Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-05T21:08:04.632Z Has data issue: false hasContentIssue false

Selection of Rattus norvegicus cumulus–oocyte complex for vitrification by brilliant cresyl blue

Published online by Cambridge University Press:  14 July 2023

Iaskara Oliveira
Affiliation:
PPG – Ciências da Saúde − Universidade Federal de Ciências da Saúde de Porto Alegre –UFCSPA, Porto Alegre, RS, Brazil
Joana Fisch
Affiliation:
PPG – Ciências da Saúde − Universidade Federal de Ciências da Saúde de Porto Alegre –UFCSPA, Porto Alegre, RS, Brazil
Juliana Gomes
Affiliation:
Laboratório de Biotecnologia Animal Aplicada− Universidade Federal do Rio Grande do Sul−UFRGS, Porto Alegre, RS, Brazil
Rui Fernando Felix Lopes
Affiliation:
Laboratório de Biotecnologia Animal Aplicada− Universidade Federal do Rio Grande do Sul−UFRGS, Porto Alegre, RS, Brazil
Alexandre Tavares Duarte de Oliveira*
Affiliation:
PPG – Ciências da Saúde − Universidade Federal de Ciências da Saúde de Porto Alegre –UFCSPA, Porto Alegre, RS, Brazil Laboratório de Biotecnologia Animal Aplicada− Universidade Federal do Rio Grande do Sul−UFRGS, Porto Alegre, RS, Brazil
*
Corresponding author: Alexandre Tavares Duarte de Oliveira; Email: atdo@ufrgs.br

Summary

The influence of the method of evaluating developmentally competent oocytes on their viability after cryopreservation still needs to be better understood. The objective of this study was to determine the cleavage and embryo developmental rates after parthenogenetic activation of cumulus–oocyte complexes (COCs) selected by different concentrations of brilliant cresyl blue (BCB) and cryopreservation. In the first experiment, COCs were separated into groups and incubated for 1 h in medium containing BCB (13 μM, 16 μM, or 20 μM). The control group was not exposed to BCB staining. In the second experiment, COCs were divided into four groups: 13 μM BCB(+), 13 μM BCB(−), fresh control (selected by morphologic observation and immediately in vitro matured) and vitrified control (selected by morphologic evaluation, vitrified, and in vitro matured). In the first experiment, the 13 μM BCB group displayed greater development rates at the morula stage (65.45%, 36/55) when compared with the other groups. In the second experiment, cleavage (47.05%, 72/153) and morula development (33.55%, 51/153) of the control group of fresh COCs were increased compared with the other groups. However, when comparing morula rates between vitrified COC control and BCB(+) groups, the BCB(+) group had better results (19.23%, 5/26 and 64.7%, 11/17, respectively). Our best result in rat COC selection by BCB staining was obtained using a concentration of 13 μM. This selection could be a valuable tool to improve vitrification outcomes, as observed by the BCB(+) group that demonstrated better results compared with the vitrified COC control.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ailia, M. J., Jin, Y. K., Kim, H. K. and Jang, G. (2021). Development of in-vitro maturation protocol for rat oocytes; under simple culture vs co-culture with cumulus cell monolayer and its developmental potential via parthenogenetic/artificial activation. BMC Veterinary Research, 17(1), 44. doi: 10.1186/s12917-020-02714-8 CrossRefGoogle ScholarPubMed
Alcoba, D. D., da Rosa Braga, B. L., Sandi-Monroy, N. L., Proença, L. A., Felix Lopes, R. F. and de Oliveira, A. T. (2013). Selection of Rattus norvegicus oocytes for in vitro maturation by brilliant cresyl blue staining. Zygote, 21(3), 238245. doi: 10.1017/S0967199411000463 CrossRefGoogle ScholarPubMed
Alcoba, D. D., Conzatti, M., Ferreira, G. D., Pimentel, A. M., Kussler, A. P., Capp, E., von Eye Corleta, H. V. E. and Brum, I. S. (2016). Safety of brilliant cresyl blue staining protocols on human granulosa and cumulus cells. Zygote, 24(1), 8388. doi: 10.1017/S0967199415000052 CrossRefGoogle ScholarPubMed
