Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T12:14:08.120Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of milrinone on the meiosis resumption and cytoplasm maturation of buffalo oocytes

Published online by Cambridge University Press:  11 May 2022

Guihua Bian Open the ORCID record for Guihua Bian [Opens in a new window] ,
Wen Shi ,
Linwei Duan ,
Yungan Zhu ,
Laiba Shafique ,
Qingyou Liu ,
Deshun Shi  and
Wenhua Xiao
Guihua Bian
Affiliation:
Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China
Wen Shi
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning, 530005, China
Linwei Duan
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning, 530005, China
Yungan Zhu
Affiliation:
Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China
Laiba Shafique
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning, 530005, China
Qingyou Liu
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning, 530005, China
Deshun Shi*
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning, 530005, China
Wenhua Xiao*
Affiliation:
Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China
*
Authors for correspondence: Deshun Shi. Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China. E-mail: ardsshi@gxu.edu.cn.Wenhua Xiao. Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China. E-mail: bkxwh2006@126.com
Authors for correspondence: Deshun Shi. Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China. E-mail: ardsshi@gxu.edu.cn.Wenhua Xiao. Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China. E-mail: bkxwh2006@126.com
Get access Rights & Permissions [Opens in a new window]

Summary

Buffalo has many excellent economic traits and it is one of the greatest potential livestock. Compared with cattle, buffalo has poorer reproductivity, it is of great significance to improve the development potential of oocytes. Buffalo oocyte in vitro maturation (IVM) has been widely used in production, but the poor development ability of bovine oocytes IVM limits the development of buffalo reproductivity. Milrinone as a phosphodiesterase inhibitor could affect the maturation of oocytes in goat and mice, but there have been few reported studies in water buffalo. To optimize buffalo oocyte in vitro maturation systems, the effects of phosphodiesterase inhibitor (milrinone) on pre-maturation culture of buffalo oocytes were investigated in this study. Buffalo cumulus–oocyte complexes (COCs) were cultured in medium with different concentrations (0, 12, 25, 50 and 100 mol/l) of milrinone for different times (0, 4, 8, 12, 16, 22 and 24 h). The results showed that the buffalo COCs nuclear maturation process could be inhibited by milrinone (25–100 mol/l) in a dose-dependent manner. The inhibitory effect of milrinone on in vitro maturation of buffalo oocytes did not decrease with the extension of time. This indicated that milrinone can be used as a nuclear maturation inhibitor during the maturation process in buffalo oocytes. In addition, milrinone can inhibit the effect of follicle stimulating hormone (FSH)-induced IVM of buffalo oocytes, but with time FSH partially eliminated the inhibition. Therefore, inhibition of milrinone on the nuclear maturation of buffalo oocytes was reversible, and buffalo oocytes can mature normally after the inhibition is lessened.

Keywords

BuffaloIVFIVMMilrinoneOocyte
Type
Research Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 571 - 576
Copyright
© The Author(s), 2022. 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.)

Footnotes

*

Equivalent contributor authors.

