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Assessment of cGMP level in medium during in vitro growth period of murine preantral follicles with and without supplementation of C-type natriuretic peptide

Published online by Cambridge University Press:  22 June 2021

Li Ang
Affiliation:
Department of Biochemistry, Shanxi Medical University, Taiyuan, 030001, China
Guo Xingping
Affiliation:
Shanxi Provincial Key Laboratory of Cell Regeneration and Birth Defects, Taiyuan, 030001, China
Cao Haixia
Affiliation:
Shanxi Provincial Key Laboratory of Cell Regeneration and Birth Defects, Taiyuan, 030001, China
Wang Zhulin
Affiliation:
School of Environment and Engineering, Tianjin Industrial University, Tianjin, 300387, China
Wang Huaixiu*
Affiliation:
Shanxi Provincial Key Laboratory of Cell Regeneration and Birth Defects, Taiyuan, 030001, China Beijing Perfect Family Hospital, Beijing, 100034, China
*
Author for correspondence: Wang Huaixiu. Shanxi Provincial Key Laboratory of Cell Regeneration and Birth Defects, Taiyuan, 030001, China. E-mail: 976378008@qq.com

Summary

To enhance the developmental competency of murine ovarian follicles cultured in vitro, C-type natriuretic peptide (CNP) was supplemented in the culture system. Although the mechanism is not fully elucidated, it was reported that the effect of CNP supplementation was mediated by increased cyclic guanosine monophosphate (cGMP). In the present study, cGMP levels in media for murine preantral follicle culture were compared both between a control group without CNP supplementation and an experimental group with CNP supplementation and between days in each group. In addition, follicle growth patterns and oocyte maturity were assessed and compared between the two groups. Results demonstrated that along with in vitro culture, cGMP levels increased (P < 0.05) both in the control group and the experimental group, whereas cGMP levels were not significantly different between the two groups on the same day of in vitro culture (P > 0.05). The oocyte’s maturity was superior in the experimental group compared with the control group (P < 0.05). As ovarian follicles grew three-dimensionally in the experimental group but were flattened in the control group, CNP might improve oocyte maturity through maintaining the three-dimensional architecture of the ovarian follicle because of increased transzonal projections (TZP) and functional gap junctions between oocyte and surrounding granulosa cells.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Alexander, B, Coppola, G, Di Berardino, D, Rho, GJ, St John, E, Betts, DH and King, WA (2006). The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos. Mol Reprod Dev 73, 2030.CrossRefGoogle ScholarPubMed
Appeltant, R, Somfai, T, Maes, D, VAN Soom, A and Kikuchi, K (2016). Porcine oocyte maturation in vitro: role of CAMP and oocyte-secreted factors – a practical approach. J Reprod Dev 62, 439–49.CrossRefGoogle ScholarPubMed
Bouhelan, R, Bockaert, J, Mermet-Bouvier, R, Guillon, G and Homburger, V (1987). Heavy isotope labeling study of the turnover of forskolin-stimulated adenylate-cyclase in BC3H1 cell line. J Biol Chem 262, 8470–5.CrossRefGoogle Scholar
Brito, IR, Lima, IM, Xu, M, Shea, LD, Woodruff, TK and Figuerrado, JR (2014). Three-dimensional systems for in vitro follicular culture: overview of alginate-based matrices Reprod Fertil Dev 26, 915–30.CrossRefGoogle ScholarPubMed
Cheng, Y, Fan, HY, Wen, DC, Tong, C, Zhu, ZY, Lei, L, Sun, QY and Chen, DY (2003). Asynchronous cytoplast and karyoplast transplantation reveals that the cytoplasm determines the developmental fate of the nucleus in mouse oocytes. Mol Reprod Dev 65, 278–82.CrossRefGoogle ScholarPubMed
