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N-Acetyl cysteine reduces the levels of reactive oxygen species and improves in vitro maturation of oocytes from medium-sized bovine antral follicles

Published online by Cambridge University Press:  23 September 2022

Laryssa G. Barrozo ,
Bianca R. Silva ,
Laís R.F.M. Paulino ,
Efigênia C. Barbalho ,
Danisvânia R. Nascimento ,
Francisco C. Costa ,
Ana L.P.S. Batista ,
Everton P.F. Lopes ,
Ana P.R. Rodrigues  and
José R.V. Silva Open the ORCID record for José R.V. Silva [Opens in a new window]
Laryssa G. Barrozo
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Bianca R. Silva
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Laís R.F.M. Paulino
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Efigênia C. Barbalho
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Danisvânia R. Nascimento
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Francisco C. Costa
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Ana L.P.S. Batista
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
Everton P.F. Lopes
Affiliation:
Faculty of Veterinary Medicine, Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), State University of Ceará, Fortaleza, CE, Brazil
Ana P.R. Rodrigues
Affiliation:
Faculty of Veterinary Medicine, Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), State University of Ceará, Fortaleza, CE, Brazil
José R.V. Silva*
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil
*
Author for correspondence: José R.V. Silva. Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Maurocélio Rocha Ponte 100, 62041–040, Sobral, CE, Brazil. E-mail: jrvsilva@ufc.br
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Summary

This study aims to evaluate the effects of N-acetylcysteine (NAC) on bovine oocyte maturation, mitochondrial activity and transzonal projections (TZP), as well as on the levels of reactive oxygen species (ROS) and messenger RNA (mRNA) for catalase (CAT) superoxide dismutase (SOD), periredoxin-6 (Prdx6), glutathione peroxidase (GPx), growth and differentiation factor-9 (GDF9), histone H1Foo, cyclin B1 (CCNB1) and c-Mos. Bovine cumulus–oocyte complexes (COC) of medium-sized antral follicles (3.0–6.0 mm) were prematured in TCM-199 for 8 h at 38.5°C in 5% CO2. After prematuration in the presence of forskolin and C-type natriuretic peptide, COCs were matured in TCM-199 alone or with 0.1, 0.5 or 2.5 mM NAC. Then, oocytes were classified according to the stage of chromatin. Furthermore, mitochondrial activity and intracellular levels of ROS and TZP were also evaluated. The levels of mRNAs for CAT, SOD, Prdx6, GPx, GDF9, H1Foo, CCNB1 and c-Mos were evaluated using real-time polymerase chain reaction (RT-PCR). The results showed that NAC significantly increased the percentages of oocytes with resumption of meiosis when compared with those oocytes matured in control medium. Oocytes had homogeneous mitochondrial distribution, and those cultured with 0.1 and 0.5 mM NAC had lower levels of ROS when compared with the control. In addition, 0.5 mM NAC reduced TZP and the levels of mRNA for CCNB1. In contrast, NAC did not influence the expression of CAT, GPx, Prdx6, SOD, GDF9, H1Foo, and c-Mos. In conclusion, 0.5 mM NAC reduced the levels of ROS, TZP and mRNA for CCNB1, and improved in vitro resumption of meiosis in oocytes from medium-sized bovine antral follicles.

