Meiotic block with roscovitine improves competence of porcine oocytes by fine-tuning activities of different cyclin-dependent kinases.
Animals
Cell Nucleus
/ drug effects
Chromatin
/ metabolism
Cyclin-Dependent Kinases
/ metabolism
Embryo, Mammalian
/ drug effects
Embryonic Development
/ drug effects
Female
In Vitro Oocyte Maturation Techniques
/ methods
Meiosis
/ drug effects
Oocytes
/ drug effects
Roscovitine
/ pharmacology
Swine
Transcription, Genetic
/ drug effects
cyclin-dependent kinase
meiosis
oocyte competence
pig
roscovitine
Journal
Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
22
11
2019
accepted:
13
02
2020
pubmed:
27
2
2020
medline:
5
3
2021
entrez:
27
2
2020
Statut:
ppublish
Résumé
Successful use of oocytes from small follicles (SFs) is of great importance for animal embryo production and human in vitro fertilization with reduced hormone-related side effects. How in vitro meiotic arrest maintenance (MAM) increases the competence of oocytes is not clear. In this study, pig oocytes recovered from SF of 1-2 mm and medium-follicles (MF) of 3-6 mm in diameter from abattoir ovaries were treated by various MAM treatments to improve their competence. The results showed that 25 µM roscovitine or 1 mM db-cAMP efficiently blocked germinal vesicle breakdown in both SF and MF oocytes suggesting a similar cyclin-dependent kinase (CDK) 1 level between the two oocyte groups. MAM with 15- and 25-µM roscovitine alone or with 1-mM db-cAMP improved competence of SF and MF oocytes, respectively, with a promoted chromatin configuration transition from surrounded nucleoli (SN) to re-decondensation (RDC) pattern that supported substantial gene transcription. However, MAM with db-cAMP alone or with higher concentrations of roscovitine did not improve oocyte competence, could not support an SN-to-RDC transition, and/or evoked a premature chromatin condensation (PMC) that suppressed gene transcription. Both CDK2 and CDK5 contents were higher (p < .05) in MF than in SF oocytes. It is concluded that the competence of pig oocytes, particularly that of SF oocytes can be improved by MAM using a proper roscovitine concentration that promotes gene transcription by inhibiting CDK5 while letting CDK2 off to prevent PMC.
Substances chimiques
Chromatin
0
Roscovitine
0ES1C2KQ94
Cyclin-Dependent Kinases
EC 2.7.11.22
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7530-7540Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Abeydeera, L. R., Wang, H., Cantley, T., Rieke, A., Prather, R. S., & 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, 395-401.
Adhikari, D., Zheng, W., Shen, Y., Gorre, N., Ning, Y., Halet, G., … Liu, K. (2012). Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Human Molecular Genetics, 21, 2476-2484.
Adona, P. R., & Leal, C. L. V. (2004). Meiotic inhibition with different cyclin-dependent kinase inhibitors in bovine oocytes and its effects on maturation and embryo development. Zygote, 12, 197-204.
Alexandrow, M. G., & Hamlin, J. L. (2005). Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. Journal of Cell Biology, 168, 875-886.
De Azevedo, W. F., Leclerc, S., Meijer, L., Havlicek, L., Strnad, M., & Kim, S. H. (1997). Inhibition of cyclin-dependent kinases by purine analogues: Crystal structure of human cdk2 complexed with roscovitine. European Journal of Biochemistry, 243, 518-526.
Bilodeau-Goeseels, S. (2012). Bovine oocyte meiotic inhibition before in vitro maturation and its value to in vitro embryo production: Does it improve developmental competence? Reproduction in Domestic Animals, 47, 687-693.
Chen, F., Lin, J., Sun, X., Xiao, B., Ning, S. F., Zhu, S., Wang, H. L., … Tan, J. H. (2017). Mechanisms by which in vitro meiotic arrest and sexual maturity improve developmental potential of mouse oocytes. Scientific Reports, 7, 15763.
Chen, M. C., Lin, H., Hsu, F. N., Huang, P. H., Lee, G. S., & Wang, P. S. (2010). Involvement of cAMP in nerve growth factor-triggered p35/Cdk5 activation and differentiation in PC12 cells. American Journal of Physiology: Cell Physiology, 299, C516-C527.
D'Angiolella, V., Costanzo, V., Gottesman, M. E., Avvedimento, E. V., Gautier, J., & Grieco, D. (2001). Role for cyclin-dependent kinase 2 in mitosis exit. Current Biology, 11, 1221-1226.
