oocyte Maturation. Meiosis - Mol Mech Cytogenet Divers. DOI:10.5772/33752.

Soto-Heras S, Paramio MT. 2020. Impact of oxidative stress on oocyte competence for in vitro embryo production programs. Res Vet Sci. 132:342–350. DOI:10. 1016/j.rvsc.2020.07.013.

Sun JT, Liu JH, Jiang XQ, Luo X, Yuan JD, Zhang Q, Qi XY, Lee S, Liu ZH, Jin JX. 2022. Tannin Reduces the Incidence of Polyspermic Penetration in Porcine Oocytes. Antioxidants. 11. DOI:0.3390/antiox11102027.

Sutton ML, Gilchrist RB, Thompson JG. 2003. Effect of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Update. 9:35–48. DOI:10.1093/humupd/dmg009.

Swain JE, Pool TB. 2008. ART failure: Oocyte contributions to unsuccessful fertilization. Hum Reprod Update. 14:431–446. DOI:10.1093/humupd/dmn025.

Urdaneta A, Jiménez AR, Paramio MT, Izquierdo D. 2004. Cysteamine, glutathione and ionomycin treatments improve in vitro fertilization of prepubertal goat oocytes. Zygote. 12:277–284. DOI:10.1017/S09671994040028 74.

Wang T, Gao YY, Chen L, Nie ZW, Cheng W, Liu X, Schatten H, Zhang X, Miao YL. 2017. Melatonin prevents postovulatory oocyte aging and promotes subsequent embryonic development in the pig. Aging. 9:1552–1564. DOI:10.18632/aging.101252.

Wang WH, Day BN, Wu GM. 2003. How does polyspermy happen in mammalian oocytes?. Microsc Res Tech. 6:335–341. DOI:0.1002/jemt.10346.

Warzych E, Lipinska P. 2020. Energy metabolism of follicular environment during oocyte growth and maturation. J Reprod Dev. 66:1–7. DOI:0.1262/jrd.2019-102.

Xia P. 2013. Biology of Polyspermy in IVF and its Clinical Indication. Curr Obstet Gynecol Rep. 2:226–231. DOI:10.1007/s13669-013-0059-2.

Xie HL, Wang YB, Jiao GZ, Kong DL, Li Q, Li H, Zheng LL, Tan JH. 2016. Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci Rep. 6:1–11. DOI:10.1038/srep20764.

Zhu J, Moawad AR, Wang CY, Li HF, Ren JY, Dai YF. 2018. Advances in in-vitro production of sheep embryos. Int J Vet Sci Med. 6:S15–S26. DOI:10.1016/j.ijvsm.2018.02. 003.

Zullo G, Albero G, Neglia G, De Canditiis C, Bifulco G, Campanile G, Gasparrini B. 2016. L-ergothioneine supplementation during culture improves quality of bovine in vitro-produced embryos. Theriogenology. 85:688–697. DOI:10.1016/j.theriogenology.2015.10.008.

Refbacks

  • There are currently no refbacks.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.



Bookmark and Share