References

Alam, M. H., Lee, J. and Miyano, T. (2018). Inhibition of PDE3A sustains meiotic arrest and gap junction of bovine growing oocytes in in vitro growth culture. Theriogenology, 118, 110–118. doi: 10.1016/j.theriogenology.2018.05.028 CrossRefGoogle ScholarPubMed
Byskov, A. G., Yding Andersen, C. Y., Hossaini, A. and Guoliang, X. (1997). Cumulus cells of oocyte-cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Molecular Reproduction and Development, 46(3), 296–305. doi: 10.1002/(SICI)1098-2795(199703)3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E. and First, N. (1998). Bovine oocyte as a universal recipient cytoplasm in mammalian nuclear transfer. Theriogenology, 49(1), 385. doi: 10.1016/S0093-691X(98)90738-5 CrossRefGoogle Scholar
Downs, S. M. and Eppig, J. J. (1984). Cyclic adenosine monophosphate and ovarian follicular fluid act synergistically to inhibit mouse oocyte maturation. Endocrinology, 114(2), 418–427. doi: 10.1210/endo-114-2-418 CrossRefGoogle ScholarPubMed
Downs, S. M., Coleman, D. L., Ward-Bailey, P. F. and Eppig, J. J. (1985). Hypoxanthine is the principal inhibitor of murine oocyte maturation in a low molecular weight fraction of porcine follicular fluid. Proceedings of the National Academy of Sciences of the United States of America, 82(2), 454–458. doi: 10.1073/pnas.82.2.454 CrossRefGoogle Scholar
Downs, S. M., Daniel, S. A., Bornslaeger, E. A., Hoppe, P. C. and Eppig, J. J. (1989). Maintenance of meiotic arrest in mouse oocytes by purines: Modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Research, 23(3), 323–334. doi: 10.1002/mrd.1120230309 CrossRefGoogle ScholarPubMed
Eppig, J. J., Ward-Bailey, P. F. and Coleman, D. L. (1985). Hypoxanthine and adenosine in murine ovarian follicular fluid: Concentrations and activity in maintaining oocyte meiotic arrest. Biology of Reproduction, 33(5), 1041–1049. doi: 10.1095/biolreprod33.5.1041 CrossRefGoogle ScholarPubMed
Gasparrini, B. (2002). In vitro embryo production in buffalo species: State of the art. Theriogenology, 57(1), 237–256. doi: 10.1016/s0093-691x(01)00669-0 CrossRefGoogle ScholarPubMed
Gershon, E., Maimon, I., Galiani, D., Elbaz, M., Karasenti, S. and Dekel, N. (2019). High cGMP and low PDE3A activity are associated with oocyte meiotic incompetence. Cell Cycle, 18(20), 2629–2640. doi: 10.1080/15384101.2019.1652472 CrossRefGoogle ScholarPubMed
Gharibi, S., Hajian, M., Ostadhosseini, S., Hosseini, S. M., Forouzanfar, M. and Nasr-Esfahani, M. H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology, 80(4), 302–312. doi: 10.1016/j.theriogenology.2013.04.012 CrossRefGoogle ScholarPubMed
Gilchrist, R. B., Luciano, A. M., Richani, D., Zeng, H. T., Wang, X., De Vos, M. D., Sugimura, S., Smitz, J., Richard, F. J. and Thompson, J. G. (2016). Oocyte maturation and quality: Role of cyclic nucleotides. Reproduction, 152(5), R143–R157. doi: 10.1530/REP-15-0606 CrossRefGoogle ScholarPubMed
Guimarães, A. L., Pereira, S. A., Kussano, N. R. and Dode, M. A. (2016). The effect of pre-maturation culture using phosphodiesterase type 3 inhibitor and insulin, transferrin and selenium on nuclear and cytoplasmic maturation of bovine oocytes. Zygote, 24(2), 219–229. doi: 10.1017/S0967199415000064 CrossRefGoogle ScholarPubMed
Guo, R., Wang, X., Li, Q., Sun, X., Zhang, J. and Hao, R. (2020). Follicular fluid meiosis-activating sterol (FF-MAS) promotes meiotic resumption via the MAPK pathway in porcine oocytes. Theriogenology, 148, 186–193. doi: 10.1016/j.theriogenology.2019.11.012 CrossRefGoogle ScholarPubMed
Jensen, J. T., Schwinof, K. M., Zelinski-Wooten, M. B., Conti, M., DePaolo, L. V. and Stouffer, R. L. (2002). Phosphodiesterase 3 inhibitors selectively block the spontaneous resumption of meiosis by macaque oocytes in vitro . Human Reproduction, 17(8), 2079–2084. doi: 10.1093/humrep/17.8.2079 CrossRefGoogle ScholarPubMed
Jia, Z., Tian, J., An, L. et al. (2013). Advances in bovine oocyte maturation in vitro . Chinese Journal of Agricultural Sciences, 46(8), 1716–1724.Google Scholar
Kalinowski, R. R., Berlot, C. H., Jones, T. L., Ross, L. F., Jaffe, L. A. and Mehlmann, L. M. (2004). Maintenance of meiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Developmental Biology, 267(1), 1–13. doi: 10.1016/j.ydbio.2003.11.011 CrossRefGoogle ScholarPubMed
Keefer, C. L. (2015). Artificial cloning of domestic animals. Proceedings of the National Academy of Sciences of the United States of America, 112(29), 8874–8878. doi: 10.1073/pnas.1501718112 CrossRefGoogle ScholarPubMed
