Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T07:26:40.837Z Has data issue: false hasContentIssue false
  • English
  • Français

Culture of preantral ovarian follicles of Bos taurus indicus with alpha-lipoic acid

Published online by Cambridge University Press:  25 August 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 ,
Suellen Miguez González ,
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 Science, 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
Suellen Miguez González
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, 86057-970, Londrina, Parana, Brazil. E-mail: larissabergamo1@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to evaluate follicular development, morphological integrity, and antioxidant potential of preantral ovarian follicles from Bos taurus indicus females grown in vitro with alpha-lipoic acid. Ovaries (n = 24) of Bos taurus indicus (n = 12) females were collected during slaughter and fragmented. A randomly obtained fragment from each pair of ovaries was fixed in Bouin (non-cultivated control; D0). These fragments were intended for classical histology (morphology and evaluation of follicular growth), and a fragment from each pair of ovaries was frozen at −80°C (non-cultivated control; D0), and assigned for analysis of oxidative stress [thiobarbituric acid reactive substances (TBARS), nitroblue tetrazolium (NBT), and ferric reducing antioxidant power (FRAP)]. The remaining fragments were cultured in vitro for 6 (D6) or 12 (D12) days, containing only minimum essential medium (MEM) or MEM supplemented with alpha-lipoic acid (50, 100, or 250 ng/ml), on an extracellular matrix of agarose gel, in an oven at 38.5ºC. Every 2 days, 100% of the culture medium was replaced. Supplementation with 100 ng/ml was effective for maintaining follicular integrity after 6 days of culture (primordial: 51.28%; development: 36.88%; P < 0.0001). There was no difference (P > 0.05) between treatments compared with the non-cultivated control treatment (D0), using the NBT and TBARS assays. Therefore, supplementation of the in vitro culture medium of bovine preantral ovarian follicles with a concentration of 100 ng/ml of alpha-lipoic acid at 6 days of culture was effective for maintaining follicular integrity and, after 6 days, maintaining stable levels of reactive oxygen species.

Keywords

AntioxidantsBovineIn vitro culture of preantral folliclesNeloreROS
Type
Research Article
Information
Zygote , Volume 30 , Issue 2 , April 2022 , pp. 206 - 212
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

