Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T08:26:18.921Z Has data issue: false hasContentIssue false
  • English
  • Français

Culture of goat preantral follicles in situ associated with mesenchymal stem cell from bone marrow

Published online by Cambridge University Press:  18 November 2019

Camila Arrivabene Neves ,
Lucilene dos Santos Silva ,
Camila Ernanda Sousa de Carvalho ,
Marina Silva Carvalho ,
José Lindenberg Rocha Sarmento ,
Tânia Vasconcelos Cavalcante ,
Mônica Arrivabene ,
Tábatta Arrivabene Neves ,
Maria Éllida de Sousa Bezerra  and
Antônio Luiz Gomes Júnior
...Show all authors
Camila Arrivabene Neves
Affiliation:
Federal University of Piauí, Integrated Nucleus of Morphology and Stem Cell Research (NUPCelt), Teresina, PI, Brazil
Lucilene dos Santos Silva
Affiliation:
Federal University of Piauí, Integrated Nucleus of Morphology and Stem Cell Research (NUPCelt), Teresina, PI, Brazil
Camila Ernanda Sousa de Carvalho
Affiliation:
Federal University of Piauí, Integrated Nucleus of Morphology and Stem Cell Research (NUPCelt), Teresina, PI, Brazil Federal University of Piauí, Agricultural Science Centre, Teresina, PI, Brazil
Marina Silva Carvalho
Affiliation:
Federal University of Piauí, Integrated Nucleus of Morphology and Stem Cell Research (NUPCelt), Teresina, PI, Brazil
José Lindenberg Rocha Sarmento
Affiliation:
Federal University of Piauí, Agricultural Science Centre, Teresina, PI, Brazil
Tânia Vasconcelos Cavalcante
Affiliation:
Federal University of Piauí, Agricultural Science Centre, Teresina, PI, Brazil
Mônica Arrivabene
Affiliation:
Federal University of Piauí, Agricultural Science Centre, Teresina, PI, Brazil
Tábatta Arrivabene Neves
Affiliation:
Federal University of Piauí, Agricultural Science Centre, Teresina, PI, Brazil
Maria Éllida de Sousa Bezerra
Affiliation:
San Francisco Valley Federal University, Nucleus of Biotechnology Applied to the Development of Ovarian Follicles, Petrolina, PE, Brazil
Antônio Luiz Gomes Júnior
Affiliation:
Federal University of Piauí, Health Science Centre, Teresina, PI, Brazil
Cleidson Manoel Gomes da Silva*
Affiliation:
Federal University of South and Southeast of Pará, Institute of Studies of the Humid Tropics, Xinguara, PA, Brazil
Maria Acelina Martins de Carvalho
Affiliation:
Federal University of Piauí, Integrated Nucleus of Morphology and Stem Cell Research (NUPCelt), Teresina, PI, Brazil
*
Author for correspondence: Cleidson Manoel Gomes da Silva, Federal University of South and Southeast of Pará, Institute of Studies of the Humid Tropics, Street Alberto Santos Dumont, s/n. Xinguara – PA. Brazil. CEP 68557-335. Tel: +55 94 2101 5934. E-mail: gomesvet@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

This study aims to develop an in vitro co-culture system of in situ goat preantral follicles with bone marrow-derived mesenchymal stem cells (BM-MSC), evaluating the influence of these cells on follicular growth, rate of activation and morphologically normal follicles. Fragments of ovarian cortex were cultured for 1 or 7 days in the presence of BM-MSC (BM-MSC+) and absence of BM-MSC (BM-MSC−). Histological sections of the fragments were analysed and data were obtained regarding morphological classification, survival rate of morphologically normal follicles and rate of follicular activation. Culture medium on days 1 and 7 was also sampled for nitrite concentration and reduced glutathione activity. There was a reduction (P < 0.05) in the percentage of morphologically normal follicles in the BM-MSC+ compared with the fresh control only on the seventh day of culture. When comparing treatments, on the seventh day of culture, a higher rate of morphologically normal preantral follicles was observed in BM-MSC+ (P < 0.05). In both treatments, primordial and developing follicle rates were similar to the fresh control (P > 0.05). When comparing treatments with each other, as well as with the fresh control, no differences were observed in follicular diameter (P > 0.05) or nitrite concentration (P > 0.05). The concentration of reduced glutathione was lower on the seventh day of co-culture in both treatments (P < 0.05). In conclusion, co-culture had no influence on follicular or oocyte development. However, it was critical to maintain the survival of preantral follicles during 7 days of culture.

