Relative transcript level of BMP15, BAX and CASP3 with qRT-PCR in vitrified equine immature cumulus-oocytes complexes
DOI:
https://doi.org/10.5433/1679-0359.2022v43n3p927Keywords:
Bcl-2-associated X protein, Bone morphogenetic protein 15, Gene expression, Caspase 3, Horse.Abstract
Research focused on female gamete vitrification has increased attention to develop a reliable cryopreservation method to preserve immature equine oocytes. Despite the intensive implementation of biotechnological procedures for horse breeding, vitrification of immature equine cumulus-oocyte complexes (COCs) remain to be clearly elucidated. We aimed to determine the relative transcript level of target genes Bone morphogenetic protein 15 (BMP15); Bcl-2-associated X protein (BAX); and Caspase 3 (CASP3) in equine COCs prior to and after vitrification. Ovarian follicles were aspirated from ovaries collected from an abattoir. A total of 240 COCs were collected and distributed into vitrified COCs (VIT, n=120) and non-vitrified (Non-VIT, n=120) groups. Then, COCs were preserved and relative transcript expressions of BMP15, BAX, CASP3 were measured and normalized against GAPDH performed by qRT-PCR. In addition, 38 COCs were evaluated to assess chromatin configuration of germinal vesicle stage prior and after vitrification by exposure to 10 ug/ml of bisbenzimide. A difference was observed in the COCs mRNA level of abundance for the BAX gene between the VIT (2.05 ± 0.47) and (0.85 ± 0.08) Non-VIT groups. There was no difference in mRNA relative transcript level of CASP3 and BMP15 in Non-VIT (0.63 ± 0.20 and 1.55 ± 0.73, respectively) compared to VIT (0.64 ± 0.01 and 2.84 ± 2.20, respectively) equine COCs. All COCs where considered at immature stage of development even though COCs in Non-VIT group showed higher condensed chromatin configuration compared to VIT (100% vs 60.7%, respectively). We demonstrate that BMP15 and CASP3 are detected in VIT and Non-VIT immature COCs. In conclusion, BAX is expressed highly in vitrified immature equine COCs and indicates that activation of apoptosis signaling cascades in cells exposed to vitrification.Downloads
Download data is not yet available.
References
Aman, R., & Parker, J. (1994). Effects of cooling and rewarming on meiotic spindle and chromosome of in vitro matured bovine oocytes. Biology of Reproduction, 50(1), 103-110. doi: 10.1095/biolreprod50.1.103
Anchamparuthy, V., Pearson, R., & Gwazdauskas, C. (2010). Expression pattern of apoptotic genes in vitrified-thawed bovine oocytes. Reproduction in Domestic Animals, 45(5), e83-90. doi: 10.1111/j.1439-0531.2009.01527.x
Araújo-Lemos, P. F. B., Freitas, L. M., Neto, Moura, M. T., Melo, J. V., Lima, P. F., & Oliveira, M. A. L. (2015). Comparison of vitrification and conventional freezing for cryopreservation of caprine embryos. Zygote, 23(4), 594-602. doi: 10.1017/S0967199414000215
Boumela, I., Assou, S., Aouacheria, A., Haouzi, D., Dechaud, H., De Vos, J.,... Hamamah, S. (2011). Involvement of BCL2 family members in the regulation of human oocyte and early embryo survival and death: gene expression and beyond. Reproduction, 141(5), 549-561. doi: 10.1530/REP-10-0504
Campos-Chillon, F., Farmerie, T., Bouma, G., Clay, C., & Carnevale, E. (2015). Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reproduction Fertility and Development, 27(6), 925-933. doi: 10.1071/RD14472
