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Effects of EGF and melatonin on gene expression of cumulus cells and further in vitro embryo development in bovines

Published online by Cambridge University Press:  08 June 2022

A. Cordova ,
M. S. Miranda Open the ORCID record for M. S. Miranda [Opens in a new window] ,
W. A. King  and
G. F. Mastromonaco
A. Cordova
Affiliation:
University of Guelph, Department of Biomedical Sciences, 50 Stone Road E, Guelph, ON N1G2W1 Canada Reproductive Physiology, Toronto Zoo Scarborough, ON, Canada
M. S. Miranda*
Affiliation:
Instituto de Medicina Veterinária, Universidade Federal do Pará, BR-316 Km 61, Castanhal, PA 68740-970, Brazil
W. A. King
Affiliation:
University of Guelph, Department of Biomedical Sciences, 50 Stone Road E, Guelph, ON N1G2W1 Canada
G. F. Mastromonaco
Affiliation:
University of Guelph, Department of Biomedical Sciences, 50 Stone Road E, Guelph, ON N1G2W1 Canada Reproductive Physiology, Toronto Zoo Scarborough, ON, Canada
*
Author for correspondence: Moysés dos Santos Miranda. Instituto de Medicina Veterinária, Universidade Federal do Pará, BR-316 Km 61, Castanhal, PA 68740-970, Brazil. E-mail: [email protected]
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Summary

Despite previous research demonstrating the benefits of including growth factors and antioxidants to maturation medium to support embryo production, to date the effect of epidermal growth factor (EGF) and melatonin (Mel) on oocyte competency has not been studied. This study supplemented in vitro maturation (IVM) medium with EGF (10 ng/ml) and Mel (50 ng/ml) alone, or in combination, and evaluated cumulus cell (CC) gene expression and the development and quality of parthenogenetic blastocysts. No differences in CC gene expression levels indicative of developmental potential were found among the treatment groups. Antioxidant gene CuZnSOD was significantly (P < 0.05) decreased in CCs from the Mel group. Moreover, blastocyst rates on day 7 were significantly increased in EGF or Mel (P < 0.05), but not EGF+Mel. Significant decrease (P < 0.05) in GPX1, CuZnSOD, SLC2A1 and HSPA1A (P = 0.07) mRNA levels was observed in blastocysts from the Mel group. OCT4 gene expression was significantly increased (P < 0.05) in EGF+Mel and confirmed using immunofluorescence. Our results indicate that, despite the lack of changes of competence-related genes in CCs, IVM medium supplemented with Mel improved the culture environment sufficiently, resulting in improved blastocysts. Moreover, EGF and Mel combined during maturation increased OCT4 gene and protein expression in blastocysts, indicating its potential for stem cells.

Keywords

Cumulus cellsEpidermal growth factorMelatoninOCT4Parthenogenesis
Type
Research Article
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 600 - 610
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abecia, J. A., Forcada, F. and Zúñiga, O. (2002). The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro . Veterinary Research Communications, 26(2), 151–158. doi: 10.1023/a:1014099719034 CrossRefGoogle ScholarPubMed
Abeydeera, L. R., Wang, W. H., Cantley, T. C., Rieke, A., Prather, R. S. and Day, B. N. (1998). Presence of epidermal growth factor during in vitro maturation of pig oocytes and embryo culture can modulate blastocyst development after in vitro fertilization. Molecular Reproduction and Development, 51(4), 395–401. doi: 10.1002/(SICI)1098-2795(199812)51:4<395::AID-MRD6>3.0.CO;2-Y 3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Amarnath, D., Li, X., Kato, Y. and Tsunoda, Y. (2007). Gene expression in individual bovine somatic cell cloned embryos at the 8-cell and blastocyst stages of preimplantation development. Journal of Reproduction and Development, 53(6), 1247–1263. doi: 10.1262/jrd.19096 CrossRefGoogle ScholarPubMed
