Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-2017-AR986
Animal Reproduction (AR)
Original Article

Oocyte maturation with royal jelly increases embryo development and reduces apoptosis in goats

Arash Veshkini, Abdollah Mohammadi-Sangcheshmeh, Nasser Ghanem, Amir Hossein Abazari-kia, Elmira Mottaghi, Reza Kamaledini, Hamid Deldar, Irfan Ozturk, Eduardo Leite Gastal

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Abstract

Royal jelly (RJ) was supplemented to goat oocyte in vitro maturation (IVM) medium at three different concentrations (2.5, 5, and 10 mg/ml). Maturation rate, embryo cleavage, and blastocyst rate were recorded. Gene expression of apoptosis-related transcripts was investigated in matured oocytes. Percentage of oocytes that reached MII-stage was increased in RJ-treated groups compared to the control group. Glutathione (GSH) content of mature oocytes was enhanced when RJ was added to IVM medium at any supplementation compared with control. Percentage of cleaved embryos and blastocysts was higher in the RJ-treated groups at a concentration of 5 mg/ml than in the 2.5 mg/ml and control group. Total number of cells per blastocyst was not different in the control and RJtreated group at 5 mg/ml. However, number of apoptotic cells per blastocyst was higher in the control group than in the RJ-treated group at 5 mg/ml. Expression profile of Bax, and p53 was down-regulated while Bcl-2 was upregulated in oocytes treated with RJ at 5 and 10 mg/ml compared with the control group. Addition of RJ at concentrations of 5 mg/ml improved embryo production through increasing maturation rate. RJ seems to improve the IVM microenvironment by reducing expression of genes inducing apoptosis, enhancing GSH content, and reducing incidence of apoptosis in blastocysts.

Keywords

embryo, gene expression, in vitro fertilization, oocyte, royal jelly.

References

Abazari-Kia AH, Mohammadi-Sangcheshmeh A, Dehghani-Mohammadabadi M, Jamshidi-Adegani F, Veshkini A, Zhandi M, Cinar MU, Salehi M. 2014. Intracellular glutathione content, developmental competence and expression of apoptosis-related genes associated with G6PDH-activity in goat oocyte. J Assist Reprod Genet, 31:313-321.

Abazari-Kia AH, Dehghani-Mohammadabadi M, Mohammadi-Sangcheshmeh A, Zhandi M, Salehi M. 2015. Regulation of embryonic development and apoptotic-related gene expression by brain-derived neurotrophic factor in two different culture conditions in ovine. Theriogenology, 84:62-69.

Albuz F, Sasseville M, Lane M, Armstrong D, Thompson J, Gilchrist R. 2010. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod, 25:2999-3011.

Ali A, Bilodeau J, Sirard M. 2003. Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology, 59:939-949.

Bărnuţiu LI, Mărghitaş LA, Dezmirean DS, Mihai CM, Bobiş O. 2011. Chemical composition and antimicrobial activity of Royal Jelly. Review. Sci Pap Anim Sci Biotechnol, 44:67-72.

Boselli E, Caboni M, Sabatini A, Marcazzan G, Lercker G. 2003. Determination and changes of free amino acids in royal jelly during storage. Apidologie, 34:129-137.

Brackett BG, Zuelke KA. 1993. Analysis of factors involved in the in vitro production of bovine embryos. Theriogenology, 39:43-64.

Brad A, Bormann C, Swain J, Durkin R, Johnson A, Clifford A, Krisher R. 2003. Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol Reprod Dev, 64:492-498.

Choi B-H, Bang J-I, Jin J-I, Kim S-S, Jo H-T, Deb GK, Ghanem N, Cho K-W, Kong I-K. 2013.

Coculturing cumulus oocyte complexes with denuded oocytes alters zona pellucida ultrastructure in in vitro matured bovine oocytes. Theriogenology, 80:1117- 1123.

Choi YH, Love CC, Varner DD, Thompson JA, Hinrichs K. 2001. Activation of cumulus-free equine oocytes: effect of maturation medium, calcium ionophore concentration and duration of cycloheximide exposure. Reproduction, 122:177-183.

Combelles CM, Gupta S, Agarwal A. 2009. Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online, 18:864-880.

Cox JF, Alfaro V. 2007. In vitro fertilization and development of OPU derived goat and sheep oocytes. Reprod Domest Anim, 42:83-87. de Matos DG, Furnus CC, Moses DF, Baldassarre H. 1995. Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol Reprod Dev, 42:432-436.

de Matos DG, Furnus C, Moses D, Martinez A, Matkovic M. 1996. Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol Reprod Dev, 45:451-457.

de Matos DG, Furnus CC. 2000. The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of betamercaptoethanol, cysteine and cystine. Theriogenology, 53:761-771.

Dey S, Deb G, Ha A, Lee J, Bang J, Lee K, Kong I. 2012. Coculturing denuded oocytes during the in vitro maturation of bovine cumulus oocyte complexes exerts a synergistic effect on embryo development. Theriogenology, 77:1064-1077.