Canesin, H., Brom-de-Luna, J., Choi, Y., Pereira, A., Macedo, G., & Hinrichs, K. (2018). Vitrification of germinal-vesicle stage equine oocytes: effect of cryoprotectant exposure time on in vitro embryo production. Cryobiology, 81, 185-191. doi: 10.1016/j.cryobiol.2018.01.001
Canesin, H., Ortiz, I., Brom-De-Luna, J., Choi, Y., Ortiz, I., Diaw, M., & Hinrichs, K. (2017). Blastocyst development after intracytoplasmic sperm injection of equine oocytes vitrified at the germinal-vesicle stage. Cryobiology, 75, 52-59. doi: 10.1016/j.cryobiol.2017.02.004
Choi, Y., & Hinrichs, K. (2017). Vitrification of in vitro-produced and in vivo-recovered equine blastocysts in a clinical program. Theriogenology, 87, 48-54. doi: 10.1016/j.theriogenology.2016.08.005
Claes, A., Galli, C., Colleoni, S., Necchi, D., Lazzari, G., Deelen, C.,… Stout, T. (2016). Factors influencing oocyte recovery and in-vitro production of equine embryos in a commercial OPU/ICSI program. Journal of Equine Veterinary Science, 41, 68-69. doi: 10.1016/J.JEVS.2016.04.055
Cox, L., Vanderwall, D., Parkinson, K., Sweat, A., & Isom, S. (2015). Expression profiles of select genes in cumulus-oocyte complexes from young and aged mares. Reproduction Fertility and Development, 27(6), 914-924. doi: 10.1071/RD14446
Curcio, B., Gastal, M., Pereira, G., Corcini, C., Landim-Alvarenga, F., Barros, S.,... Gastal, E. (2014). Ultrastructural morphology and nuclear maturation rates of immature equine oocytes vitrified with different solutions and exposure times. Journal of Equine Veterinary Science, 34(5), 632-640. doi: 10.10 16/j.jevs.2013.12.002
De Bem, T., Adona, P., Bressan, F., Mesquita, L., Chiaratti, M., Meirelles, F., & Leal, C. (2014). The influence of morphology, follicle size and Bcl-2 and Bax transcripts on the developmental competence of bovine oocytes. Reproduction in Domestic Animals, 49(4), 576-583. doi: 10.1111/rda.12325
De Coster, T., Velez, D. A., Van Soom, A., Woelders, H., & Smits, K. (2020). Cryopreservation of equine oocytes: looking into the crystal ball. Reproduction Fertility and Development, 32(5), 453-467. doi: 10. 1071/RD19229
Ducheyne, K. D., Rizzo, M., Daels, P. F., Stout, T. A. E., & de Ruijter-Villani, M. (2019). Vitrifying immature equine oocytes impairs their ability to correctly align the chromosomes on the MII spindle. Reproduction Fertility and Development, 31(8), 1330-1338. doi: 10.1071/RD18276
Ebrahimi, B., Valojerdi, M., Eftekhari-Yazdi, P., Baharvand, H., & Farrokhi, A. (2010). IVM and gene expression of sheep cumulus-oocyte complexes following different methods of vitrification. Reproductive BioMedicine Online, 20(1), 26-34. doi: 10.1016/j.rbmo.2009.10.020
Eldridge-Panuska, W., Caracciolo di Brienza, V., Seidel, G., Squires, E., & Carnevale, E. (2005). Establishment of pregnancies after serial dilution or direct transfer by vitrified equine embryos. Theriogenology, 63(5), 1308-1319. doi: 10.1016/j.theriogenology.2004.06.015
Galli, C., Colleoni, S., Duchi, R., Lagutina, I., & Lazzari, G. (2013). Equine assisted reproduction and embryo technologies. Animal Reproduction, 10(3), 334-343. Retrieved from https://www.animal-reproduction. org/article/5b5a604cf7783717068b46a1/pdf/animreprod-10-3-334.pdf
Galloway, S., McNatty, K., Cambridge, L., Laitinen, M., Juengel, J., Jokiranta, T.,… Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP-15) cause increased ovulation rate and infertility in a dosage sensitive manner. Nature Genetics, 25(3), 279-283. doi: 10.1038/77033
Hinrichs, K. (2018). Assisted reproductive techniques in mares. Reproduction in Domestic Animals, 53(2), 4-13. doi: 10.1111/rda.13259