Anchordoquy, J. M., Anchordoquy, J. P., Testa, J. A., Sirini, M. Á. and Furnus, C. C. (2015). Influence of vascular endothelial growth factor and cysteamine on in vitro bovine oocyte maturation and subsequent embryo development. Cell Biology International, 39(10), 1090–1098. doi: 10.1002/cbin.10481 CrossRefGoogle ScholarPubMed
Assidi, M., Dieleman, S. J. and Sirard, M. A. (2010). Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: Potential early markers of oocyte competence. Reproduction, 140(6), 835–852. doi: 10.1530/REP-10-0248 CrossRefGoogle ScholarPubMed
Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S. and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro . Biology of Reproduction, 79(2), 209–222. doi: 10.1095/biolreprod.108.067686 CrossRefGoogle ScholarPubMed
Balasubramanian, S. and Rho, G. J. (2007). Effect of cysteamine supplementation of in vitro matured bovine oocytes on chilling sensitivity and development of embryos. Animal Reproduction Science, 98(3–4), 282–292. doi: 10.1016/j.anireprosci.2006.03.011 CrossRefGoogle ScholarPubMed
Banwell, K. M., Lane, M., Russell, D. L., Kind, K. L. and Thompson, J. G. (2007). Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Human Reproduction, 22(10), 2768–2775. doi: 10.1093/humrep/dem203 CrossRefGoogle ScholarPubMed
Betts, D. H., Bain, N. T. and Madan, P. (2014). The p66(Shc) adaptor protein controls oxidative stress response in early bovine embryos. PLoS One, 9(1), e86978. doi: 10.1371/journal.pone.0086978 CrossRefGoogle ScholarPubMed
Bhardwaj, R., Ansari, M. M., Pandey, S., Parmar, M. S., Chandra, V., Kumar, G. S. and Sharma, G. T. (2016). GREM1, EGFR, and HAS2; the oocyte competence markers for improved buffalo embryo production in vitro . Theriogenology, 86(8), 2004–2011. doi: 10.1016/j.theriogenology.2016.06.019 CrossRefGoogle ScholarPubMed
Boni, R., Tosti, E., Roviello, S. and Dale, B. (1999). Intercellular communication in vivo- and in vitro-produced bovine embryos. Biology of Reproduction, 61(4), 1050–1055. doi: 10.1095/biolreprod61.4.1050 CrossRefGoogle ScholarPubMed
Choi, W. J., Lee, J. H., Lee, S. H., Yum, S. Y., Lee, S. J., Lim, C. W. and Jang, G. (2016). Developmental competence and cryotolerance of caprine parthenogenetic embryos cultured in chemically defined media. Theriogenology, 86(2), 596–603. doi: 10.1016/j.theriogenology.2016.02.012 CrossRefGoogle ScholarPubMed
Córdova, B., Morató, R., Izquierdo, D., Paramio, T. and Mogas, T. (2010). Effect of the addition of insulin-transferrin-selenium and/or L-ascorbic acid to the in vitro maturation of prepubertal bovine oocytes on cytoplasmic maturation and embryo development. Theriogenology, 74(8), 1341–1348. doi: 10.1016/j.theriogenology.2010.06.003 CrossRefGoogle ScholarPubMed
Dalvit, G., Llanes, S. P., Descalzo, A., Insani, M., Beconi, M. and Cetica, P. (2005). Effect of alpha-tocopherol and ascorbic acid on bovine oocyte in vitro maturation. Reproduction in Domestic Animals, 40(2), 93–97. doi: 10.1111/j.1439-0531.2004.00522.x CrossRefGoogle ScholarPubMed
De La Fuente, R., O’Brien, M. J. and Eppig, J. J. (1999). Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Human Reproduction, 14(12), 3060–3068. doi: 10.1093/humrep/14.12.3060 CrossRefGoogle ScholarPubMed
Do, L. T., Shibata, Y., Taniguchi, M., Nii, M., Nguyen, T. V., Tanihara, F., Takagi, M. and Otoi, T. (2015). Melatonin supplementation during in vitro maturation and development supports the development of porcine embryos. Reproduction in Domestic Animals, 50(6), 1054–1058. doi: 10.1111/rda.12607 CrossRefGoogle ScholarPubMed