Alcoba, D. D., Schneider, J., Arruda, L., Martiny, P. B., Capp, E., von Eye Corleta, H. V. E. and Brum, I. S. (2017). Brilliant cresyl blue staining does not present cytotoxic effects on human luteinized follicular cells, according to gene/protein expression, as well as to cytotoxicity tests. Reproductive Biology, 17(1), 6068. doi: 10.1016/j.repbio.2016.12.003 CrossRefGoogle Scholar
Alm, H., Torner, H., Löhrke, B., Viergutz, T., Ghoneim, I. M. and Kanitz, W. (2005). Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology, 63(8), 21942205. doi: 10.1016/j.theriogenology.2004.09.050 CrossRefGoogle ScholarPubMed
Ashry, M., Lee, K. B., Mondal, M., Datta, T. K., Folger, J. K., Rajput, S. K., Zhang, K., Hemeida, N. A. and Smith, G. W. (2015). Expression of TGFβ superfamily components and other markers of oocyte quality in oocytes selected by brilliant cresyl blue staining: Relevance to early embryonic development. Molecular Reproduction and Development, 82(3), 251264. doi: 10.1002/mrd.22468 CrossRefGoogle ScholarPubMed
Brambillasca, F., Guglielmo, M. C., Coticchio, G., Mignini Renzini, M. M., Dal Canto, M. and Fadini, R. (2013). The current challenges to efficient immature oocyte cryopreservation. Journal of Assisted Reproduction and Genetics, 30(12), 15311539. doi: 10.1007/s10815-013-0112-0 CrossRefGoogle ScholarPubMed
Catalá, M. G., Izquierdo, D., Uzbekova, S., Morató, R., Roura, M., Romaguera, R., Papillier, P. and Paramio, M. T. (2011). Brilliant cresyl blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction, 142(4), 517527. doi: 10.1530/REP-10-0528 CrossRefGoogle ScholarPubMed
Díez, C., Muñoz, M., Caamaño, J. N. and Gómez, E. (2012). Cryopreservation of the bovine oocyte: Current status and perspectives. Reproduction in Domestic Animals, 47 Suppl. 3, 7683. doi: 10.1111/j.1439-0531.2012.02029.x CrossRefGoogle Scholar
Fathi, M., Ashry, M., Salama, A. and Badr, M. R. (2017). Developmental competence of Dromedary camel (Camelus dromedarius) oocytes selected using brilliant cresyl blue staining. Zygote, 25(4), 529536. doi: 10.1017/S0967199417000387 CrossRefGoogle ScholarPubMed
Fujiwara, K., Kamoshita, M., Kato, T., Ito, J. and Kashiwazaki, N. (2017). Generation of rats from vitrified oocytes with surrounding cumulus cells via in vitro fertilization with cryopreserved sperm. Animal Science Journal, 88(1), 180184. doi: 10.1111/asj.12666 CrossRefGoogle ScholarPubMed
Galat, V., Zhou, Y., Taborn, G., Garton, R. and Iannaccone, P. (2007). Overcoming MIII arrest from spontaneous activation in cultured rat oocytes. Cloning and Stem Cells, 9(3), 303314. doi: 10.1089/clo.2006.0059 CrossRefGoogle ScholarPubMed
Gandolfi, F., Brevini, T. A. L., Luciano, A. M., Modina, S., Passoni, L. and Pocar, P. (1995). In vitro development of preimplantation embryos from domestic species. Toxicology in Vitro, 9(5), 607613. doi: 10.1016/0887-2333(95)00073-h CrossRefGoogle ScholarPubMed
Ghanem, N., Hölker, M., Rings, F., Jennen, D., Tholen, E., Sirard, M. A., Torner, H., Kanitz, W., Schellander, K. and Tesfaye, D. (2007). Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Developmental Biology, 7, 90. doi: 10.1186/1471-213X-7-90 CrossRefGoogle ScholarPubMed
Hadi, H., Wahid, H., Rosnina, Y., Daliri, M., Dashtizad, M., Karamishab, H., Faizah, A., Iswadi, M. I. and Mazni, O. A. (2010). Selection of immature bovine oocytes using brilliant cresyl blue enhances nuclear maturity after vitrification. Journal of Animal and Veterinary Advances, 9(21), 27102713. doi: 10.3923/javaa.2010.2710.2713 Google Scholar
Hayes, E., Galea, S., Verkuylen, A., Pera, M., Morrison, J., Lacham-Kaplan, O. and Trounson, A. (2001). Nuclear transfer of adult and genetically modified fetal cells of the rat. Physiological Genomics, 5(4), 193204. doi: 10.1152/physiolgenomics.2001.5.4.193 CrossRefGoogle ScholarPubMed