Hinrichs, K., & Schmidt, A. (2000). Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biology of Reproduction, 62(5), 1402-1408. doi: 10.1095/biolreprod62.5.1402
Hinrichs, K., Choi, Y., Love, L., Varner, D., Love, C., & Walckenaer, B. (2005). Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence. Biology of Reproduction, 72(5), 1142-1150. doi: 10.1095/biolreprod.104.03 6012
Hinrichs, K., Schmidt, A., Friedman, P., Selgarth, J., & Martin, M. (1993). In vitro maturation of horse oocytes: characterization of chromatin configuration using fluorescence microscopy. Biology of Reproduction, 48(2), 363-370. doi: 10.1095/biolreprod48.2.363
Hurtt, A., Landim-Alvarenga, F., Seidel, G., & Squires, E. (2000). Vitrification of immature and mature equine and bovine oocytes in an ethylene glycol, ficoll and sucrose solution using open-pulled straws. Theriogenology, 54(1), 119-128. doi: 10.1016/S0093-691X(00)00330-7
Hussein, T., Froiland, D., Amato, F., Thompson, J., & Gilchrist, R. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. Journal of Cell Science, 118(22), 5257-5268. doi: 10.1242/jcs.02644
Jang, W., Lee, S., Choi, H., Lim, J., Heo, Y., Cui, X., & Kim, N. (2014). Vitrification of immature mouse oocytes by the modified-cut standard straw method. Cell Biology International, 38(2), 164-171. doi: 10. 1002/cbin.10163
Kim, M., & Tilly, J. (2004). Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim Biophys Acta, 1644(2-3), 205-220. doi: 10.1016/j.bbamcr.2003.10. 012
Knight, P., & Glister, C. (2003). Local roles of TGF-b superfamily members in the control of ovarian follicle development. Animal Reproduction Science, 78(3-4), 165-183. doi: 10.1016/S0378-4320(03)00089-7
Lan, Z., Gu, P., Xu, X., Jackson, K., Demayo, F., O’Malley, B., & Cooney, A. (2003). GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO Journal, 22(1), 4070-4081. doi: 10.1093/emboj/cdg405
Leibo, S. P. (2008). Cryopreservation of oocytes and embryos: optimization by theoretical versus empirical analysis. Theriogenology, 69(1), 37-47. doi: 10.1016/j.theriogenology.2007.10.006
Leon, P., Campos, V., Kaefer, C., Begnini, K., McBride, A., Dellagostin, O.,… Collares, T. (2013). Expression of apoptotic genes in immature and in vitro matured equine oocytes and cumulus cells. Zygote, 21(3), 279-285. doi: 10.1017/S0967199411000554
Li, Y., Li, R., Ou, S., Zhang, N., Ren, L., Wei, L.,… Yang, D. (2014). Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reproduction Biology and Endocrinology, 12, 81. doi: 10.1186/1477-7827-12-81
Lin, J., Chen, F., Sun, M., Zhu, J., Li, Y., Pan, L.,… Tan, J. (2016). The relationship between apoptosis, chromatin configuration, histone modification and competence of oocytes: a study using the mouse ovary-holding stress model. Scientific Reports, 6, 28347. doi: 10.1038/srep28347
Livak, K., & Schmittgen, T. (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
Machado, M. F., Caixeta, E. S., Sudiman, J., Gilchrist, R. B., Thompson, J. G., Lima, P. F.,… 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
Maclellan, L., Carnevale, E., Coutinho Silva, M., Scoggin, C., Bruemmer, J., & Squires, E. (2002). Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology, 58(5), 911-919. doi: 10.1016/S0093-691X(02)00920-2
Martino, N., Dell'Aquila, M., Filioli Uranio, M., Rutigliano, L., Nicassio, M., Lacalandra, G., & Hinrichs, K. (2014). Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reproductive Biology and Endocrinology, 12, 99. doi: 10.1186/1477-7827-12-99