Choi, JK, Agarwal, P and He, X (2013). In vitro culture of early secondary preantral follicles in hanging drop of ovarian cell-conditioned medium to obtain MII oocytes from out-bred deer mice. Tissue Eng Part A 19(23–24), 2626–37.CrossRefGoogle Scholar
Eppig, JJ and O’Brien, MJ (1996). Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 54, 197207.CrossRefGoogle ScholarPubMed
Eppig, JJ, Pendola, FL, Wigglesworth, K and Pendola, JK (2005). Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol Reprod 73, 351–7.CrossRefGoogle ScholarPubMed
Follin-Arbelet, V, Misund, K, Naderi, EH, Ugland, H, Sundan, A and Blomhoff, HK (2015). The natural compound forskolin synergized with dexamethasone to induce cell death in myeloma cells via BIM. Scirep-UK 5, 13001.Google Scholar
Franciosi, F, Coticchio, G, Lodde, V, Tessaro, I, Modina, SC, Fadini, R, Dal Canto, M, Renzini, MM, Albertini, DF and Luciano, AM (2014). Natriuretic peptide precursor C delays meiotic resumptions and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod 91, 61.CrossRefGoogle Scholar
Gilchrist, RB, Luciano, AM, Richani, D, Zeng, HT, Wang, X, Devos, M, Sugimura, S, Smitz, J, Richard, FJ and Thompson, JG (2016). Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R14357.CrossRefGoogle ScholarPubMed
Green, LJ and Shikanov, A (2016). In vitro culture methods of preantral follicles. Theriogenology 86, 229–38.CrossRefGoogle ScholarPubMed
Hiradate, Y, Hoshino, Y, Taemura, K and Sato, E (2013). C-type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote 22, 372–7.CrossRefGoogle ScholarPubMed
Hsueh, AJW, Kawamura, K, Cheng, Y and Fauser, BC (2015). Intraovarian control of early folliculogenesis. Endocr Rev 36, 124.CrossRefGoogle ScholarPubMed
Jin, SY, Lei, J, Shikanov, A, Shea, LD and Woodruff, TK (2010). A novel two-step strategy for in vitro culture of early stage ovarian follicles in the mouse. Fertil Steril 93, 2633–9.CrossRefGoogle ScholarPubMed
Kim, EJ, Lee, J, Youm, HW, Kim, SK, Lee, JR, Suh, CS and Kim, SH (2018). Comparison of follicle isolation methods for mouse ovarian follicle culture in vitro . Reprod Sci 25, 1270–8.CrossRefGoogle ScholarPubMed
Kreegar, PK, Deck, JW, Woodruff, TK and Shea, LD (2006). The in vitro regulation of ovarian follicle development using alginate extracellular matrix gels. Biomaterials 27, 714–23.CrossRefGoogle Scholar
Li, A, Cao, HX, Li, HX, Li, RJ, Guo, XP and Wang, HX (2021). Supplementation of C-type natriuretic peptide during the in vitro growth period benefits the development of murine preantral follicles. Zygote 29, 15.Google Scholar
Machaty, Z, Miller, AR and Zhang, L (2017). Egg activation at fertilization. Adv Exp Med Biol 953, 147.CrossRefGoogle ScholarPubMed
Mainigi, MA, Ord, T and Schultz, RM (2011). Meiotic and developmental competence in mice are compromised following follicle development in vitro using an alginate-based culture system. Biol Reprod 85, 269–76.CrossRefGoogle ScholarPubMed
Mochida, N, Akatani-Hasegawa, A, Saka, K, Ogino, M, Hosoda, Y, Wada, R, Sawai, H and Shibahara, H (2013). Live births from isolated primary/early secondary follicles following a multistep culture without organ culture in mice. Reproduction 146, 3747.CrossRefGoogle ScholarPubMed
Romero, S, Sanchez, F, Lolicato, F, Van Ranst, H and 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. Biol Reprod 95, 6473.CrossRefGoogle ScholarPubMed
Samake, S and Smith, LC (1997). Synchronization of cell division in eight-cell bovine embryos produced in vitro: effects of 6-dimethylaminopurine. J Reprod Fertil 48, 969–76.Google Scholar