Keywords

AntioxidantsmRNAOocyte maturationROS
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 882 - 890
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abbassi, L., El-Hayek, S., Carvalho, K. F., Wang, W., Yang, Q., Granados-Aparici, S., Mondadori, R., Bordignon, V. and Clarke, H. J. (2021). Epidermal growth factor receptor signaling uncouples germ cells from the somatic follicular compartment at ovulation. Nature Communications, 12(1), 1438. doi: 10.1038/s41467-021-21644-z CrossRefGoogle ScholarPubMed
Atkuri, K. R., Mantovani, J. J., Herzenberg, L. A. and Herzenberg, L. A. (2007). N-acetylcysteine—A safe antidote for cysteine/glutathione deficiency. Current Opinion in Pharmacology, 7(4), 355–359. doi: 10.1016/j.coph.2007.04.005 CrossRefGoogle ScholarPubMed
Barrozo, L. G., Paulino, L. R. F. M., Silva, B. R., Barbalho, E. C., Nascimento, D. R., Neto, M. F. L. and Silva, J. R. V. (2021). N-acetyl-cysteine and the control of oxidative stress during in vitro ovarian follicle growth, oocyte maturation, embryo development and cryopreservation. Animal Reproduction Science, 231, 106801. doi: 10.1016/j.anireprosci.2021.106801 CrossRefGoogle ScholarPubMed
Bezerra, F. T. G., Silva, A. W. B., Rissi, V. B., Rosa, P. A., Cesaro, M. P., Costa, J. J. N., Gonçalves, P. B. D. and Silva, J. R. V. (2016). Cilostamide and follicular hemisections inhibit oocyte meiosis resumption and regulate gene expression and cAMP levels in bovine cumulus–oocyte complexes. Livestock Science, 184, 112–118. doi: 10.1016/j.livsci.2015.12.014 CrossRefGoogle Scholar
Bezerra, F. T. G., Lima, F. E. O., Paulino, L. R. F. M., Silva, B. R., Silva, A. W. B., Souza, A. L. P., van den Hurk, R. and Silva, J. R. V. (2019). In vitro culture of secondary follicles and prematuration of cumulus–oocyte complexes from antral follicles increase the levels of maturation-related transcripts in bovine oocytes. Molecular Reproduction and Development, 86(12), 1874–1886. doi: 10.1002/mrd.23284 CrossRefGoogle ScholarPubMed
Bezerra, F. T. G., Dau, A. M. P., Van Den Hurk, R. and Silva, J. R. V. (2021). Molecular characteristics of oocytes and somatic cells of follicles at different sizes that influence in vitro oocyte maturation and embryo production. Domestic Animal Endocrinology, 74, 106485. doi: 10.1016/j.domaniend.2020.106485 CrossRefGoogle ScholarPubMed
Biase, F. H. and Kimble, K. M. (2018). Functional signaling and gene regulatory networks between the oocyte and the surrounding cumulus cells. BMC Genomics, 19(1), 351. doi: 10.1186/s12864-018-4738-2 CrossRefGoogle ScholarPubMed
Brand, M. D., Orr, A. L., Perevoshchikova, I. V. and Quinlan, C. L. (2013). The role of mitochondrial function and cellular bioenergetics in ageing and disease. British Journal of Dermatology, 169, Suppl. 2, 1–8. doi: 10.1111/bjd.12208 CrossRefGoogle ScholarPubMed
Cajas, Y. N., Cañón-Beltrán, K., Ladrón de Guevara, M., Millán de la Blanca, M. G., Ramos-Ibeas, P., Gutiérrez-Adán, A., Rizos, D. and González, E. M. (2020). Antioxidant nobiletin enhances oocyte maturation and subsequent embryo development and quality. International Journal of Molecular Sciences, 21(15), e5340. doi: 10.3390/ijms21155340 CrossRefGoogle ScholarPubMed
de Vantéry, C., Gavin, A. C., Vassalli, J. D. and Schorderet-Slatkine, S. (1996). An accumulation of P34cdc2at the end of mouse oocyte growth correlates with the acquisition of meiotic competence. Developmental Biology, 174(2), 335–344. doi: 10.1006/dbio.1996.0078 CrossRefGoogle Scholar
Dieci, C., Lodde, V., Labreque, R., Dufort, I., Tessaro, I., Sirard, M. A. and Luciano, A. M. (2016). Differences in cumulus cell gene expression indicate the benefit of a prematuration step to improve in vitro bovine embryo production. Molecular Human Reproduction, 22(12), 882–897. doi: 10.1093/molehr/gaw055 Google Scholar
Dumollard, R., Duchen, M. and Sardet, C. (2006). Calcium signals and mitochondria at fertilisation. Seminars in Cell and Developmental Biology, 17(2), 314–323. doi: 10.1016/j.semcdb.2006.02.009 CrossRefGoogle ScholarPubMed