Nowak, A., Kochan, J., Papis, K., & Okólski, A. (2014). Studies on survival of horse oocytes after rapid-I method vitrification. Journal of Equine Veterinary Science, 34(5), 675-679. doi: 10.1016/j.jevs.2013.1 2.013
Oltvai, Z., Milliman, C., & Korsmeyer, S. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74(4), 609-619. doi: 10.1016/0092-8674(93)90509-O
Opiela, J., Katska-Ksiazkiewicz, L., Lipinski, D., Slomski, R., Bzowska, M., & Rynska, B. (2008). Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis- related genes Bcl-2 and Bax, and developmental competence following IVP in cattle. Theriogenology, 69(5), 546-555. doi: 10.1016/j.theriogenology.2007.11.001
Ortiz-Escribano, N., Pascottini, O. B., Woelders, H., Vandenberghe, L., De Schauwer, C., Govaere, J.,… Smits, K. (2018). An improved vitrification protocol for equine immature oocytes, resulting in a first live foal. Equine Veterinary Journal, 50(3), 391-397. doi: 10.1111/evj.12747
Otsuka, F., & Shimasaki, S. (2002). A novel function of Bone Morphogenetic Protein-15 in the pituitary: selective synthesis and secretion of FSH by gonadotropes. Endocrinology, 143(12), 4938-4941. doi: 10. 1210/en.2002-220929
Purohit, G., Meena, H., & Solanki, K. (2012). Effects of vitrification on immature and in vitro matured, denuded and cumulus compact goat oocytes and their subsequent fertilization. Journal Reproduction and Infertility, 13(1), 53-59. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3719371/
Rao, B., Mahesh, Y., Charan, K., Suman, K., Sekhar, N., & Shivaji, S. (2012). Effect of vitrification on meiotic maturation and expression of genes in immature goat cumulus oocyte complexes. Cryobiology, 64(3), 176-84. doi: 10.1016/j.cryobiol.2012.01.005
Rodrigues, B., Silveira, J., Bruemmer, J., Bouma, G., Carnevale, E., & Clay, C. (2010). Caspase 3 expression in equine granulosa cells and oocytes in young and old mares. Biology of Reproduction, 83(1), 694. doi: 10.1093/biolreprod/83.s1.694
Sanfins, A., Rodrigues, P., & Albertini, D. (2018). GDF-9 and BMP-15 direct the follicle symphony. Journal of Assisted Reproduction and Genetics, 35(1), 1741-1750. doi: 10.1007/s10815-018-1268-4
Smits, K., Hoogewijs, M., Woelders, H., Daels, P., & Van Soom, A. (2012). Breeding or assisted reproduction? Relevance of the horse model applied to the conservation of endangered equids. Reproduction in Domestic Animals, 47(4), 239-48. doi: 10.1111/j.1439-0531.2012.02082.x
Somfai, T., Nguyen, H. T., Nguyen, M. T., Dang-Nguyen, T. Q., Kaneko, H., Noguchi, J., & Kikuchi, K. (2020). Vitrification of porcine cumulus-oocyte complexes at the germinal vesicle stage does not trigger apoptosis in oocytes and early embryos, but activates anti-apoptotic Bcl-XL gene expression beyond the 4-cell stage. Journal of Reproduction and Development, 66(2), 115-123. doi: 10.1262/jrd.2019-094
Stout, T. (2012). Cryopreservation of equine embryos: current state-of-the-art. Reproduction in Domestic Animals, 47(3), 84-89. doi: 10.1111/j.1439-0531.2012.02030.x
Tharasanit, T., Colleoni, S., Galli, C., Colenbrander, B., & Stout, T. (2009). Protective effects of the cumulus-corona radiata complex during vitrification of horse oocytes. Reproduction, 137(3), 391-401. doi: 10.153 0/REP-08-0333
Tharasanit, T., Colleoni, S., Lazzari, G., Colenbrander, B., Galli, C., & Stout, T. (2006). Effect of cumulus morphology and maturation stage on the cryopreservability of equine oocytes. Reproduction, 132(5), 759-769. doi: 10.1530/rep.1.01156