Driver, A. M., Peñagaricano, F., Huang, W., Ahmad, K. R., Hackbart, K. S., Wiltbank, M. C. and Khatib, H. (2012). RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics, 13, 118. doi: 10.1186/1471-2164-13-118 CrossRefGoogle ScholarPubMed
Duan, X. X., Ou, J. S., Li, Y., Su, J. J., Ou, C., Yang, C., Yue, H. F. and Ban, K. C. (2005). Dynamic expression of apoptosis-related genes during development of laboratory hepatocellular carcinoma and its relation to apoptosis. World Journal of Gastroenterology, 11(30), 4740–4744. doi: 10.3748/wjg.v11.i30.4740 CrossRefGoogle Scholar
Dyce, P. W., Liu, J., Tayade, C., Kidder, G. M., Betts, D. H. and Li, J. (2011). In vitro and in vivo germ line potential of stem cells derived from newborn mouse skin. PLoS ONE, 6(5), e20339. doi: 10.1371/journal.pone.0020339 CrossRefGoogle ScholarPubMed
El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A. E., Sosa, G. A., El-Roos, M. E. and Nagai, T. (2011). Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Molecular Reproduction and Development, 78(4), 250–262. doi: 10.1002/mrd.21295 CrossRefGoogle ScholarPubMed
El-Sanea, A. M., Abdoon, A. S. S., Kandil, O. M., El-Toukhy, N. E., El-Maaty, A. M. A. and Ahmed, H. H. (2021). Effect of oxygen tension and antioxidants on the developmental competence of buffalo oocytes cultured in vitro . Veterinary World, 14(1), 78–84. doi: 10.14202/vetworld.2021.78-84 CrossRefGoogle ScholarPubMed
Farin, C. E., Rodriguez, K. F., Alexander, J. E., Hockney, J. E., Herrick, J. R. and Kennedy-Stoskopf, S. (2007). The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro . Animal Reproduction Science, 98(1–2), 97–112. doi: 10.1016/j.anireprosci.2006.10.007 CrossRefGoogle ScholarPubMed
Fischer, T. W., Slominski, A., Zmijewski, M. A., Reiter, R. J. and Paus, R. (2008). Melatonin as a major skin protectant: From free radical scavenging to DNA damage repair. Experimental Dermatology, 17(9), 713–730. doi: 10.1111/j.1600-0625.2008.00767.x CrossRefGoogle ScholarPubMed
Galano, A., Tan, D. X. and Reiter, R. J. (2011). Melatonin as a natural ally against oxidative stress: A physicochemical examination. Journal of Pineal Research, 51(1), 1–16. doi: 10.1111/j.1600-079X.2011.00916.x CrossRefGoogle ScholarPubMed
Gómez, E., Caamaño, J. N., Bermejo-Alvarez, P., Díez, C., Muñoz, M., Martín, D., Carrocera, S. and Gutiérrez-Adán, A. (2009a). Gene expression in early expanded parthenogenetic and in vitro fertilized bovine blastocysts. Journal of Reproduction and Development, 55(6), 607–614. doi: 10.1262/jrd.09-077m CrossRefGoogle ScholarPubMed
Gómez, E., Gutiérrez-Adán, A., Díez, C., Bermejo-Alvarez, P., Muñoz, M., Rodriguez, A., Otero, J., Alvarez-Viejo, M., Martín, D., Carrocera, S. and Caamaño, J. N. (2009b). Biological differences between in vitro produced bovine embryos and parthenotes. Reproduction, 137(2), 285–295. doi: 10.1530/REP-08-0220 CrossRefGoogle ScholarPubMed
Guérin, P., El Mouatassim, S. and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update, 7(2), 175–189. doi: 10.1093/humupd/7.2.175 CrossRefGoogle ScholarPubMed
Guimarães, A. L., Pereira, S. A., Diógenes, M. N. and Dode, M. A. (2016). Effect of insulin-transferrin-selenium (ITS) and l-ascorbic acid (AA) during in vitro maturation on in vitro bovine embryo development. Zygote, 24(6), 890–899. doi: 10.1017/S0967199416000228 CrossRefGoogle ScholarPubMed
Hasler, J. F. (2000). In-vitro production of cattle embryos: Problems with pregnancies and parturition. Human Reproduction, 15, Suppl. 5, 47–58. doi: 10.1093/humrep/15.suppl_5.47 CrossRefGoogle ScholarPubMed
Ikeda, S., Imai, H. and Yamada, M. (2003). Apoptosis in cumulus cells during in vitro maturation of bovine cumulus-enclosed oocytes. Reproduction, 125(3), 369–376. doi: 10.1530/rep.0.1250369 CrossRefGoogle ScholarPubMed
