Pre-IVM treatment with C-type natriuretic peptide in the presence of cysteamine enhances bovine oocytes antioxidant defense ability and developmental competence in vitro

Document Type : Full paper (Original article)

Authors

Department of Animal Genetic Breeding and Reproduction, College of Animal Science and Technology, Inner Mongolia University for the Nationalities, Tongliao, 028043, China

Abstract

Background: The use of C-type natriuretic peptide (CNP) combined with cysteamine during pre-in vitro maturation (IVM) can help establish an effective pre-IVM system. Aims: This study was designed to investigate the effects of CNP combined with cysteamine on meiotic maturation and developmental competence of bovine oocytes in vitro. Methods: Oocytes were cultured in pre-IVM medium supplemented with 100 nM CNP for 6 h in the absence or presence of 100 μM cysteamine, followed by standard IVM for 24 h. Oocytes matured by standard IVM for 24 h (no pre-IVM) were used as the control. The percentage of oocytes arrested at germinal vesicle (GV) stage in each treatment group was examined at 0 h of IVM, and the nuclear maturation rate was assessed by evaluating the percentages of oocytes that reached metaphase II (M II) stage at 24 h of IVM. After 24 h of IVM, oocytes were subjected to in vitro fertilization (IVF) and in vitro embryo culture (IVC). Cleavage rates were assessed 48 h post-insemination. Blastocyst production rates were recorded on day 8 after IVF. In addition, intra-oocyte glutathione (GSH) and reactive oxygen species (ROS) content for each treatment were tested at 0 h and 24 h of IVM. Results: No differences were observed between the CNP pre-IVM treatment and control groups in the rate of bovine oocytes maturing to the M II stage, cleavage and blastocysts production rates after IVF, and intra-oocyte GSH levels. Notably, the presence of cysteamine during pre-IVM culture with CNP significantly improved the rate of embryos developed to the blastocyst stage after in vitro maturation and fertilization, moreover, it increased the levels of GSH and reduced the levels of ROS in bovine oocytes. Conclusion: The improvement to IVM bovine oocyte developmental competence through pre-IVM with CNP combined with cysteamine may be associated with an increased antioxidant defense. Therefore, such an approach may be a good option for establishing a pre-IVM system.