Vallorani, C., Spinaci, M., Bucci, D., Porcu, E., Tamanini, C., & Galeati, G. (2012). Pig oocyte vitrification by Cryotop method and the activation of the apoptotic cascade. Animal Reproduction Science, 135(1-4), 68-74. doi: 10.1016/j.anireprosci.2012.08.020
Wong, K. M., Mastenbroek, S., & Repping, S. (2014). Cryopreservation of human embryos and its contribution to in vitro fertilization success rates. Fertility and Sterility, 102(1), 19-26. doi: 10.1016/j.fertnstert.2014. 05.027
Yang, M., & Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Animal Reproduction Science, 70(3-4), 159-169. doi: 10.1016/ S0378-4320(01)00186-5
Zander-Fox, D., Lane, M., & Hamilton, H. (2013). Slow freezing and vitrification of mouse morula and early blastocysts. Journal of Assisted Reproduction and Genetics, 30(8), 1091-1098. doi: 10.1007/s10815-013-0056-4
Anchamparuthy, V., Pearson, R., & Gwazdauskas, C. (2010). Expression pattern of apoptotic genes in vitrified-thawed bovine oocytes. Reproduction in Domestic Animals, 45(5), e83-90. doi: 10.1111/j.1439-0531.2009.01527.x
Araújo-Lemos, P. F. B., Freitas, L. M., Neto, Moura, M. T., Melo, J. V., Lima, P. F., & Oliveira, M. A. L. (2015). Comparison of vitrification and conventional freezing for cryopreservation of caprine embryos. Zygote, 23(4), 594-602. doi: 10.1017/S0967199414000215
Boumela, I., Assou, S., Aouacheria, A., Haouzi, D., Dechaud, H., De Vos, J.,... Hamamah, S. (2011). Involvement of BCL2 family members in the regulation of human oocyte and early embryo survival and death: gene expression and beyond. Reproduction, 141(5), 549-561. doi: 10.1530/REP-10-0504
Campos-Chillon, F., Farmerie, T., Bouma, G., Clay, C., & Carnevale, E. (2015). Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reproduction Fertility and Development, 27(6), 925-933. doi: 10.1071/RD14472
Canesin, H., Brom-de-Luna, J., Choi, Y., Pereira, A., Macedo, G., & Hinrichs, K. (2018). Vitrification of germinal-vesicle stage equine oocytes: effect of cryoprotectant exposure time on in vitro embryo production. Cryobiology, 81, 185-191. doi: 10.1016/j.cryobiol.2018.01.001
Canesin, H., Ortiz, I., Brom-De-Luna, J., Choi, Y., Ortiz, I., Diaw, M., & Hinrichs, K. (2017). Blastocyst development after intracytoplasmic sperm injection of equine oocytes vitrified at the germinal-vesicle stage. Cryobiology, 75, 52-59. doi: 10.1016/j.cryobiol.2017.02.004
Choi, Y., & Hinrichs, K. (2017). Vitrification of in vitro-produced and in vivo-recovered equine blastocysts in a clinical program. Theriogenology, 87, 48-54. doi: 10.1016/j.theriogenology.2016.08.005
Claes, A., Galli, C., Colleoni, S., Necchi, D., Lazzari, G., Deelen, C.,… Stout, T. (2016). Factors influencing oocyte recovery and in-vitro production of equine embryos in a commercial OPU/ICSI program. Journal of Equine Veterinary Science, 41, 68-69. doi: 10.1016/J.JEVS.2016.04.055
Cox, L., Vanderwall, D., Parkinson, K., Sweat, A., & Isom, S. (2015). Expression profiles of select genes in cumulus-oocyte complexes from young and aged mares. Reproduction Fertility and Development, 27(6), 914-924. doi: 10.1071/RD14446
Curcio, B., Gastal, M., Pereira, G., Corcini, C., Landim-Alvarenga, F., Barros, S.,... Gastal, E. (2014). Ultrastructural morphology and nuclear maturation rates of immature equine oocytes vitrified with different solutions and exposure times. Journal of Equine Veterinary Science, 34(5), 632-640. doi: 10.10 16/j.jevs.2013.12.002