Do L, Shibata Y, Taniguchi M, Nii M, Nguyen T, Tanihara F, Takagi M, Otoi T. 2015. Melatonin supplementation during in vitro maturation and development supports the development of porcine embryos. Reprod Domest Anim, 50:1054-1058.

Edward R. 2007. Are minimal stimulation IVF and IVM set to replace routine IVF? Reprod Biomed Online, 14:267-270.

El-Nekeety AA, El-Kholy W, Abbas NF, Ebaid A, Amra HA, Abdel-Wahhab MA. 2007. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon, 50:256-269.

Elnagar S. 2010. Royal jelly counteracts bucks’summer infertility. Anim Reprod Sci, 121:174-180.

Elnagar S, Elghalid O, Abd-Elhady A. 2010. Royal jelly: can it reduce physiological strain of growing rabbits under Egyptian summer conditions? Animal, 4:1547-1552.

Fakruzzaman M, Ghanem N, Bang J-I, Ha A-N, Lee K-L, Sohn S-H, Wang Z, Lee D-S, Kong I-K. 2015.

Effect of peroxiredoxin II on the quality and mitochondrial activity of pre-implantation bovine embryos. Anim Reprod Sci, 159:172-183.

Favetta LA, John EJS, King WA, Betts DH. 2007. High levels of p66 shc and intracellular ROS in permanently arrested early embryos. Free Radic Biol Med, 42:1201-1210.

Furnus C, De Matos D, Picco S, García P. P, Inda A, Mattioli G, Errecalde A. 2008. Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim Reprod Sci, 109:88-99.

Gardiner CS, Reed DJ. 1995. Synthesis of glutathione in the preimplantation mouse embryo. Arch Biochem Biophys, 318:30-36.

Ghanem N, Ha A-N, Fakruzzaman M, Bang J-I, Lee S-C, Kong I-K. 2014. Differential expression of selected candidate genes in bovine embryos produced in vitro and cultured with chemicals modulating lipid metabolism. Theriogenology, 82:238-250.

Greve T, Xu K, Callesen H, Hyttel P. 1987. In vivo development of in vitro fertilized bovine oocytes matured in vivo versus in vitro. J In Vitro Fert Embryo Transf, 4:281-285.

Guerin P, El Mouatassim S, Menezo Y. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update, 7:175-189.

Guo H, Kouzuma Y, Yonekura M. 2009. Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chem, 113:238-245.

Hashimoto S, Minami N, Yamada M, Imai H. 2000. Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol Reprod Dev, 56:520-526.

Howe S, Dimick P, Benton A. 1985. Composition of freshly harvested and commercial royal jelly. J Apicult Res, 24:52-61.

Husein M, Haddad S. 2006. A new approach to enhance reproductive performance in sheep using royal jelly in comparison with equine chorionic gonadotropin. Anim Reprod Sci, 93:24-33.

Isidorova VA, Czyzewskaa U, Isidorovab AG, Bakier S. 2009. Gas chromatographic and mass spectrometric characterization of the organic acids extracted from some preparations containing lyophilized royal jelly. J Chromatogr B Analyt Technol Biomed Life Sc., 877:3776-3780.

Jin J, Lee S, Khoirinaya C, Oh A, Kim G, Lee B. 2016. Supplementation with spermine during in vitro maturation of porcine oocytes improves early embryonic development after parthenogenetic activation and somatic cell nuclear transfer. J Anim Sci, 94:963- 970.

Kim E, Jeon Y, Kim DY, Lee E, Hyun S-H. 2015. Antioxidative effect of carboxyethylgermanium sesquioxide (Ge-132) on IVM of porcine oocytes and subsequent embryonic development after parthenogenetic activation and IVF. Theriogenology, 84:226-236.

Kodai T, Umebayashi K, Nakatani T, Ishiyama K, Noda N. 2007. Compositions of royal jelly II. Organic acid glycosides and sterols of the royal jelly of honeybees (Apis mellifera). Chem Pharm Bull (Tokyo), 55:1528-1531.

Kridli R, Husein M, Humphrey W. 2003. Effect of royal jelly and GnRH on the estrus synchronization and pregnancy rate in ewes using intravaginal sponges. Small Rumin Res, 49:25-30.

Kridli R, Al-Khetib S. 2006. Reproductive responses in ewes treated with eCG or increasing doses of royal jelly. Anim Reprod Sci, 92:75-85.

Kwak S-S, Cheong S-A, Jeon Y, Lee E, Choi K-C, Jeung E-B, Hyun S-H. 2012. The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology, 78 86-101.

Leyens G, Knoops B, Donnay I. 2004. Expression of peroxiredoxins in bovine oocytes and embryos produced in vitro. Mol Reprod Dev, 69:243-251.

Lorenzo P, Illera M, Illera J, Illera M. 1994. Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. J Reprod Fertil, 101:697-701.

Maleki EM, Eimani H, Bigdeli MR, Narenji AG, Abedi R. 2016. Effects of crocin supplementation during in vitro maturation of mouse oocytes on glutathione synthesis and cytoplasmic maturation. Int J Fertil Steril, 10:53-61.