Sato, Y, Cheng, Y, Kawamura, K, Takae, S and Hsueh, AJ (2012). C-type natriuretic peptide stimulates ovarian follicle development. Mol Endocrinol 26, 1158–66.CrossRefGoogle ScholarPubMed
Shikanov, A, Xu, M, Woodruff, TK and Shea, LD (2009). Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476–85.CrossRefGoogle ScholarPubMed
Simli, M, Pellerano, P, Pigullo, S, Tavosanis, G, Ottaggio, L, de Saint-Georges, L and Bonatti, S (1997). 6-DMAP inhibition of early cell cycle events and induction of mitotic abnormalities. Mutagenesis 12, 313–9.CrossRefGoogle Scholar
Soto-Heras, S, Peramzo, M-T and Thompson, JG (2019). Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus–oocyte communication and oocyte developmental competence in cattle. Anim Reprod Sci 202, 4957.CrossRefGoogle ScholarPubMed
Telfer, EE and Zelinski, MB (2013). Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil Steril 99, 1523–33.CrossRefGoogle ScholarPubMed
Tiwari, M, Prasad, S, Tripathi, A, Pandey, AN, Ali, I, Singh, AK, Shrivastav, TG and Chaube, SK (2015). Apoptosis in mammalian oocytes: a review. Apoptosis 20, 1019–25.CrossRefGoogle ScholarPubMed
Vanacker, J and Amorim, CA (2017). Alginate: a versatile biomaterial to encapsulate isolated ovarian follicles. Ann Biomed Eng 45, 1633–49.CrossRefGoogle ScholarPubMed
Wei, Q, Zhou, C, Yuan, M, Miao, Y, Zhao, X and Ma, B (2017). Effect of c-type natriuretic peptide on maturation and developmental competence of immature mouse oocytes in vitro . Reprod Fertil Dev 29, 319–24.CrossRefGoogle ScholarPubMed
West, ER, Shea, LD and Woodruff, TK (2007). Engineering the follicle microenvironment. Semin Reprod Med 25, 287–99.CrossRefGoogle ScholarPubMed
Wycheley, G, Downey, D, Kane, MT and Hynes, AC (2004). A novel follicle culture system markedly increases follicle volume, cell number and oestradiol secretion. Reproduction 127, 669–77.CrossRefGoogle Scholar
Xi, GY, Wang, W, Fazlani, SA, Yao, F, Yang, M, Hao, J, An, L and Tian, J (2019). C-type natriuretic peptide enhances mouse preantral follicle growth. Reproduction 157, 445–55.CrossRefGoogle ScholarPubMed
Yang, L, Wei, Q, Li, W, Ge, J, Zhao, X and Ma, B (2016). C-type natriuretic peptide improved vitrified-warmed mouse cumulus oocyte complexes developmental competence. Cryobiology 72, 161–4.CrossRefGoogle ScholarPubMed
Zhang, JH, Wei, Q, Cai, J, Zhao, X and Ma, B (2015). Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro . PLoS One 10, e0132318.CrossRefGoogle ScholarPubMed
Zhang, MJ, Su, YQ, Sugiura, K, Xia, G and Eppig, JJ (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330(6002), 366–9.CrossRefGoogle ScholarPubMed
Zhang, T, Zhang, C, Fan, X, Li, R and Zhang, J (2017a). Effect of C-type natriuretic peptide pretreatment on in vitro bovine maturation. In Vitro Cell Dev Biol 53, 199206.CrossRefGoogle ScholarPubMed
Zhang, YH, Wang, H, Liu, W, Yang, Y, Wang, X, Zhang, Z, Guo, Q, Wang, C and Xia, G (2017b). Natriuretic peptides improve the developmental competence of in vitro cultured porcine oocytes. Reprod Biol Endocrinol 15, 4152.CrossRefGoogle ScholarPubMed
Zhong, T, Fan, X, Li, R, Zhang, C and Zhang, J (2018). Effects of pre-incubation with C-type natriuretic peptide on nuclear maturation, mitochondrial behavior and developmental competence of sheep oocytes. Oogenesis 497, 200–6.Google Scholar
Zhong, YG, Lin, J, Liu, X, Hou, J, Zhang, Y and Zhao, X (2015). C-type natriuretic peptide maintains domestic cat oocytes in meiotic arrest. Reprod Fertil Dev doi.org/10.1071./RD14425. Epub ahead of print.Google ScholarPubMed