De Bem, T., Adona, P., Bressan, F., Mesquita, L., Chiaratti, M., Meirelles, F., & Leal, C. (2014). The influence of morphology, follicle size and Bcl-2 and Bax transcripts on the developmental competence of bovine oocytes. Reproduction in Domestic Animals, 49(4), 576-583. doi: 10.1111/rda.12325
De Coster, T., Velez, D. A., Van Soom, A., Woelders, H., & Smits, K. (2020). Cryopreservation of equine oocytes: looking into the crystal ball. Reproduction Fertility and Development, 32(5), 453-467. doi: 10. 1071/RD19229
Ducheyne, K. D., Rizzo, M., Daels, P. F., Stout, T. A. E., & de Ruijter-Villani, M. (2019). Vitrifying immature equine oocytes impairs their ability to correctly align the chromosomes on the MII spindle. Reproduction Fertility and Development, 31(8), 1330-1338. doi: 10.1071/RD18276
Ebrahimi, B., Valojerdi, M., Eftekhari-Yazdi, P., Baharvand, H., & Farrokhi, A. (2010). IVM and gene expression of sheep cumulus-oocyte complexes following different methods of vitrification. Reproductive BioMedicine Online, 20(1), 26-34. doi: 10.1016/j.rbmo.2009.10.020
Eldridge-Panuska, W., Caracciolo di Brienza, V., Seidel, G., Squires, E., & Carnevale, E. (2005). Establishment of pregnancies after serial dilution or direct transfer by vitrified equine embryos. Theriogenology, 63(5), 1308-1319. doi: 10.1016/j.theriogenology.2004.06.015
Galli, C., Colleoni, S., Duchi, R., Lagutina, I., & Lazzari, G. (2013). Equine assisted reproduction and embryo technologies. Animal Reproduction, 10(3), 334-343. Retrieved from https://www.animal-reproduction. org/article/5b5a604cf7783717068b46a1/pdf/animreprod-10-3-334.pdf
Galloway, S., McNatty, K., Cambridge, L., Laitinen, M., Juengel, J., Jokiranta, T.,… Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP-15) cause increased ovulation rate and infertility in a dosage sensitive manner. Nature Genetics, 25(3), 279-283. doi: 10.1038/77033
Hinrichs, K. (2018). Assisted reproductive techniques in mares. Reproduction in Domestic Animals, 53(2), 4-13. doi: 10.1111/rda.13259
Hinrichs, K., & Schmidt, A. (2000). Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biology of Reproduction, 62(5), 1402-1408. doi: 10.1095/biolreprod62.5.1402
Hinrichs, K., Choi, Y., Love, L., Varner, D., Love, C., & Walckenaer, B. (2005). Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence. Biology of Reproduction, 72(5), 1142-1150. doi: 10.1095/biolreprod.104.03 6012
Hinrichs, K., Schmidt, A., Friedman, P., Selgarth, J., & Martin, M. (1993). In vitro maturation of horse oocytes: characterization of chromatin configuration using fluorescence microscopy. Biology of Reproduction, 48(2), 363-370. doi: 10.1095/biolreprod48.2.363
Hurtt, A., Landim-Alvarenga, F., Seidel, G., & Squires, E. (2000). Vitrification of immature and mature equine and bovine oocytes in an ethylene glycol, ficoll and sucrose solution using open-pulled straws. Theriogenology, 54(1), 119-128. doi: 10.1016/S0093-691X(00)00330-7
Hussein, T., Froiland, D., Amato, F., Thompson, J., & Gilchrist, R. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. Journal of Cell Science, 118(22), 5257-5268. doi: 10.1242/jcs.02644
Jang, W., Lee, S., Choi, H., Lim, J., Heo, Y., Cui, X., & Kim, N. (2014). Vitrification of immature mouse oocytes by the modified-cut standard straw method. Cell Biology International, 38(2), 164-171. doi: 10. 1002/cbin.10163