Ishizuka, B., Kuribayashi, Y., Murai, K., Amemiya, A. and Itoh, M. T. (2000). The effect of melatonin on in vitro fertilization and embryo development in mice. Journal of Pineal Research, 28(1), 48–51. doi: 10.1034/j.1600-079x.2000.280107.x CrossRefGoogle ScholarPubMed
Itoh, M. T., Ishizuka, B., Kuribayashi, Y., Amemiya, A. and Sumi, Y. (1999). Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Molecular Human Reproduction, 5(5), 402–408. doi: 10.1093/molehr/5.5.402 CrossRefGoogle ScholarPubMed
Jiang, W. J., Yao, X. R., Zhao, Y. H., Gao, Q. S., Jin, Q. G., Li, Y. H., Yan, A. G. and Xu, Y. N. (2019). L-Carnitine prevents bovine oocyte aging and promotes subsequent embryonic development. Journal of Reproduction and Development, 65(6), 499–506. doi: 10.1262/jrd.2019-046 CrossRefGoogle ScholarPubMed
Kaneda, M., Takahashi, M., Yamanaka, K. I., Saito, K., Taniguchi, M., Akagi, S., Watanabe, S. and Takashi, N. (2017). Epigenetic analysis of bovine parthenogenetic embryonic fibroblasts. Journal of Reproduction and Development, 19(63), 365–375.CrossRefGoogle Scholar
Kang, J. T., Koo, O. J., Kwon, D. K., Park, H. J., Jang, G., Kang, S. K. and Lee, B. C. (2009). Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. Journal of Pineal Research, 46(1), 22–28. doi: 10.1111/j.1600-079X.2008.00602.x CrossRefGoogle ScholarPubMed
Khurana, N. K. and Niemann, H. (2000a). Effects of cryopreservation on glucose metabolism and survival of bovine morulae and blastocysts derived in vitro or in vivo . Theriogenology, 54(2), 313–326. doi: 10.1016/S0093-691X(00)00351-4 CrossRefGoogle ScholarPubMed
Khurana, N. K. and Niemann, H. (2000b). Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo . Biology of Reproduction, 62(4), 847–856. doi: 10.1095/biolreprod62.4.847 CrossRefGoogle ScholarPubMed
Kim, M. K., Park, E. A., Kim, H. J., Choi, W. Y., Cho, J. H., Lee, W. S., Cha, K. Y., Kim, Y. S., Lee, D. R. and Yoon, T. K. (2013). Does supplementation of in-vitro culture medium with melatonin improve IVF outcome in PCOS? Reproductive Biomedicine Online, 26(1), 22–29. doi: 10.1016/j.rbmo.2012.10.007 CrossRefGoogle ScholarPubMed
Knijn, H. M., Wrenzycki, C., Hendriksen, P. J., Vos, P. L., Herrmann, D., van der Weijden, G. C., Niemann, H. and Dieleman, S. J. (2002). Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo . Reproduction, 124(3), 365–375. doi: 10.1530/rep.0.1240365 CrossRefGoogle ScholarPubMed
Korhonen, K., Kananen, K., Ketoja, E., Matomäki, J., Halmekytö, M. and Peippo, J. (2010). Effects of serum-free in vitro maturation of bovine oocytes on subsequent embryo development and cell allocation in two developmental stages of day 7 blastocysts. Reproduction in Domestic Animals, 45(1), 42–49. doi: 10.1111/j.1439-0531.2008.01203.x CrossRefGoogle ScholarPubMed
Kwak, S. S., Cheong, S. A., Jeon, Y., Lee, E., Choi, K. C., Jeung, E. B. and 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(1), 86–101. doi: 10.1016/j.theriogenology.2012.01.024 CrossRefGoogle ScholarPubMed
Labrecque, R. and Sirard, M. A. (2011). Gene expression analysis of bovine blastocysts produced by parthenogenic activation or fertilization. Reproduction, Fertility, and Development, 23(4), 591–602. doi: 10.1071/RD10243 CrossRefGoogle ScholarPubMed
Lager, A. E., Kocabas, A. M., Otu, H. H., Ruppel, P., Langerveld, A., Schnarr, P., Suarez, M., Jarrett, J. C., Conaghan, J., Rosa, G. J., Fernandez, E., Rawlins, R. G., Cibelli, J. B. and Crosby, J. A. (2013). Identification of a novel gene set in human cumulus cells predictive of an oocyte’s pregnancy potential. Fertility and Sterility, 99(3), 745–752 e6.Google Scholar
Leibfried-Rutledge, M. L. (1999). Factors determining competence of in vitro produced cattle embryos. Theriogenology, 51(2), 473–485. doi: 10.1016/S0093-691X(98)00241-6 CrossRefGoogle ScholarPubMed
Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25(4), 402–408. doi: 10.1006/meth.2001.1262 CrossRefGoogle ScholarPubMed
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H. and Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro . Biology of Reproduction, 54(6), 1420–1429. doi: 10.1095/biolreprod54.6.1420 CrossRefGoogle ScholarPubMed
Lott, W. M., Anchamparuthy, V. M., Mcgilliard, M. L., Mullarky, I. K. and Gwazdauskas, F. C. (2011). Influence of cysteine in conjunction with growth factors on the development of in vitro-produced bovine embryos. Reproduction in Domestic Animals, 46(4), 585–594. doi: 10.1111/j.1439-0531.2010.01706.x CrossRefGoogle ScholarPubMed
Machado, M. F., Caixeta, E. S., Sudiman, J., Gilchrist, R. B., Thompson, J. G., Lima, P. F., Price, C. A. and Buratini, J. (2015). Fibroblast growth factor 17 and bone morphogenetic protein 15 enhance cumulus expansion and improve quality of in vitro-produced embryos in cattle. Theriogenology, 84(3), 390–398. doi: 10.1016/j.theriogenology.2015.03.031 CrossRefGoogle ScholarPubMed
Makarevich, A. V. and Markkula, M. (2002). Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biology of Reproduction, 66(2), 386–392. doi: 10.1095/biolreprod66.2.386 CrossRefGoogle ScholarPubMed
Manda, K., Anzai, K., Kumari, S. and Bhatia, A. L. (2007). Melatonin attenuates radiation-induced learning deficit and brain oxidative stress in mice. Acta Neurobiologiae Experimentalis, 67(1), 63–70.Google ScholarPubMed
Mao, J., Smith, M. F., Rucker, E. B., Wu, G. M., McCauley, T. C., Cantley, T. C., Prather, R. S., Didion, B. A. and Day, B. N. (2004). Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro . Journal of Animal Science, 82(7), 1967–1975. doi: 10.2527/2004.8271967x CrossRefGoogle ScholarPubMed
Mastromonaco, G. F., Favetta, L. A., Smith, L. C., Filion, F. and King, W. A. (2007). The influence of nuclear content on developmental competence of gaur x cattle hybrid in vitro fertilized and somatic cell nuclear transfer embryos. Biology of Reproduction, 76(3), 514–523. doi: 10.1095/biolreprod.106.058040 CrossRefGoogle ScholarPubMed
McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P. and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: A predictor of fertilization and embryo selection in women undergoing IVF. Human Reproduction, 19(12), 2869–2874. doi: 10.1093/humrep/deh535 CrossRefGoogle ScholarPubMed
Mehrzadi, S., Safa, M., Kamrava, S. K., Darabi, R., Hayat, P. and Motevalian, M. (2017). Protective mechanisms of melatonin against hydrogen peroxide induced toxicity in human bone-marrow derived mesenchymal stem cells. Canadian Journal of Physiology and Pharmacology, 95(7), 773–786. doi: 10.1139/cjpp-2016-0409 CrossRefGoogle ScholarPubMed
Miranda, Mdos S., Bressan, F. F., De Bem, T. H., Merighe, G. K., Ohashi, O. M., King, W. A. and Meirelles, F. V. (2012). Nuclear transfer with apoptotic bovine fibroblasts: Can programmed cell death be reprogrammed? Cell Reprogram, 14(3), 217–224. doi: 10.1089/cell.2011.0080 CrossRefGoogle Scholar
Muñoz, M., Penarossa, G., Caamaño, J. N., Díez, C., Brevini, T. A. L. and Gómez, E. (2015). Research with parthenogenetic stem cells will help decide whether a safer clinical use is possible. Journal of Tissue Engineering and Regenerative Medicine, 9(4), 325–331. doi: 10.1002/term.1779 CrossRefGoogle ScholarPubMed
Myers, M., Tripurani, S. K., Middlebrook, B., Economides, A. N., Canalis, E. and Pangas, S. A. (2011). Loss of gremlin delays primordial follicle assembly but does not affect female fertility in mice. Biology of Reproduction, 85(6), 1175–1182. doi: 10.1095/biolreprod.111.091728 CrossRefGoogle Scholar