Ferreira, E. M., Vireque, A. A., Adona, P. R., Meirelles, F. V., Ferriani, R. A. and Navarro, P. A. (2009). Cytoplasmic maturation of bovine oocytes: Structural and biochemical modifications and acquisition of developmental competence. Theriogenology, 71(5), 836–848. doi: 10.1016/j.theriogenology.2008.10.023 CrossRefGoogle ScholarPubMed
Fisher, A. B., Vasquez-Medina, J. P., Dodia, C., Sorokina, E. M., Tao, J. Q. and Feinstein, S. I. (2018). Peroxiredoxin 6 phospholipid hydroperoxidase activity in the repair of peroxidized cell membranes. Redox Biology, 14, 41–46. doi: 10.1016/j.redox.2017.08.008 CrossRefGoogle ScholarPubMed
Fu, G., Ghadam, P., Sirotkin, A., Khochbin, S., Skoultchi, A. I. and Clarke, H. J. (2003). Mouse oocytes and early embryos express multiple histone H1 subtypes. Biology of Reproduction, 68(5), 1569–1576. doi: 10.1095/biolreprod.102.012336 CrossRefGoogle ScholarPubMed
Furuya, M., Tanaka, M., Teranishi, T., Matsumoto, K., Hosoi, Y., Saeki, K., Ishimoto, H., Minegishi, K., Iritani, A. and Yoshimura, Y. (2007). H1foo is indispensable for meiotic maturation of the mouse oocyte. Journal of Reproduction and Development, 53(4), 895–902. doi: 10.1262/jrd.19008 CrossRefGoogle ScholarPubMed
Gui, L. M. and Joyce, I. M. (2005). RNA interference evidence that growth differentiation factor-9 mediates oocyte regulation of cumulus expansion in mice. Biology of Reproduction, 72(1), 195–199. doi: 10.1095/biolreprod.104.033357 CrossRefGoogle ScholarPubMed
Güntürk, I., Yazici, C., Köse, S. K., Dağli, F., Yücel, B. and Yay, A. H. (2019). The effect of N-acetylcysteine on inflammation and oxidative stress in cisplatin-induced nephrotoxicity: A rat model. Turkish Journal of Medical Sciences, 49(6), 1789–1799. doi: 10.3906/sag-1903-225 Google ScholarPubMed
Hyttel, P., Greve, T. and Callesen, H. (1989). Ultrastructural aspects of oocyte maturation and fertilization in cattle. Journal of Reproduction and Fertility. Supplement, 38, 35–47.Google ScholarPubMed
Jaffe, L. A. and Egbert, J. R. (2017). Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Annual Review of Physiology, 79, 237–260. doi: 10.1146/annurev-physiol-022516-034102 CrossRefGoogle ScholarPubMed
Kala, M., Shaikh, M. V. and Nivsarkar, M. (2016). Equilibrium between anti-oxidants and reactive oxygen species: A requisite for oocyte development and maturation. Reproductive Medicine and Biology, 16(1), 28–35. doi: 10.1002/rmb2.12013 CrossRefGoogle ScholarPubMed
Lequarre, A. S., Vigneron, C., Ribaucour, F., Holm, P., Donnay, I., Dalbiès-Tran, R., Callesen, H. and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology, 63(3), 841–859. doi: 10.1016/j.theriogenology.2004.05.015 CrossRefGoogle ScholarPubMed
Li, Q. and Zhao, Z. (2019). Influence of N-acetyl-l-cysteine against bisphenol A on the maturation of mouse oocytes and embryo development: In vitro study. BMC Pharmacology and Toxicology, 20(1), 43. doi: 10.1186/s40360-019-0323-9 CrossRefGoogle ScholarPubMed
Lima, F. E. O., Bezerra, F. T. G., Souza, G. B., Matos, M. H. T., van den Hurk, R. and Silva, J. R. V. (2018). Influence of interleukin 1 beta and tumour necrosis factor alpha on the in vitro growth, maturation and mitochondrial distribution of bovine oocytes from small antral follicles. Zygote, 26(5), 381–387. doi: 10.1017/S0967199418000382 CrossRefGoogle ScholarPubMed
Livak, K. J. and 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(4), 402–408. doi: 10.1006/meth.2001.1262 CrossRefGoogle ScholarPubMed
Lonergan, P. and Fair, T. (2008). In vitro-produced bovine embryos: Dealing with the warts. Theriogenology, 69(1), 17–22. doi: 10.1016/j.theriogenology.2007.09.007 CrossRefGoogle ScholarPubMed
Lopes, E. P. F., Rodrigues, G. Q., de Brito, D. C. C., Rocha, R. M. P., Ferreira, A. C. A., de Sá, N. A. R., Silva, R. F. D., de Alcântara, G. L. H., Alves, B. G., Figueiredo, J. R., Zelinski, M. and Rodrigues, A. P. R. (2020). Vitrification of caprine secondary and early antral follicles as a perspective to preserve fertility function. Reproductive Biology, 20(3), 371–378. doi: 10.1016/j.repbio.2020.05.001 CrossRefGoogle ScholarPubMed