Kim, M., & Tilly, J. (2004). Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim Biophys Acta, 1644(2-3), 205-220. doi: 10.1016/j.bbamcr.2003.10. 012
Knight, P., & Glister, C. (2003). Local roles of TGF-b superfamily members in the control of ovarian follicle development. Animal Reproduction Science, 78(3-4), 165-183. doi: 10.1016/S0378-4320(03)00089-7
Lan, Z., Gu, P., Xu, X., Jackson, K., Demayo, F., O’Malley, B., & Cooney, A. (2003). GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO Journal, 22(1), 4070-4081. doi: 10.1093/emboj/cdg405
Leibo, S. P. (2008). Cryopreservation of oocytes and embryos: optimization by theoretical versus empirical analysis. Theriogenology, 69(1), 37-47. doi: 10.1016/j.theriogenology.2007.10.006
Leon, P., Campos, V., Kaefer, C., Begnini, K., McBride, A., Dellagostin, O.,… Collares, T. (2013). Expression of apoptotic genes in immature and in vitro matured equine oocytes and cumulus cells. Zygote, 21(3), 279-285. doi: 10.1017/S0967199411000554
Li, Y., Li, R., Ou, S., Zhang, N., Ren, L., Wei, L.,… Yang, D. (2014). Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reproduction Biology and Endocrinology, 12, 81. doi: 10.1186/1477-7827-12-81
Lin, J., Chen, F., Sun, M., Zhu, J., Li, Y., Pan, L.,… Tan, J. (2016). The relationship between apoptosis, chromatin configuration, histone modification and competence of oocytes: a study using the mouse ovary-holding stress model. Scientific Reports, 6, 28347. doi: 10.1038/srep28347
Livak, K., & Schmittgen, T. (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
Machado, M. F., Caixeta, E. S., Sudiman, J., Gilchrist, R. B., Thompson, J. G., Lima, P. F.,… 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
Maclellan, L., Carnevale, E., Coutinho Silva, M., Scoggin, C., Bruemmer, J., & Squires, E. (2002). Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology, 58(5), 911-919. doi: 10.1016/S0093-691X(02)00920-2
Martino, N., Dell'Aquila, M., Filioli Uranio, M., Rutigliano, L., Nicassio, M., Lacalandra, G., & Hinrichs, K. (2014). Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reproductive Biology and Endocrinology, 12, 99. doi: 10.1186/1477-7827-12-99
Nowak, A., Kochan, J., Papis, K., & Okólski, A. (2014). Studies on survival of horse oocytes after rapid-I method vitrification. Journal of Equine Veterinary Science, 34(5), 675-679. doi: 10.1016/j.jevs.2013.1 2.013
Oltvai, Z., Milliman, C., & Korsmeyer, S. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74(4), 609-619. doi: 10.1016/0092-8674(93)90509-O
Opiela, J., Katska-Ksiazkiewicz, L., Lipinski, D., Slomski, R., Bzowska, M., & Rynska, B. (2008). Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis- related genes Bcl-2 and Bax, and developmental competence following IVP in cattle. Theriogenology, 69(5), 546-555. doi: 10.1016/j.theriogenology.2007.11.001
Ortiz-Escribano, N., Pascottini, O. B., Woelders, H., Vandenberghe, L., De Schauwer, C., Govaere, J.,… Smits, K. (2018). An improved vitrification protocol for equine immature oocytes, resulting in a first live foal. Equine Veterinary Journal, 50(3), 391-397. doi: 10.1111/evj.12747
Otsuka, F., & Shimasaki, S. (2002). A novel function of Bone Morphogenetic Protein-15 in the pituitary: selective synthesis and secretion of FSH by gonadotropes. Endocrinology, 143(12), 4938-4941. doi: 10. 1210/en.2002-220929
Purohit, G., Meena, H., & Solanki, K. (2012). Effects of vitrification on immature and in vitro matured, denuded and cumulus compact goat oocytes and their subsequent fertilization. Journal Reproduction and Infertility, 13(1), 53-59. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3719371/