Agarwal, A, Gupta, S and Sharma, R (2005). Oxidative stress and its implications in female infertility—a clinician’s perspective. Reprod Biomed Online 11, 641–50.CrossRefGoogle Scholar
Agarwal, A, Gupta, S and Sikka, S (2006). The role of free radicals and antioxidants in reproduction. Curr Opin Obstetr Gynecol 18, 325–32.CrossRefGoogle ScholarPubMed
Andrade, E, Melo-Sterza, F, Seneda, M and Alfieri, A (2010). Consequências da produção das espécies reativas de oxigênio na reprodução e principais mecanismos antioxidantes. Rev Brasil Reprod Anim 34, 79–85.Google Scholar
Andrade, ER, van den Hurk, R, Lisboa, LA, Hertel, MF, Melo-Sterza, FA, Moreno, K, Bracarense, AP, 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.Google 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(2–3), 175–9.CrossRefGoogle Scholar
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.Google ScholarPubMed
Blondin, P, Coenen, K and Sirard, MA (1997). The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J Androl 18, 454–60.Google ScholarPubMed
Búfalo, I, González, SM, da Silva, CB, Lindquist, AG, Bergamo, LZ, Costa, CB, Marinho, LSR and Seneda, MM (2016). Effect of fixative type and fixation time on the morphology of equine preantral ovarian follicles. Semina: Cienc Agrar 37, 243–50.Google Scholar
Cakatay, U (2006). Pro-oxidant actions of alpha-lipoic acid and dihydrolipoic acid. Med Hypotheses 66, 110–7.Google ScholarPubMed
Combelles, CM, Gupta, S and Agarwal, A (2009). Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online 18, 864–80.CrossRefGoogle ScholarPubMed
de Sá, NAR, Ferreira, ACA, Sousa, FGC, Duarte, ABG, Paes, VM, Cadenas, J (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(Suppl. 1), 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, TR, Marinho, LS 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
Goto, Y, Noda, Y, Narimoto, K, Umaoka, Y and Mori, T (1992). Oxidative stress on mouse embryo development in vitro . Free Radical Biol Med 13, 47–53.Google ScholarPubMed
Green, LJ and Shikanov, A (2016). In vitro culture methods of preantral follicles. Theriogenology 86, 229–38.CrossRefGoogle ScholarPubMed
Halliwell, B and Gutteridge, JM (1988). Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 7, 7–13.CrossRefGoogle ScholarPubMed
Hatami, S, Zavareh, S, Salehnia, M, Lashkarbolouki, T and Karimi, I (2014). Comparison of oxidative status of mouse pre-antral follicles derived from vitrified whole ovarian tissue and vitrified pre-antral follicles in the presence of alpha lipoic acid. J Obstet Gynaecol Res 40, 1680–8.CrossRefGoogle ScholarPubMed
Hatzirodos, N, Hummitzsch, K, Irving-Rodgers, HF, Harland, ML, Morris, SE and Rodgers, RJ (2014). Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia. BMC Genomics 15, 40.CrossRefGoogle ScholarPubMed
Langbeen, A, De Porte, HF, Bartholomeus, E, Leroy, JL and Bols, PE (2015). Bovine in vitro reproduction models can contribute to the development of (female) fertility preservation strategies. Theriogenology 84, 477–89.Google Scholar
Marsh, SA, Pat, BK, Gobe, GC and Coombes, JS (2005). Evidence for a non-antioxidant, dose-dependent role of alpha-lipoic acid in caspase-3 and ERK2 activation in endothelial cells. Apoptosis 10, 657–65.Google 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.Google ScholarPubMed
Moini, H, Packer, L and Saris, NE (2002). Antioxidant and prooxidant activities of alpha-lipoic acid and dihydrolipoic acid. Toxicol Appl Pharmacol 182, 84–90.Google ScholarPubMed
Packer, L, Witt, EH and Tritschler, HJ (1995). Alpha-lipoic acid as a biological antioxidant. Free Radical Biol Med 19, 227–50.Google 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.Google 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 (2017). 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-Santos, KC, Santos, GM, Siloto, LS, Hertel, MF, Andrade, ER, Rubin, MI, Sturion, L, Melo-Sterza, FA and Seneda, MM (2011). Estimate of the population of preantral follicles in the ovaries of Bos taurus indicus and Bos taurus taurus cattle. Theriogenology 76, 1051–7.CrossRefGoogle ScholarPubMed
Talebi, A, Zavareh, S, Kashani, MH, Lashgarbluki, T and Karimi, I (2012). The effect of alpha lipoic acid on the developmental competence of mouse isolated preantral follicles. J Assist Reprod Genet 29, 175–83.CrossRefGoogle ScholarPubMed
Wenzel, U, Nickel, A and Daniel, H (2005). Alpha-lipoic acid induces apoptosis in human colon cancer cells by increasing mitochondrial respiration with a concomitant O2−*-generation. Apoptosis 10, 359–68.CrossRefGoogle ScholarPubMed
Zoheir, KM, Harisa, GI, Allam, AA, Yang, L, Li, X, Liang, A, Abd-Rabou, AA and Harrath, AH (2017). Effect of alpha lipoic acid on in vitro development of bovine secondary preantral follicles. Theriogenology 88, 124–30.Google ScholarPubMed
Supplementary material: PDF

Bergamo et al. supplementary material

Bergamo et al. supplementary material 1

Download Bergamo et al. supplementary material(PDF)
PDF 58.3 KB
Supplementary material: File

Bergamo et al. supplementary material

Bergamo et al. supplementary material 2

Download Bergamo et al. supplementary material(File)
File 14.5 KB