Naturil-Alfonso, C., Saenz-de-Juano, M. D., Peñaranda, D. S., Vicente, J. S. and Marco-Jiménez, F. (2011). Parthenogenic blastocysts cultured under in vivo conditions exhibit proliferation and differentiation expression genes similar to those of normal embryos. Animal Reproduction Science, 127(3–4), 222–228. doi: 10.1016/j.anireprosci.2011.08.005 CrossRefGoogle ScholarPubMed
Niemann, H. and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: Implications for subsequent development. Theriogenology, 53(1), 21–34. doi: 10.1016/s0093-691x(99)00237-x CrossRefGoogle ScholarPubMed
Niwa, H., Miyazaki, J. and Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics, 24(4), 372–376. doi: 10.1038/74199 CrossRefGoogle ScholarPubMed
Palmerini, M. G., Nottola, S. A., Tunjung, W. A., Kadowaki, A., Bianchi, S., Cecconi, S., Sato, E. and Macchiarelli, G. (2016). EGF-FSH supplementation reduces apoptosis of pig granulosa cells in co-culture with cumulus–oocyte complexes. Biochemical and Biophysical Research Communications, 481(1–2), 159–164. doi: 10.1016/j.bbrc.2016.10.151 CrossRefGoogle ScholarPubMed
Park, Y. S. and Lin, Y. C. (1993). Effect of epidermal growth factor (EGF) and defined simple media on in vitro bovine oocyte maturation and early embryonic development. Theriogenology, 39(2), 475–484. doi: 10.1016/0093-691x(93)90390-q CrossRefGoogle ScholarPubMed
Park, K. W., Iga, K. and Niwa, K. (1997). Exposure of bovine oocytes to EGF during maturation allows them to develop to blastocysts in a chemically defined medium. Theriogenology, 48(7), 1127–1135. doi: 10.1016/s0093-691x(97)00345-2 CrossRefGoogle Scholar
Park, S. A., Sung, N. J., Choi, B. J., Kim, W., Kim, S. H. and Surh, Y. J. (2020). Gremlin-1 augments the oestrogen-related receptor α signalling through EGFR activation: Implications for the progression of breast cancer. British Journal of Cancer, 123(6), 988–999. doi: 10.1038/s41416-020-0945-0 CrossRefGoogle ScholarPubMed
Pavani, K. C., Baron, E., Correia, P., Lourenço, J., Bettencourt, B. F., Sousa, M. and da Silva, F. M. (2016). Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock. Zygote, 24(5), 748–759. doi: 10.1017/S0967199416000071 CrossRefGoogle ScholarPubMed
Peng, X. R., Hsueh, A. J., LaPolt, P. S., Bjersing, L. and Ny, T. (1991). Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology, 129(6), 3200–3207. doi: 10.1210/endo-129-6-3200 CrossRefGoogle ScholarPubMed
Piras, A. R., Ariu, F., Falchi, L., Zedda, M. T., Pau, S., Schianchi, E., Paramio, M. T. and Bogliolo, L. (2020). Resveratrol treatment during maturation enhances developmental competence of oocytes after prolonged ovary storage at 4°C in the domestic cat model. Theriogenology, 144(144), 152–157. doi: 10.1016/j.theriogenology.2020.01.009 CrossRefGoogle ScholarPubMed
Reiter, R. J., Tan, D. X. and Korkmaz, A. (2009). The circadian melatonin rhythm and its modulation: Possible impact on hypertension. Journal of Hypertension. Supplement, 27(6), S17–S20. doi: 10.1097/01.hjh.0000358832.41181.bf CrossRefGoogle ScholarPubMed
Remião, M. H., Lucas, C. G., Domingues, W. B., Silveira, T., Barther, N. N., Komninou, E. R., Basso, A. C., Jornada, D. S., Beck, R. C., Pohlmann, A. R., Junior, A. S., Seixas, F. K., Campos, V. F., Guterres, S. S. and Collares, T. (2016). Melatonin delivery by nanocapsules during in vitro bovine oocyte maturation decreased the reactive oxygen species of oocytes and embryos. Reproductive Toxicology, 63, 70–81. doi: 10.1016/j.reprotox.2016.05.016 CrossRefGoogle ScholarPubMed
Richani, D. and Gilchrist, R. B. (2018). The epidermal growth factor network: Role in oocyte growth, maturation and developmental competence. Human Reproduction Update, 24(1), 1–14. doi: 10.1093/humupd/dmx029 CrossRefGoogle ScholarPubMed