Rao, B., Mahesh, Y., Charan, K., Suman, K., Sekhar, N., & Shivaji, S. (2012). Effect of vitrification on meiotic maturation and expression of genes in immature goat cumulus oocyte complexes. Cryobiology, 64(3), 176-84. doi: 10.1016/j.cryobiol.2012.01.005
Rodrigues, B., Silveira, J., Bruemmer, J., Bouma, G., Carnevale, E., & Clay, C. (2010). Caspase 3 expression in equine granulosa cells and oocytes in young and old mares. Biology of Reproduction, 83(1), 694. doi: 10.1093/biolreprod/83.s1.694
Sanfins, A., Rodrigues, P., & Albertini, D. (2018). GDF-9 and BMP-15 direct the follicle symphony. Journal of Assisted Reproduction and Genetics, 35(1), 1741-1750. doi: 10.1007/s10815-018-1268-4
Smits, K., Hoogewijs, M., Woelders, H., Daels, P., & Van Soom, A. (2012). Breeding or assisted reproduction? Relevance of the horse model applied to the conservation of endangered equids. Reproduction in Domestic Animals, 47(4), 239-48. doi: 10.1111/j.1439-0531.2012.02082.x
Somfai, T., Nguyen, H. T., Nguyen, M. T., Dang-Nguyen, T. Q., Kaneko, H., Noguchi, J., & Kikuchi, K. (2020). Vitrification of porcine cumulus-oocyte complexes at the germinal vesicle stage does not trigger apoptosis in oocytes and early embryos, but activates anti-apoptotic Bcl-XL gene expression beyond the 4-cell stage. Journal of Reproduction and Development, 66(2), 115-123. doi: 10.1262/jrd.2019-094
Stout, T. (2012). Cryopreservation of equine embryos: current state-of-the-art. Reproduction in Domestic Animals, 47(3), 84-89. doi: 10.1111/j.1439-0531.2012.02030.x
Tharasanit, T., Colleoni, S., Galli, C., Colenbrander, B., & Stout, T. (2009). Protective effects of the cumulus-corona radiata complex during vitrification of horse oocytes. Reproduction, 137(3), 391-401. doi: 10.153 0/REP-08-0333
Tharasanit, T., Colleoni, S., Lazzari, G., Colenbrander, B., Galli, C., & Stout, T. (2006). Effect of cumulus morphology and maturation stage on the cryopreservability of equine oocytes. Reproduction, 132(5), 759-769. doi: 10.1530/rep.1.01156
Vallorani, C., Spinaci, M., Bucci, D., Porcu, E., Tamanini, C., & Galeati, G. (2012). Pig oocyte vitrification by Cryotop method and the activation of the apoptotic cascade. Animal Reproduction Science, 135(1-4), 68-74. doi: 10.1016/j.anireprosci.2012.08.020
Wong, K. M., Mastenbroek, S., & Repping, S. (2014). Cryopreservation of human embryos and its contribution to in vitro fertilization success rates. Fertility and Sterility, 102(1), 19-26. doi: 10.1016/j.fertnstert.2014. 05.027
Yang, M., & Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Animal Reproduction Science, 70(3-4), 159-169. doi: 10.1016/ S0378-4320(01)00186-5
Zander-Fox, D., Lane, M., & Hamilton, H. (2013). Slow freezing and vitrification of mouse morula and early blastocysts. Journal of Assisted Reproduction and Genetics, 30(8), 1091-1098. doi: 10.1007/s10815-013-0056-4
Downloads
Published
2022-02-28
How to Cite
Polenz, M. F., Pereira, G. R., Rissi, V. B., Bertolin, K., Gonçalves, P. B., Augusto, G. C., & Rechsteiner, S. M. F. (2022). Relative transcript level of BMP15, BAX and CASP3 with qRT-PCR in vitrified equine immature cumulus-oocytes complexes. Semina: Ciências Agrárias, 43(3), 927–942. https://doi.org/10.5433/1679-0359.2022v43n3p927
Issue
Section
Articles
License
Copyright (c) 2022 Semina: Ciências Agrárias
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.