Day, B. N., & Funahashi, H. (1996). In vitro maturation and fertilization of pig oocytes. In R. H. Miller, V. G. Pursel & H. D. Norman (Eds.), Beltsville symposia in agricultural research XX. Biotechnology's role in the genetic improvement of farm animals (pp. 125-144). Savoy, IL: American Society of Animal Science.
Ezoe, K., Yabuuchi, A., Tani, T., Mori, C., Miki, T., Takayama, Y., … Kato, K. (2015). Developmental competence of vitrified-warmed bovine oocytes at the germinal-vesicle stage is improved by cyclic adenosine monophosphate modulators during in vitro maturation. PLoS One, 10, e0126801.
Funahashi, H., Cantley, T. C., & Day, B. N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biology of Reproduction, 57, 49-53.
Funahashi, H., & Day, B. N. (1997). Advances in in vitro production of pig embryos. Journal of Reproduction and Fertility, Supplement 52, 271-283.
Gil, M. A., Cuello, C., Parrilla, I., Vazquez, J. M., Roca, J., & Martinez, E. A. (2010). Advances in swine in vitro embryo production technologies. Reproduction in Domestic Animals, 45(Suppl 2), 40-48.
Gosden, R., Krapez, J., & Briggs, D. (1997). Growth and development of the mammalian oocyte. BioEssays, 19, 875-882.
Han, D., Lan, G. C., Wu, Y. G., Han, Z. B., Wang, H. L., & Tan, J. H. (2006). Factors affecting the efficiency and reversibility of roscovitine (ROS) block on the meiotic resumption of goat oocytes. Molecular Reproduction and Development, 73, 238-246.
Han, S. J., & Conti, M. (2006). New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle, 5, 227-231.
Hashimoto, S., Minami, N., Takakura, R., & Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biology of Reproduction, 66, 1696-1701.
Hyttel, P., Fair, T., Callesen, H., & Greve, T. (1997). Oocyte growth, capacitation, and final maturation in cattle. Theriogenology, 47, 23-32.
Jeon, S., Kim, Y., Chung, I. W., & Kim, Y. S. (2015). Clozapine induces chloride channel-4 expression through PKA activation and modulates CDK5 expression in SH-SY5Y and U87 cells. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 56, 168-173.
Jiao, G. Z., Cui, W., Yang, R., Lin, J., Gong, S., Lian, H. Y., … Tan, J. H. (2016). Optimized protocols for in vitro maturation of rat oocytes dramatically improve their developmental competence to a level similar to that of ovulated oocytes. Cellular Reprogramming, 18, 17-29.
Jimenez-Macedo, A. R., Izquierdo, D., Urdaneta, A., Anguita, B., & Paramio, M. T. (2006). Effect of roscovitine on nuclear maturation, MPF and MAP kinase activity and embryo development of prepubertal goat oocytes. Theriogenology, 65, 1769-1782.
Kohata, C., Izquierdo-Rico, M. J., Romar, R., & Funahashi, H. (2013). Development competence and relative transcript abundance of oocytes derived from small and medium follicles of prepubertal gilts. Theriogenology, 80, 970-978.
Li, Z., David, G., Hung, K. W., DePinho, R. A., Fu, A. K., & Ip, N. Y. (2004). Cdk5/p35 phosphorylates mSds3 and regulates mSds3-mediated repression of transcription. Journal of Biological Chemistry, 279, 54438-54444.
Livak, K. J., & 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, 402-408.
Lodde, V., Franciosi, F., Tessaro, I., Modina, S. C., & Luciano, A. M. (2013). Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. Journal Of Assisted Reproduction And Genetics, 30, 1219-1226.
Marchal, R., Vigneron, C., Perreau, C., Bali-Papp, A., & Mermillod, P. (2002). Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology, 57, 1523-1532.
Meijer, L., Borgne, A., Mulner, O., Chong, J. P., Blow, J. J., Inagaki, N., … Moulinoux, J. P. (1997). Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2, and cdk5. European Journal of Biochemistry, 243, 527-536.
Monti, M., Zanoni, M., Calligaro, A., Ko, M. S., Mauri, P., & Redi, C. A. (2013). Developmental arrest and mouse antral not-surrounded nucleolus oocytes. Biology of Reproduction, 88(1), 2.
Morbeck, D. E., Esbenshade, K. L., Flowers, W. L., & Britt, J. H. (1992). Kinetics of follicle growth in the prepubertal gilt. Biology of Reproduction, 47, 485-491.
Nagai, T., Funahashi, H., Yoshioka, K., & Kikuchi, K. (2006). Up date of in vitro production of porcine embryos. Frontiers in Bioscience, 11, 2565-2573.