Ríos, G. L., Buschiazzo, J., Mucci, N. C., Kaiser, G. G., Cesari, A. and Alberio, R. H. (2015). Combined epidermal growth factor and hyaluronic acid supplementation of in vitro maturation medium and its impact on bovine oocyte proteome and competence. Theriogenology, 83(5), 874–880. doi: 10.1016/j.theriogenology.2014.11.022 CrossRefGoogle ScholarPubMed
Rizos, D., Ward, F., Duffy, P., Boland, M. P. and 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. Molecular Reproduction and Development, 61(2), 234–248. doi: 10.1002/mrd.1153 CrossRefGoogle ScholarPubMed
Rodrigues-Cunha, M. C., Mesquita, L. G., Bressan, F., Collado, M. D., Balieiro, J. C., Schwarz, K. R., de Castro, F. C., Watanabe, O. Y., Watanabe, Y. F., de Alencar Coelho, L. and Leal, C. L. (2016). Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology, 86(7), 1685–1694. doi: 10.1016/j.theriogenology.2016.05.026 CrossRefGoogle ScholarPubMed
Rönnberg, L., Kauppila, A., Leppäluoto, J., Martikainen, H. and Vakkuri, O. (1990). Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. Journal of Clinical Endocrinology and Metabolism, 71(2), 492–496. doi: 10.1210/jcem-71-2-493 CrossRefGoogle ScholarPubMed
Sakatani, M., Yamanaka, K., Balboula, A. Z. and Takahashi, M. (2017). Different thermotolerances in in vitro-produced embryos derived from different maternal and paternal genetic backgrounds. Animal Science Journal, 88(12), 1934–1942. doi: 10.1111/asj.12875 CrossRefGoogle ScholarPubMed
Sampaio, R. V., Conceição, S., Miranda, M. S., Sampaio, Lde F. and Ohashi, O. M. (2012). MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro . Reproductive Biology and Endocrinology: RB&E, 10, 103. doi: 10.1186/1477-7827-10-103 CrossRefGoogle ScholarPubMed
Schultz, R. M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Human Reproduction Update, 8(4), 323–331. doi: 10.1093/humupd/8.4.323 CrossRefGoogle ScholarPubMed
Shabankareh, H. K. and Zandi, M. (2010). Developmental potential of sheep oocytes cultured in different maturation media: Effects of epidermal growth factor, insulin-like growth factor I, and cysteamine. Fertility and Sterility, 94(1), 335–340. doi: 10.1016/j.fertnstert.2009.01.160 CrossRefGoogle ScholarPubMed
Shi, J. M., Tian, X. Z., Zhou, G. B., Wang, L., Gao, C., Zhu, S. E., Zeng, S. M., Tian, J. H. and Liu, G. S. (2009). Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. Journal of Pineal Research, 47(4), 318–323. doi: 10.1111/j.1600-079X.2009.00717.x CrossRefGoogle ScholarPubMed
Singhal, S., Prasad, S., Singh, B., Prasad, J. K. and Gupta, H. P. (2009). Effect of including growth factors and antioxidants in maturation medium used for in vitro culture of buffalo oocytes recovered in vivo . Animal Reproduction Science, 113(1–4), 44–50. doi: 10.1016/j.anireprosci.2008.05.078 CrossRefGoogle ScholarPubMed
Sirisathien, S., Hernandez-Fonseca, H. J. and Brackett, B. G. (2003). Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro . Animal Reproduction Science, 77(1–2), 21–32. doi: 10.1016/s0378-4320(02)00272-5 CrossRefGoogle ScholarPubMed
Sovernigo, T. C., Adona, P. R., Monzani, P. S., Guemra, S., Barros, F., Lopes, F. G. and Leal, C. (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reproduction in Domestic Animals, 52(4), 561–569. doi: 10.1111/rda.12946 CrossRefGoogle ScholarPubMed
Sudo, S., Avsian-Kretchmer, O., Wang, L. S. and Hsueh, A. J. W. (2004). Protein related to DAN and Cerberus is a bone morphogenetic protein antagonist that participates in ovarian paracrine regulation. Journal of Biological Chemistry, 279(22), 23134–23141. doi: 10.1074/jbc.M402376200 CrossRefGoogle ScholarPubMed
Surani, M. A. and Barton, S. C. (1983). Development of gynogenetic eggs in the mouse: Implications for parthenogenetic embryos. Science, 222(4627), 1034–1036. doi: 10.1126/science.6648518 CrossRefGoogle ScholarPubMed