Kempisty, B., Jackowska, M., Piotrowska, H., Antosik, P., Woźna, M., Bukowska, D., Brüssow, K. P. and Jaśkowski, J. M. (2011). Zona pellucida glycoprotein 3 (pZP3) and integrin β2 (ITGB2) mRNA and protein expression in porcine oocytes after single and double exposure to brilliant cresyl blue test. Theriogenology, 75(8), 15251535. doi: 10.1016/j.theriogenology.2010.12.016 CrossRefGoogle ScholarPubMed
Kim, S. S., Olsen, R., Kim, D. D. and Albertini, D. F. (2014). The impact of vitrification on immature oocyte cell cycle and cytoskeletal integrity in a rat model. Journal of Assisted Reproduction and Genetics, 31(6), 739747. doi: 10.1007/s10815-014-0216-1 CrossRefGoogle ScholarPubMed
Krivokharchenko, A., Popova, E., Zaitseva, I., Vil’ianovich, L., Ganten, D. and Bader, M. (2003). Development of parthenogenetic rat embryos. Biology of Reproduction, 68(3), 829836. doi: 10.1095/biolreprod.102.006494 CrossRefGoogle ScholarPubMed
Lopes, E. F., Marques, L. S., Duranti, R. G., de Oliveira, A. T. D., Lopes, R. F. F. and Rodrigues, J. L. (2015). Gene expression of monocarboxylate transporters and oocyte-secreted factors in bovine cumulus–oocyte complexes selected by brilliant cresyl blue. Reproduction in Domestic Animals, 50(5), 763770. doi: 10.1111/rda.12585 CrossRefGoogle ScholarPubMed
Mirshamsi, S. M., KaramiShabankareh, H., Ahmadi-Hamedani, M., Soltani, L., Hajarian, H. and Abdolmohammadi, A. R. (2013). Combination of oocyte and zygote selection by brilliant cresyl blue (BCB) test enhanced prediction of developmental potential to the blastocyst in cattle. Animal Reproduction Science, 136(4), 245251. doi: 10.1016/j.anireprosci.2012.11.002 CrossRefGoogle Scholar
Miyoshi, K., Abeydeera, L. R., Okuda, K. and Niwa, K. (1995). Effects of osmolarity and amino acids in a chemically defined medium on development of rat one-cell embryos. Journal of Reproduction and Fertility, 103(1), 2732. doi: 10.1530/jrf.0.1030027 CrossRefGoogle Scholar
Mizutani, E., Jiang, J. Y., Mizuno, S., Tomioka, I., Shinozawa, T., Kobayashi, J., Sasada, H. and Sato, E. (2004). Determination of optimal conditions for parthenogenetic activation and subsequent development of rat oocytes in vitro . Journal of Reproduction and Development, 50(1), 139146. doi: 10.1262/jrd.50.139 CrossRefGoogle ScholarPubMed
Opiela, J. and Kątska-Książkiewicz, L. (2013). The utility of brilliant cresyl blue (BCB) staining of mammalian oocytes used for in vitro embryo production (IVP). Reproductive Biology, 13(3), 177183. doi: 10.1016/j.repbio.2013.07.004 CrossRefGoogle ScholarPubMed
Opiela, J., Lipiński, D., Słomski, R. and Kątska-Książkiewicz, L. (2010). Transcript expression of mitochondria related genes is correlated with bovine oocyte selection by BCB test. Animal Reproduction Science, 118(2–4), 188193. doi: 10.1016/j.anireprosci.2009.07.007 CrossRefGoogle Scholar
Paim, L. M. G., Gal, L. L., Lopes, R. F. F. and Oliveira, A. T. D. (2015). Vitrification of Rattus norvegicus immature cumulus–oocyte complexes using hyaluronic acid. In Vitro Cellular and Developmental Biology. Animal, 51(10), 9951002. doi: 10.1007/s11626-015-9940-9 CrossRefGoogle ScholarPubMed
Pornwiroon, S., Kunathikom, S., Makemaharn, O. and Huanaraj, R. (2006). Vitrification of mouse oocyte using open pulled straws compared with needles. Journal of the Medical Association of Thailand, 89(12), 20152020.Google ScholarPubMed
Quinn, P., Barros, C. and Whittingham, D. G. (1982). Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. Journal of Reproduction and Fertility, 66(1), 161168. doi: 10.1530/jrf.0.0660161 CrossRefGoogle ScholarPubMed
Rienzi, L., Balaban, B., Ebner, T. and Mandelbaum, J. (2012). The oocyte. Human Reproduction, 27 Suppl. 1, i2i21. doi: 10.1093/humrep/des200 CrossRefGoogle Scholar
Santos, E. C., Sato, D., Lucia, T. Jr. and Iwata, H. (2015). Brilliant cresyl blue staining negatively affects mitochondrial functions in porcine oocytes. Zygote, 23(3), 352359. doi: 10.1017/S0967199413000610 CrossRefGoogle ScholarPubMed