Kumar, D. and Anand, T. (2012). In vitro embryo production in buffalo: Basic concepts. Journal of Buffalo Science, 1(1), 50–54. doi: 10.6000/1927-520X.2012.01.01.09 CrossRefGoogle Scholar
Le Beux, G., Richard, F. J. and Sirard, M. A. (2003). Effect of cycloheximide, 6-DMAP, roscovitine and butyrolactone I on resumption of meiosis in porcine oocytes. Theriogenology, 60(6), 1049–1058. doi: 10.1016/s0093-691x(03)00124-9 CrossRefGoogle ScholarPubMed
Lee, J. H. and Maalouf, W. E. (2015). Nuclear transfer in ruminants. In. Methods in Molecular Biology, 1222, 25–36. doi: 10.1007/978-1-4939-1594-1_3 CrossRefGoogle ScholarPubMed
Lonergan, P., Dinnyes, A., Fair, T., Yang, X. and Boland, M. (2000). Bovine oocyte and embryo development following meiotic inhibition with butyrolactone I. Molecular Reproduction and Development, 57(2), 204–209. doi:10.1002/1098-2795(200010)57:2<204::AID-MRD12>3.0.CO;2-N3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Maurice, D. H. and Haslam, R. J. (1990). Molecular basis of the synergistic inhibition of platelet function by nitrovasodilators and activators of adenylate cyclase: Inhibition of cyclic AMP breakdown by cyclic GMP. Molecular Pharmacology, 37(5), 671–681.Google ScholarPubMed
Nogueira, D., Cortvrindt, R., De Matos, D. G., Vanhoutte, L. and Smitz, J. (2003). Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro . Biology of Reproduction, 69(6), 2045–2052. doi: 10.1095/biolreprod.103.021105 CrossRefGoogle ScholarPubMed
Rime, H., Neant, I., Guerrier, P. and Ozon, R. (1989). 6-dimethylaminopurine (6-DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte. Developmental Biology, 133(1), 169–179. doi: 10.1016/0012-1606(89)90308-4 CrossRefGoogle Scholar
Romero, S. and Smitz, J. (2010). Improvement of in vitro culture of mouse cumulus–oocyte complexes using PDE3-inhibitor followed by meiosis induction with epiregulin. Fertility and Sterility, 93(3), 936–944. doi: 10.1016/j.fertnstert.2008.10.016 CrossRefGoogle ScholarPubMed
Rubessa, M., Boccia, L. and Di Francesco, S. (2019). In vitro embryo production in buffalo species (Bubalus bubalis). In. Methods in Molecular Biology, 2006, 179–190. doi: 10.1007/978-1-4939-9566-0_13 CrossRefGoogle Scholar
Shafiee-Nick, R., Afshari, A. R., Mousavi, S. H., Rafighdoust, A., Askari, V. R., Mollazadeh, H., Fanoudi, S., Mohtashami, E., Rahimi, V. B., Mohebbi, M. and Vahedi, M. M. (2017). A comprehensive review on the potential therapeutic benefits of phosphodiesterase inhibitors on cardiovascular diseases. Biomedicine and Pharmacotherapy, 94, 541–556. doi: 10.1016/j.biopha.2017.07.084 CrossRefGoogle ScholarPubMed
Silva, B. R., Maside, C., Vieira, L. A., Cadenas, J., Alves, B. G., Ferreira, A. C. A., Aguiar, F. L. N., Silva, A. L. C., Figueiredo, J. R. and Silva, J. R. V. (2018). Dose-dependent effects of frutalin on in vitro maturation and fertilization of pig oocytes. Animal Reproduction Science, 192, 216–222. doi: 10.1016/j.anireprosci.2018.03.015 CrossRefGoogle ScholarPubMed
Sirard, M. A. and Blondin, P. (1996). Oocyte maturation and IVF in cattle. Animal Reproduction Science, 42(1–4), 417–426. doi: 10.1016/0378-4320(96)01518-7 CrossRefGoogle Scholar
Thomas, R. E., Armstrong, D. T. and Gilchrist, R. B. (2002). Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Developmental Biology, 244(2), 215–225. doi: 10.1006/dbio.2002.0609 CrossRefGoogle ScholarPubMed
Thomas, R. E., Armstrong, D. T. and Gilchrist, R. B. (2004). Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biology of Reproduction, 70(3), 548–556. doi: 10.1095/biolreprod.103.021204 CrossRefGoogle ScholarPubMed
Wang, L., Jiang, X., Wu, Y., Lin, J., Zhang, L., Yang, N. and Huang, J. (2016). Effect of milrinone on the developmental competence of growing lamb oocytes identified with brilliant cresyl blue. Theriogenology, 86(8), 2020–2027. doi: 10.1016/j.theriogenology.2016.06.024 CrossRefGoogle ScholarPubMed
Yi, Y. J. and Park, C. S. (2005). Parthenogenetic development of porcine oocytes treated by ethanol, cycloheximide, cytochalasin B and 6-dimethylaminopurine. Animal Reproduction Science, 86(3–4), 297–304. doi: 10.1016/j.anireprosci.2004.07.007 CrossRefGoogle ScholarPubMed
Supplementary material: File

Bian et al. supplementary material

Bian et al. supplementary material

Download Bian et al. supplementary material(File)
File 1.1 MB