Takada, L., Junior, A. M., Mingoti, G. Z., Balieiro, J. C., Cipolla-Neto, J. and Coelho, L. A. (2012). Effect of melatonin on DNA damage of bovine cumulus cells during in vitro maturation (IVM) and on in vitro embryo development. Research in Veterinary Science, 92(1), 124–127. doi: 10.1016/j.rvsc.2010.11.004 CrossRefGoogle ScholarPubMed
Tamura, H., Nakamura, Y., Korkmaz, A., Manchester, L. C., Tan, D. X., Sugino, N. and Reiter, R. J. (2009). Melatonin and the ovary: Physiological and pathophysiological implications. Fertility and Sterility, 92(1), 328–343. doi: 10.1016/j.fertnstert.2008.05.016 CrossRefGoogle ScholarPubMed
Tao, Y., Zhou, B., Xia, G., Wang, F., Wu, Z. and Fu, M. (2004). Exposure to L-ascorbic acid or alpha-tocopherol facilitates the development of porcine denuded oocytes from metaphase I to metaphase II and prevents cumulus cells from fragmentation. Reproduction in Domestic Animals, 39(1), 52–57. doi: 10.1046/j.1439-0531.2003.00478.x CrossRefGoogle ScholarPubMed
Tesfaye, D., Ghanem, N., Carter, F., Fair, T., Sirard, M. A., Hoelker, M., Schellander, K. and Lonergan, P. (2009). Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro . Reproduction, Fertility, and Development, 21(3), 451–461. doi: 10.1071/rd08190 CrossRefGoogle ScholarPubMed
Tirone, E., D’Alessandris, C., Hascall, V. C., Siracusa, G. and Salustri, A. (1997). Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor beta1). Journal of Biological Chemistry, 272(8), 4787–4794. doi: 10.1074/jbc.272.8.4787 CrossRefGoogle Scholar
Torres, V., Muñoz, L., Urrego, R., Echeverry, J. J. and Lopez, A. (2016). 181 resveratrol during in vitro maturation improves the quality of bovine oocyte and enhances embryonic development in vitro . Reproduction, Fertility and Development, 29(1), 199. doi: 10.1071/RDv29n1Ab181 CrossRefGoogle Scholar
Uyar, A., Torrealday, S. and Seli, E. (2013). Cumulus and granulosa cell markers of oocyte and embryo quality. Fertility and Sterility, 99(4), 979–997. doi: 10.1016/j.fertnstert.2013.01.129 CrossRefGoogle ScholarPubMed
Vandaele, L., Mateusen, B., Maes, D., de Kruif, A. and Van Soom, A. (2006). Is apoptosis in bovine in vitro produced embryos related to early developmental kinetics and in vivo bull fertility? Theriogenology, 65(9), 1691–1703. doi: 10.1016/j.theriogenology.2005.09.014 CrossRefGoogle ScholarPubMed
Wang, F., Tian, X., Zhang, L., He, C., Ji, P., Li, Y., Tan, D. and Liu, G. (2014). Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertility and Sterility, 101(2), 577–586. doi: 10.1016/j.fertnstert.2013.10.041 CrossRefGoogle ScholarPubMed
Warzych, E., Peippo, J., Szydlowski, M. and Lechniak, D. (2007). Supplements to in vitro maturation media affect the production of bovine blastocysts and their apoptotic index but not the proportions of matured and apoptotic oocytes. Animal Reproduction Science, 97(3–4), 334–343. doi: 10.1016/j.anireprosci.2006.01.011 CrossRefGoogle Scholar
Watson, A. J., De Sousa, P., Caveney, A., Barcroft, L. C., Natale, D., Urquhart, J. and Westhusin, M. E. (2000). Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number, and apoptosis. Biology of Reproduction, 62(2), 355–364. doi: 10.1095/biolreprod62.2.355 CrossRefGoogle ScholarPubMed
Zhang, K., Hansen, P. J. and Ealy, A. D. (2010). Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro . Reproduction, 140(6), 815–826. doi: 10.1530/REP-10-0190 CrossRefGoogle ScholarPubMed
Zhao, X. M., Min, J. T., Du, W. H., Hao, H. S., Liu, Y., Qin, T., Wang, D. and Zhu, H. B. (2015). Melatonin enhances the in vitro maturation and developmental potential of bovine oocytes denuded of the cumulus oophorus. Zygote, 23(4), 525–536. doi: 10.1017/S0967199414000161 CrossRefGoogle ScholarPubMed