Santos, E. C., Pradieé, J., Madeira, E. M., Pereira, M. M., Mion, B., Mondadori, R. G., Vieira, A. D., Pegoraro, L. M. C. and Lucia, T., Jr. (2017). Selection of porcine oocytes in vitro through brilliant cresyl blue staining in distinct incubation media. Zygote, 25(1), 4955. doi: 10.1017/S0967199416000319 CrossRefGoogle ScholarPubMed
Shinozawa, T., Mizutani, E., Tomioka, I., Kawahara, M., Sasada, H., Matsumoto, H. and Sato, E. (2004). Differential effect of recipient cytoplasm for microtubule organization and preimplantation development in rat reconstituted embryos with two-cell embryonic cell nuclear transfer. Molecular Reproduction and Development, 68(3), 313318. doi: 10.1002/mrd.20083 CrossRefGoogle ScholarPubMed
Silva, D. S., Rodriguez, P., Galuppo, A., Arruda, N. S. and Rodrigues, J. L. (2013). Selection of bovine oocytes by brilliant cresyl blue staining: Effect on meiosis progression, organelle distribution and embryo development. Zygote, 21(3), 250255. doi: 10.1017/S0967199411000487 CrossRefGoogle ScholarPubMed
Su, J., Wang, Y., Li, R., Peng, H., Hua, S., Li, Q., Quan, F., Guo, Z. and Zhang, Y. (2012). Oocytes selected using BCB staining enhance nuclear reprogramming and the in vivo development of SCNT embryos in cattle. PLOS ONE, 7(4), e36181. doi: 10.1371/journal.pone.0036181 CrossRefGoogle ScholarPubMed
Tabandeh, M. R., Golestani, N., Kafi, M., Hosseini, A., Saeb, M. and Sarkoohi, P. (2012). Gene expression pattern of adiponectin and adiponectin receptors in dominant and atretic follicles and oocytes screened based on brilliant cresyl blue staining. Animal Reproduction Science, 131(1–2), 3040. doi: 10.1016/j.anireprosci.2012.02.006 CrossRefGoogle ScholarPubMed
Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M. and de Kruif, A. (2002). Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Molecular Reproduction and Development, 61(3), 414424. doi: 10.1002/mrd.10102 CrossRefGoogle ScholarPubMed
Taketsuru, H. and Kaneko, T. (2016). In vitro maturation of immature rat oocytes under simple culture conditions and subsequent developmental ability. Journal of Reproduction and Development, 62(5), 521526. doi: 10.1262/jrd.2016-057 CrossRefGoogle ScholarPubMed
Torner, H., Ghanem, N., Ambros, C., Hölker, M., Tomek, W., Phatsara, C., Alm, H., Sirard, M. A., Kanitz, W., Schellander, K. and Tesfaye, D. (2008). Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction, 135(2), 197212. doi: 10.1530/REP-07-0348 CrossRefGoogle ScholarPubMed
Van Blerkom, J. (1989). Maturation at high frequency of germinal-vesicle-stage mouse oocytes after cryopreservation: Alterations in cytoplasmic, nuclear, nucleolar and chromosomal structure and organization associated with vitrification. Human Reproduction, 4(8), 883898. doi: 10.1093/oxfordjournals.humrep.a137006 CrossRefGoogle ScholarPubMed
Vajta, G., Holm, P., Kuwayama, M., Booth, P. J., Jacobsen, H., Greve, T. and Callesen, H. (1998). Open pulled straw (OPS) vitrification: A new way to reduce cryoinjuries of bovine ova and embryos. Molecular Reproduction and Development, 51(1), 5358. doi: 10.1002/(SICI)1098-2795(199809)51:1<53::AID-MRD6>3.0.CO;2-V 3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Whittingham, D. G. (1971). Culture of mouse ova. Journal of Reproduction and Fertility. Supplement, 14, 721.Google ScholarPubMed
Wongsrikeao, P., Otoi, T., Yamasaki, H., Agung, B., Taniguchi, M., Naoi, H., Shimizu, R. and Nagai, T. (2006). Effects of single and double exposure to brilliant cresyl blue on the selection of porcine oocytes for in vitro production of embryos. Theriogenology, 66(2), 366372. doi: 10.1016/j.theriogenology.2005.12.001 CrossRefGoogle ScholarPubMed
Wu, Y. G., Liu, Y., Zhou, P., Lan, G. C., Han, D., Miao, D. Q. and Tan, J. H. (2007). Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: A study using the mouse model. Cell Research, 17(8), 722731. doi: 10.1038/cr.2007.66 CrossRefGoogle ScholarPubMed