Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T22:15:38.008Z Has data issue: false hasContentIssue false
  • English
  • Français

Follicular development, morphological integrity, and oxidative stress in bovine preantral follicles cultured in vitro with ascorbic acid

Published online by Cambridge University Press:  02 December 2021

Larissa Zamparone Bergamo Open the ORCID record for Larissa Zamparone Bergamo [Opens in a new window] ,
Denis Vinicius Bonato ,
Camila Bizarro-Silva Open the ORCID record for Camila Bizarro-Silva [Opens in a new window] ,
Francieli Gesleine Capote Bonato ,
Tamires Korchovei Sanches ,
Marcela Bortoletto Cerezetti ,
Ana Carolina Rossaneis ,
Waldiceu A. Verri Jr ,
Fábio Morotti  and
Marcelo Marcondes Seneda
Larissa Zamparone Bergamo*
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil Department of Veterinary Sciences, Federal University of Parana, Palotina, Parana, Brazil
Denis Vinicius Bonato
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil Paranaense University, Umuarama, Parana, Brazil
Camila Bizarro-Silva
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil Animal Reproduction Laboratory, School of Life Sciences; Pontifical Catholic University of Parana; Toledo, Parana, Brazil
Francieli Gesleine Capote Bonato
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil
Tamires Korchovei Sanches
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil
Marcela Bortoletto Cerezetti
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil
Ana Carolina Rossaneis
Affiliation:
Department of Pathological Sciences; Biological Sciences Center; State University of Londrina; Londrina, Parana, Brazil
Waldiceu A. Verri Jr
Affiliation:
Department of Pathological Sciences; Biological Sciences Center; State University of Londrina; Londrina, Parana, Brazil
Fábio Morotti
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil
Marcelo Marcondes Seneda
Affiliation:
Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil
*
Author for correspondence: Larissa Zamparone Bergamo. Laboratory of Biotechnology of Animal Reproduction; Department of Veterinary Clinics; Center of Agrarian Sciences; State University of Londrina; Londrina, Parana, Brazil. Tel: +55 43 99915 6521. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to evaluate the follicular development, morphological integrity, and oxidative stress of preantral ovarian follicles from Bos taurus indicus females grown in vitro with ascorbic acid. Ovaries (n = 20) from Bos taurus indicus females were collected, fragmented, and were cultured in vitro for 6 or 12 days in minimum essential medium (MEM), or MEM supplemented with 50 or 100 ng/ml ascorbic acid, with an extracellular matrix of agarose gel, in an incubator at 38.5°C; every 2 days, 100% of the culture medium was replaced. The data were analyzed using the chi-squared test and/or Fisher’s exact test. In the event of a significant effect, the proportions were compared using a 2 × 2 proportion test. The oxidative stress analysis data were submitted to analysis of variance followed by the Bonferroni test. Values were considered significant when P ≤ 0.05. The addition of 100 ng/ml of ascorbic acid to the in vitro culture medium of preantral ovarian follicles from bovine females promoted follicular development, was efficient in maintaining morphological integrity, as well as the stability of reactive oxygen species, after 6 days of in vitro culture.

Keywords

Bos taurus indicusFRAPNBTReactive oxygen speciesTBARS
Type
Research Article
Information
Zygote , Volume 30 , Issue 3 , June 2022 , pp. 391 - 397
Copyright
© The Author(s), 2021. 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.)