Keywords


Albuz, FK; Sasseville, M; Lane, M; Armstrong, DT; Thompson, JG and Gilchrist, RB (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod., 25: 2999-3011.
Bannai, S (1984). Transport of cystine and cysteine in mammalian cells. Biochim. Biophys. Acta. 779: 289-306.
Curnow, EC; Ryan, JP; Saunders, DM and Hayes, ES (2010). Developmental potential of bovine oocytes following IVM in the presence of glutathione ethyl ester. Reprod. Fertil. Dev., 22: 597-605.
de Matos, DG and Furnus, CC (2000). The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of beta-mercaptoethanol, cysteine and cystine. Theriogenology. 53: 761-771.
de Matos, DG; Furnus, CC; Moses, DF and Baldassarre, H (1995). Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol. Reprod. Dev., 42: 432-436.
de Matos, DG; Herrera, C; Cortvrindt, R; Smitz, J; Van Soom, A; Nogueira, D and Pasqualini, RS (2002). Cysteamine supplementation during in vitro maturation and embryo culture: a useful tool for increasing the efficiency of bovine in vitro embryo production. Mol. Reprod. Dev., 62: 203-209.
Farghaly, T; Khalifa, E; Mostafa, S; Hussein, M; Bedaiwy, M and Ahmady, A (2015). The effect of temporary meiotic attenuation on the in vitro maturation outcome of bovine oocytes. In Vitro Cell. Dev. Biol. Anim., 51: 662-671.
Ferreira, EM; Vireque, AA; Adona, PR; Meirelles, FV; Ferriani, RA and Navarro, PA (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology. 71: 836-848.
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 resumption and sustains gap junction-mediated communication in bovine cumulus enclosed oocytes. Biol. Reprod., 91: 61.
Gilchrist, RB (2011). Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev., 23: 23-31.
Grupen, CG; Nagashima, H and Nottle, MB (1995). Cysteamine enhances in vitro development of porcine oocytes matured and fertilized in vitro. Biol. Reprod., 53: 173-178.
Guimarães, AL; Pereira, SA; Leme, LO and Dode, MA (2015). Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology. 83: 52-57.
Guixue, Z; Luciano, AM; Coenen, K; Gandolfi, F and Sirard, MA (2001). The influence of cAMP before or during bovine oocyte maturation on embryonic developmental competence. Theriogenology. 55: 1733-1743.
Izumi, H; Miyamoto, Y; Mori, T; Hashigami, Y; Chiba, Y; Teramura, T; Hashimoto, S; Fukuda, K; Morimoto, Y and Hosoi, Y (2013). Cysteamine supplementation during in vitro maturation (IVM) of rabbit oocyte improves the developmental capacity after intracytoplasmic sperm injection. Reprod. Med. Biol., 12: 179-185.
Li, HJ; Sutton-McDowall, ML; Wang, X; Sugimura, S; Thompson, JG and Gilchrist, RB (2016). Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum. Reprod., 31: 810-821.
Lodde, V; Franciosi, F; Tessaro, I; Modina, SC and Luciano, AM (2013). Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. J. Assist. Reprod. Genet., 30: 1219-1226.
Luciano, AM; Franciosi, F; Modina, SC and Lodde, V (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol. Reprod., 85: 1252-1259.
Mayes, MA and Sirard, MA (2001). Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol. Reprod., 66: 180-184.
Merton, JS; Knijn, HM; Flapper, H; Dotinga, F; Roelen, BA; Vos, PL and Mullaart, E (2013). Cysteamine supplementation during in vitro maturation of slaughterhouse-and opu-derived bovine oocytes improves embryonic development without affecting cryotolerance, pregnancy rate, and calf characteristics. Theriogenology. 80: 365-371.
Nedambale, TL; Du, F; Xu, J; Chaubal, SA; Dinnyes, A; Groen, W; Faber, D; Dobrinsky, JR; Yang, X and Tian, XC (2006). Prolonging bovine sperm-oocyte incubation in modified medium 199 improves embryo development rate and the viability of vitrified blastocysts. Theriogenology. 66: 1951-1960.
Ozawa, M; Hirabayashi, M and Kanai, Y (2002). Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction. 124: 683-689.
Ozawa, M; Nagai, T; Somfai, T; Nakai, M; Maedomari, N; Miyazaki, H; Kaneko, H; Noguchi, J and Kikuchi, K (2010). Cumulus cell-enclosed oocytes acquire a capacity to synthesize GSH by FSH stimulation during in vitro maturation in pigs. J. Cell. Physiol., 222: 294-301.
Razza, EM; Pedersen, HS; Stroebech, L; Fontes, PK; Kadarmideen, HN; Callesen, H; Pihl, M; Nogueira, MFG and Hyttel, P (2019). Simulated physiological oocyte maturation has side effects on bovine oocytes and embryos. J. Assist. Reprod. Genet., 36: 413-424.
Rizos, D; Ward, F; Duffy, P; Boland, MP and Lonergan, P (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev., 61: 234-248.
Rosenkrans, CFJr; Zeng, GQ; MCNamara, GT; Schoff, PK and First, NL (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod., 49: 459-462.
Sato, E; Matsuo, M and Miyamoto, H (1990). Meiotic maturation of bovine oocytes in vitro: improvement of meiotic competence by dibutyryl cyclic adenosine 3´,5´-monophosphate. J. Anim. Sci., 68: 1182-1187.
Soto-Heras, S; Paramio, MT and Thompson, JG (2019). Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus-oocyte com-munication and oocyte developmental competence in cattle. Anim. Reprod. Sci., 202: 49-57.
Sutton, ML; Gilchrist, RB and Thompson, JG (2003). Effects of in-vivo and in vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update. 9: 35-48.
Takahashi, M; Nagai, T; Hamano, S; Kuwayama, M; Okamura, N and Okano, A (1993). Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol. Reprod., 49: 228-232.
Tesfaye, D; Ghanem, N; Carter, F; Fair, T; Sirard, MA; Hoelker, M; Schellander, K and Lonergan, P (2009). Gene expression profile of cumulus cells derived from
cumulus-oocyte complexes matured either in vivo or in vitro. Reprod. Fertil. Dev., 21: 451-461.
Xi, G; An, L; Jia, Z; Tan, K; Zhang, J; Wang, Z; Zhang, C; Miao, K; Wu, Z and Tian, J (2018). Natriuretic peptide receptor 2 (NPR2) localized in bovine oocyte underlies a unique mechanism for C-type natriuretic peptide (CNP)-induced meiotic arrest. Theriogenology. 106: 198-209.
Zavareh, S; Karimi, I; Salehnia, M and Rahnama, A (2016). Effect of in vitro maturation technique and alpha lipoic acid supplementation on oocyte maturation rate: focus on oxidative status of oocytes. Int. J. Fertil. Steril., 9: 442-451.
Zeng, HT; Richani, D; Sutton-McDowall, ML; Ren, Z; Smitz, JE; Stokes, Y; Gilchrist, RB and Thompson, JG (2014). Prematuration with cyclic adenosine mono-phosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol. Reprod., 91: 47.
Zhang, W; Chen, Q; Yang, Y; Liu, W; Zhang, M; Xia, G and Wang, C (2014). Epidermal growth factor-network signaling mediates luteinizing hormone regulation of BNP and CNP and their receptor NPR2 during porcine oocyte meiotic resumption. Mol. Reprod. Dev., 81: 1030-1041.
Zhang, M; 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: 366-369.
Zhou, P; Wu, YG; Li, Q; Lan, GC; Wang, G; Gao, D and Tan, JH (2008). The interactions between cysteamine, cystine and cumulus cells increase the intracellular glutathione level and developmental capacity of goat cumulus-denuded oocytes. Reproduction. 135: 605-611.