Nastri, C. O., Ferriani, R. A., Rocha, I. A., & Martins, W. P. (2010). Ovarian hyperstimulation syndrome: Pathophysiology and prevention. Journal Of Assisted Reproduction And Genetics, 27, 121-128.
Onishi, T., & Hruska, K. (1997). Expression of p27Kip1 in osteoblast-like cells during differentiation with parathyroid hormone. Endocrinology, 138, 1995-2004.
Pan, L. Z., Zhu, S., Zhang, M., Sun, M. J., Lin, J., Chen, F., & Tan, J. H. (2018). A new classification of the germinal vesicle chromatin configurations in pig oocytes. Biology of Reproduction, 99, 1149-1158.
Pandey, S., Somal, A., Parmar, M. S., Gupta, S., Bharti, M. K., Bhat, I. A., … Sharma, G. T. (2018). Effect of roscovitine on developmental competence of small follicle-derived buffalo oocytes. Indian Journal of Medical Research, 148(Suppl), S140-S150.
Pandey, S., Somal, A., Parmar, M. S., Gupta, S., Chandra, V., Kumar, G. S., & Sharma, G. T. (2017). Comparative analysis of developmental and molecular correlates of developmental competence of buffalo oocytes derived from small and large follicles. Indian Journal of Animal Sciences, 87, 1194-1199.
Pavlok, A., Kanka, J., Motlík, J., & Vodicka, P. (2000). Culture of bovine oocytes from small antral follicles in meiosis-inhibiting medium with butyrolactone I: RNA synthesis, nucleolar morphology, and meiotic competence. Animal Reproduction Science, 64, 1-11.
Romero, S., Sánchez, F., Lolicato, F., Van Ranst, H., & Smitz, J. (2016). Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium. Biology of Reproduction, 95, 64.
Sananmuang, T., Techakumphu, M., & Tharasanit, T. (2010). The effects of roscovitine on cumulus cell apoptosis and the developmental competence of domestic cat oocytes. Theriogenology, 73, 199-207.
Solc, P., Schultz, R. M., & Motlik, J. (2010). Prophase I arrest and progression to metaphase I in mouse oocytes: Comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Molecular Human Reproduction, 16, 654-664.
Sun, M. J., Zhu, S., Li, Y. W., Lin, J., Gong, S., Jiao, G. Z., Chen, F., … Tan, J. H. (2016). An essential role for the intra-oocyte MAPK activity in the NSN-to-SN transition of germinal vesicle chromatin configuration in porcine oocytes. Scientific Reports, 6, 23555.
Sánchez, F., Lolicato, F., Romero, S., De Vos, M., Van Ranst, H., Verheyen, G., … Smitz, J. E. J. (2017). An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Human Reproduction, 32, 2056-2068.
Tan, J. H., Wang, H. L., Sun, X. S., Liu, Y., Sui, H. S., & Zhang, J. (2009). Chromatin configurations in the germinal vesicle of mammalian oocytes. Molecular Human Reproduction, 15, 1-9.
Wu, G. M., Sun, Q. Y., Mao, J., Lai, L., McCauley, T. C., Park, K. W., … Day, B. N. (2002). High developmental competence of pig oocytes after meiotic inhibition with a specific M-phase promoting factor kinase inhibitor, butyrolactone I. Biology of Reproduction, 67, 170-177.
Yoon, J. D., Jeon, Y., Cai, L., Hwang, S. U., Kim, E., Lee, E., … Hyun, S. H. (2015). Effects of coculture with cumulus-derived somatic cells on in vitro maturation of porcine oocytes. Theriogenology, 83, 294-305.
Yoon, K. W., Shin, T. Y., Park, J. I., Roh, S., Lim, J. M., Lee, B. C., … Lee, E. S. (2000). Development of porcine oocytes from preovulatory follicles of different sizes after maturation in media supplemented with follicular fluids. Reproduction, Fertility, and Development, 12, 133-139.
Zeng, H. T., Ren, Z., Guzman, L., Wang, X., Sutton-McDowall, M. L., Ritter, L. J., … Gilchrist, R. B. (2013). Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Human Reproduction, 28, 1536-1545.
Zeng, H. T., Richani, D., Sutton-McDowall, M. L., Ren, Z., Smitz, J. E., Stokes, Y., … Thompson, J. G. (2014). Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biology of Reproduction, 91, 47.
Zhang, M., Zhang, C. X., Pan, L. Z., Gong, S., Cui, W., Yuan, H. J., … Tan, J. H. (2017). Meiotic arrest with roscovitine and follicular fluid improves cytoplasmic maturation of porcine oocytes by promoting chromatin de-condensation and gene transcription. Scientific Reports, 7, 11574.