References

Abdollahifar, MA, Azad, N, Sajadi, E, Shams Mofarahe, ZS, Zare, F, Moradi, A, Rezaee, F, Gholamin, M and Abdi, S (2019). Vitamin C restores ovarian follicular reservation in a mouse model of aging. Anat Cell Biol 52, 196–203.CrossRefGoogle Scholar
Andrade, ER, van den Hurk, R, Lisboa, LA, Hertel, MF, Melo-Sterza, FA, Moreno, K, Bracarense, APFRL, Landim-Alvarenga, FC, Seneda, MM and Alfieri, AA (2012). Effects of ascorbic acid on in vitro culture of bovine preantral follicles. Zygote 20, 379–88.CrossRefGoogle ScholarPubMed
Araújo, VR, Gastal, MO, Figueiredo, JR and Gastal, EL (2014). In vitro culture of bovine preantral follicles: a review. Reprod Biol Endocrinol 12, 78.CrossRefGoogle ScholarPubMed
Ayres, H, Ferreira, RM, de Souza Torres-Júnior, JR, Demétrio, CGB, de Lima, CG and Baruselli, PS (2009). Validation of body condition score as a predictor of subcutaneous fat in Nelore (Bos indicus). cows. Livest Sci 123, 175–9.CrossRefGoogle Scholar
Barja, G, López-Torres, M, Pérez-Campo, R, Rojas, C, Cadenas, S, Prat, J and Pamplona, R (1994). Dietary vitamin C decreases endogenous protein oxidative damage, malondialdehyde, and lipid peroxidation and maintains fatty acid unsaturation in the guinea pig liver. Free Radic Biol Med 17, 105–15.CrossRefGoogle ScholarPubMed
Bizarro-Silva, C, Santos, MM, Gerez, JR, González, SM, Lisboa, LA and Seneda, MM (2018). Influence of follicle-stimulating hormone concentrations on the integrity and development of bovine follicles cultured in vitro . Zygote 26, 417–23.CrossRefGoogle ScholarPubMed
Búfalo, I, González, SM, Silva, CB, Lindquist, AG, Bergamo, LZ, Costa, CB, Marinho, LSR and Seneda, MM (2016). Efeito do tipo de fixador e tempo de fixação na morfologia de folículos pré-antrais equinos. Sem Ci Agr 37, 243–50.CrossRefGoogle Scholar
de Sá, NAR, Ferreira, ACA, Sousa, FGC, Duarte, ABG, Paes, VM, Cadenas, J, Anjos, JC, Fernandes, CCL, Rosseto, R, Cibin, FWS, Alves, BG, Rodrigues, APR, Rondina, D, Gastal, EL and Figueiredo, JR (2020). First pregnancy after in vitro culture of early antral follicles in goats: positive effects of anethole on follicle development and steroidogenesis. Mol Reprod Dev 87, 966–77.Google ScholarPubMed
Figueiredo JRd de Lima LFd Silva JRV and Santos, RR (2018). Control of growth and development of preantral follicle: insights from in vitro culture. Anim Reprod 15, 648–59.Google Scholar
Frydman, R and Grynberg, M (2016). Introduction: female fertility preservation: innovations and questions. Fertil Steril 105, 4–5.CrossRefGoogle ScholarPubMed
Gomes, RG, Lisboa, LA, Silva, CB, Max, MC, Marino, PC, Oliveira, RL, González, SM, Barreiros, TRR, Marinho, LSR and Seneda, MM (2015). Improvement of development of equine preantral follicles after 6 days of in vitro culture with ascorbic acid supplementation. Theriogenology 84, 750–5.CrossRefGoogle ScholarPubMed
Gomes, RG, Silva, CB, González, SM, Oliveira, RL, Max, MC, Lisboa, LA, Barreiros, TRR, Santos, MM, Sarapião, FD, Gastal, EL and Seneda, MM (2018). Alpha lipoic acid (ALA). effects on developmental competence of equine preantral follicles in short-term culture. Theriogenology 105, 169–73.CrossRefGoogle ScholarPubMed
He, Y, Meng, K, Wang, X, Dong, Z, Zhang, Y and Quan, F (2020). Comparison of bovine small antral follicle development in two- and three-dimensional culture systems. An Acad Bras Cienc 92, e20180935.CrossRefGoogle ScholarPubMed
Lutsenko, EA, Cárcamo, JM and Golde, DW (2002). Vitamin C prevents DNA mutation induced by oxidative stress. J Biol Chem 277, 16895–9.CrossRefGoogle ScholarPubMed
Matsuda, F, Inoue, N, Manabe, N and Ohkura, S (2012). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev 58, 44–50.CrossRefGoogle ScholarPubMed
Max, MC, Bizarro-Silva, C, Búfalo, I, González, SM, Lindquist, AG, Gomes, RG, Barreiros, TRR, Lisboa, LA, Morotti, F and Seneda, MM (2018). In vitro culture supplementation of EGF for improving the survival of equine preantral follicles. In Vitro Cell Dev Biol Anim 54, 687–91.CrossRefGoogle ScholarPubMed
Melo, MA, Oskam, IC, Celestino, JJ, Carvalho, AA, Castro, SV, Figueiredo, JR, Rodrigues, AP and Santos, RR (2011). Adding ascorbic acid to vitrification and IVC medium influences preantral follicle morphology, but not viability. Reprod Domest Anim 46, 742–5.CrossRefGoogle Scholar
Murray, AA, Molinek, MD, Baker, SJ, Kojima, FN, Smith, MF, Hillier, SG and Spears, N (2001). Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro . Reproduction 121, 89–96.CrossRefGoogle ScholarPubMed
Packer, L, Witt, EH and Tritschler, HJ (1995). Alpha-lipoic acid as a biological antioxidant. Free Radic Biol Med 19, 227–50.CrossRefGoogle ScholarPubMed
Pinho-Ribeiro, FA, Zarpelon, AC, Mizokami, SS, Borghi, SM, Bordignon, J, Silva, RL, Cunha, TM, Alves-Filho, JC, Cunha, FQ, Casagrande, R and Verri, WA Jr (2016). The citrus flavonone naringenin reduces lipopolysaccharide-induced inflammatory pain and leukocyte recruitment by inhibiting NF-κB activation. J Nutr Biochem 33, 8–14.CrossRefGoogle ScholarPubMed
Sato, T, Katagiri, K, Gohbara, A, Inoue, K, Ogonuki, N, Ogura, A, Kubota, Y and Ogawa, T (2011). In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471, 504–7.CrossRefGoogle ScholarPubMed
Silva, AWB, Ribeiro, RP, Menezes, VG, Barberino, RS, Passos, JRS, Dau, AMP, Costa, JJN, Melo, LRF, Bezerra, FTG, Donato, MAM, Peixoto, CA, Matos, MHT, Gonçalves, PBD, van den Hurk, R and Silva, JRV (2017a). Expression of TNF-α system members in bovine ovarian follicles and the effects of TNF-α or dexamethasone on preantral follicle survival, development and ultrastructure in vitro . Anim Reprod Sci 182, 56–68.CrossRefGoogle ScholarPubMed
Silva, CB, Bergamo, LZ, Búfalo, I, Bonato, DV and Seneda, MM (2017b). Comparison among different systems of in vitro culture of preantral follicles in cattle. Anim Reprod 14, 793.Google Scholar
Silva, G, Araújo, V, Duarte, A, Chaves, R, Silva, C, Lobo, C, Almeida, A, Matos, M, Tavares, L and Campelo, C (2011). Ascorbic acid improves the survival and in vitro growth of isolated caprine preantral follicles. Anim Reprod 8, 14–24.Google Scholar
Thomas, FH, Leask, R, Srsen, V, Riley, SC, Spears, N and Telfer, EE (2001). Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture. Reproduction 122, 487–95.CrossRefGoogle ScholarPubMed