Luciano, A. M., Franciosi, F., Modina, S. C. and Lodde, V. (2011). Gap junction mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biology of Reproduction, 85(6), 1252–1259. doi: 10.1095/biolreprod.111.092858 CrossRefGoogle Scholar
Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M. A., Clarke, H. J., Khandjian, É. W., Richard, F. J., Hyttel, P. and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biology of Reproduction, 91(4), 90. doi: 10.1095/biolreprod.114.119867 CrossRefGoogle Scholar
Mahmoodi, M., Soleimani Mehranjani, M. S., Shariatzadeh, S. M. A., Eimani, H. and Shahverdi, A. (2015). N-acetylcysteine improves function and follicular survival in mice ovarian grafts through inhibition of oxidative stress. Reproductive Biomedicine Online, 30(1), 101–110. doi: 10.1016/j.rbmo.2014.09.013 CrossRefGoogle ScholarPubMed
Mastrorocco, A., Cacopardo, L., Martino, N. A., Fanelli, D., Camillo, F., Ciani, E., Roelen, B. A. J., Ahluwalia, A. and Dell’Aquila, M. E. (2020). One-step automated bioprinting-based method for cumulus–oocyte complex microencapsulation for 3D in vitro maturation. PLOS ONE, 15(9), e0238812. doi: 10.1371/journal.pone.0238812 CrossRefGoogle ScholarPubMed
Phillips, K. P., Petrunewich, M. A., Collins, J. L., Booth, R. A., Liu, X. J. and Baltz, J. M. (2002). Inhibition of MEK or cdc2 kinase parthenogenetically activates mouse eggs and yields the same phenotypes as Mos parthenogenotes. Developmental Biology, 247(1), 210–223. doi: 10.1006/dbio.2002.0680 CrossRefGoogle ScholarPubMed
Romek, M., Gajda, B., Rolka, M. and Smorąg, Z. (2011). Mitochondrial activity and morphology in developing porcine oocytes and pre-implantation non-cultured and cultured embryos. Reproduction in Domestic Animals, 46(3), 471–480. doi: 10.1111/j.1439-0531.2010.01691.x CrossRefGoogle ScholarPubMed
Sovernigo, T. C., Adona, P. R., Monzani, P. S., Guemra, S., Barros, F., Lopes, F. G. and Leal, C. L. V. (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reproduction in Domestic Animals, 52(4), 561–569. doi: 10.1111/rda.12946 CrossRefGoogle ScholarPubMed
Sun, W. S., Jang, H., Park, M. R., Oh, K. B., Lee, H., Hwang, S., Xu, L. J., Hwang, I. S. and Lee, J. W. (2021). N-acetyl-L-cysteine improves the developmental competence of bovine oocytes and embryos cultured in vitro by attenuating oxidative damage and apoptosis. Antioxidants, 10(6), 1–15. doi: 10.3390/antiox10060860 CrossRefGoogle ScholarPubMed
Takahashi, Y., Hashimoto, S., Yamochi, T., Goto, H., Yamanaka, M., Amo, A., Matsumoto, H., Inoue, M., Ito, K., Nakaoka, Y., Suzuki, N. and Morimoto, Y. (2016). Dynamic changes in mitochondrial distribution in human oocytes during meiotic maturation. Journal of Assisted Reproduction and Genetics, 33(7), 929–938. doi: 10.1007/s10815-016-0716-2 CrossRefGoogle ScholarPubMed
Wang, Q., Hou, Y., Yi, D., Wang, L., Ding, B., Chen, X., Long, M., Liu, Y. and Wu, G. (2013). Protective effects of N-acetylcysteine on acetic acid-induced colitis in a porcine model. BMC Gastroenterology, 13, 133. doi: 10.1186/1471-230X-13-133 CrossRefGoogle ScholarPubMed
Whitaker, B. D., Casey, S. J. and Taupier, R. (2012). The effects of N-acetyl-l-cysteine supplementation on in vitro porcine oocyte maturation and subsequent fertilisation and embryonic development. Reproduction, Fertility, and Development, 24(8), 1048–1054. doi: 10.1071/RD12002 CrossRefGoogle ScholarPubMed
Wu, B., Ignotz, G., Currie, W. B. and Yang, X. (1997). Dynamics of maturation-promoting factor and its constituent proteins during in vitro maturation of bovine oocytes. Biology of Reproduction, 56(1), 253–259. doi: 10.1095/biolreprod56.1.253 CrossRefGoogle ScholarPubMed
Yun, Y., An, P., Ning, J., Zhao, G. M., Yang, W. L., and Lei, A. M. (2015). H1foo is essential for in vitro meiotic maturation of bovine oocytes. Zygote, 23(3), 416–425. doi: 10.1017/S0967199414000021 CrossRefGoogle ScholarPubMed