Mishra A, Reddy I, Gupta P, Mondal S. 2016. Lcarnitine mediated reduction in oxidative stress and alteration in transcript level of antioxidant enzymes in sheep embryos produced in vitro. Reprod Domest Anim, 51:311-321.

Mohammadi-Sangcheshmeh A, Soleimani M, Deldar H, Salehi M, Soudi S, Hashemi SM, Schellander K, Hoelker M. 2012. Prediction of oocyte developmental competence in ovine using glucose-6-phosphate dehydrogenase (G6PDH) activity determined at retrieval time. J Assist Reprod Genet, 29:153-158.

Moradi A, Malekinejad H, Farrokhi-Ardabili F, Bernousi I. 2013. Royal Jelly improves the sperm parameters of ram semen during liquid storage and serves as an antioxidant source. Small Rumin Res, 113:346-352.

Mukherjee A, Malik H, Saha AP, Dubey A, Singhal DK, Boateng S, Saugandhika S, Kumar S, De S, Guha SK, Malakar D. 2014. Resveratrol treatment during goat oocytes maturation enhances developmental competence of parthenogenetic and hand-made cloned blastocysts by modulating intracellular glutathione level and embryonic gene expression. J Assist Reprod Genet, 31:229-239.

Nagai T, Inoue R. 2004. Preparation and functional properties of water extract and alkaline extract of royal jelly. Food Chem, 84:181-186.

Oyawoye O, Gadir AA, Garner A, Constantinovici N, Perrett C, Hardiman P. 2003. Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum Reprod, 18:2270-2274.

Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. 2002. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev, 61:234-248.

Rodríguez‐González E, López‐Bejar M, Mertens MJ, Paramio MT. 2003. Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes. Mol Reprod Dev, 65:446-453.

Romero-Arredondo A, Seidel GE Jr. 1996. Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development. Biol Reprod, 55:1012-1016.

Shahzad Q, Mehmood MU, Khan H, ul Husna A, Qadeer S, Azam A, Naseer Z, Ahmad E, Safdar M, Ahmad M. 2016. Royal jelly supplementation in semen extender enhances post-thaw quality and fertility of Nili-Ravi buffalo bull sperm. Anim Reprod Sci, 167:83- 88.

Silici S, Ekmekcioglu O, Eraslan G, Demirtas A. 2009. Antioxidative effect of royal jelly in cisplatininduced testes damage. Urology, 74:545-551.

Soto-Heras S, Roura M, Catalá MG, MenéndezBlanco I, Izquierdo D, Fouladi-Nashta AA, Paramio MT. 2018. Beneficial effects of melatonin on in vitro embryo production from juvenile goat oocytes. Reprod Fertil Dev, 30:253-261.

Souza-Fabjan JM, Locatelli Y, Duffard N, Corbin E, Touzé JL, Perreau C, Beckers JF, Freitas VJ, Mermillod P. 2014. In vitro embryo production in goats: slaughterhouse and laparoscopic ovum pick up– derived oocytes have different kinetics and requirements regarding maturation media. Theriogenology, 81:1021- 1031.

Souza-Fabjan JMG, Locatelli Y, Duffard N, Corbin E, Batista RITP, de Figueirêdo Freitas VJ, Beckers JF, Mermillod P. 2016. Intrinsic quality of goat oocytes already found denuded at collection for in vitro embryo production. Theriogenology, 86:1989-1998.

Sutton M, Gilchrist R, Thompson J. 2003. Effects 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.

Tamura S, Kono T, Harada C, Yamaguchi K, Moriyama T. 2009. Estimation and characterisation of major royal jelly proteins obtained from the honeybee Apis merifera. Food Chem, 114:1491-1497.

Tarin JJ, Vendrell FJ, Ten J, Blanes R, Van Blerkom J, Cano A. 1996. The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes. Mol Hum Reprod, 2:895-901.

Valiollahpoor Amiri M, Deldar H, Pirsaraei ZA. 2016. Impact of supplementary royal jelly on in vitro maturation of sheep oocytes: genes involved in apoptosis and embryonic development. Syst Biol Reprod Med, 62:31-38.

Van Soom A, Vandaele L, Goossens K, de Kruif A, Peelman L. 2007. Gamete origin in relation to early embryo development. Theriogenology, 68:S131-S137.

Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Pérez-Alvarez JA. 2008. Functional properties of honey, propolis, and royal jelly. J Food Sci, 73:117-124.

Wrenzycki C, Stinshoff H. 2013. Maturation environment and impact on subsequent developmental competence of bovine oocytes. Reprod Domest Anim, 48:38-43.

Yoneda A, Suzuki K, Mori T, Ueda J, Watanabe T. 2004. Effects of delipidation and oxygen concentration on in vitro development of porcine embryos. J Reprod Dev, 50:287-295.

Zhou Z, Jia RX, Zhang G, Wan Y, Zhang Y, Fan Y, Wang Z, Huang P, Wang F. 2016. Using cysteine/cystine to overcome oxidative stress in goat oocytes and embryos cultured in vitro. Mol Med Rep, 14:1219-1226.

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