Keywords

Co-cultureGlutathioneGoatNitriteOvary
Type
Research Article
Information
Zygote , Volume 28 , Issue 1 , February 2020 , pp. 65 - 71
Copyright
© Cambridge University Press 2019 

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

Aguiar, FLN, Lunardi, FO, Lima, LF, Rocha, RMP, Bruno, JB, Magalhães-Padilha, DM, Cibin, FWS, Nunes-Pinheiro, DCS, Gastal, MO, Rodrigues, APR, Apgar, GA, Gastal, EL and Figueiredo, JR (2016) FSH supplementation to culture medium is beneficial for activation and survival of preantral follicles enclosed in equine ovarian tissue. Theriogenology 85, 1106–12.CrossRefGoogle ScholarPubMed
Araújo, VR, Silva, CMG, Magalhães, DM, Silva, GM, Báo, SN, Silva, JRV, Figueiredo, JR and Rodrigues, APR (2010) Effect of bone morphogenetic protein-7 (BMP-7) on in vitro survival of caprine preantral follicles. Pesq Vet Bras 30, 305–10.CrossRefGoogle Scholar
Araújo, VR, Gastal, MO, Figueiredo, JR and Gastal, EL (2014) In vitro culture of bovine preantral follicles: a review. Reprod Biol Endocrinol 12, 1–14.CrossRefGoogle ScholarPubMed
Arunakumari, G, Shanmugasundaram, N and Rao, VH (2010) Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.CrossRefGoogle ScholarPubMed
Bruno, JB, Lima-Verde, IB, Martins, FS, Matos, MHT, Lopes, CAP, Maia, JE, Báo, SN, Nobre Junior, HV, Maia, FD, Pessoa, C, Moraes, MO, Silva, JRV, Figueiredo, JR and Rodrigues, APR (2008) Característica histológica, ultra-estrutural e produção de nitrito de folículos pré-antrais caprinos cultivados in vitro na ausência ou presença de soro. Arq Bras Med Vet e Zootec 60, 1329–37.CrossRefGoogle Scholar
Carreira, AC, Alves, GG, Zambuzzi, WF, Sogayar, MC and Granjeiro, JM (2014) Bone morphogenetic proteins: structure, biological function and therapeutic applications. Arch Biochem Biophys 561, 64–73.CrossRefGoogle ScholarPubMed
Crocomo, LF, Marques Fillho, WC, Landin-Alvarenga, FC and Bicudo, SD (2012) Produção de embriões in vitro: Estresse oxidativo e antioxidantes. Vet e Zootec 19, 470–9.Google Scholar
Fatehi, AN, Van Den Hurk, R, Colenbrander, B, Daemen, AJJM, Van Tol, HTA, Monteiro, RM, Roelen, BAJ and Bevers, MM (2005) Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–89.CrossRefGoogle Scholar
Glister, C, Kemp, CF and Knight, PG (2004) Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: Actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation of follistatin. Reproduction 127, 239–54.CrossRefGoogle ScholarPubMed
Green, LC, Tannenbaum, SR and Goldman, P (1978) Nitrite and nitrate are formed by endogenous synthesis in the human intestine. Science 200, 1487–9.Google Scholar
Green, LJ, Zhou, H and Shikanov, A (2016) Utilization of adipose derived stem cells for the in vitro maturation of primary and early secondary ovarian follicles. Fertil Steril 106, 49.CrossRefGoogle Scholar
Gupta, PSP, Ramesh, HS, Manjunatha, BM, Nandi, S and Ravindra, JP (2008) Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16, 57–63.CrossRefGoogle ScholarPubMed
Itoh, T and Hoshi, H (2000) Efficient isolation and long-term viability of bovine small preantral follicles in vitro . In Vitro Cell Dev Biol Anim 36, 235–40.2.0.CO;2>CrossRefGoogle ScholarPubMed
Kim, HS, Yun, JW, Shin, TH, Lee, SH, Lee, BC, Yu, KR, Seo, Y, Lee, S, Kang, TW, Choi, SW, Seo, KW and Kang, KS (2015) Human umbilical cord blood mesenchymal stem cell-derived PGE2 and TGF-β1 alleviate atopic dermatitis by reducing mast cell degranulation. Stem Cells 33, 1254–66.CrossRefGoogle ScholarPubMed
Kim, WS, Park, BS, and Sung, JH (2009) Protective role of adipose-derived stem cells and their soluble factors in photoaging. Arch Dermatol Res 301, 329–36.CrossRefGoogle ScholarPubMed
Magalhães, DM, Duarte, ABG, Araújo, VR, Brito, IR, Soares, TG, Lima, IMT, Lopes, CAP, Campello, CC, Rodrigues, APR and Figueiredo, JR (2011) In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–8.CrossRefGoogle ScholarPubMed
Miranda, M, Nascimento, H and Costa, M (2016) Increasing of blastocyst rate and gene expression in co-culture of bovine embryos with adult adipose tissue-derived mesenchymal stem cells. J Assist 33, 1395–403.CrossRefGoogle ScholarPubMed
Moshkdanian, G, Nematollahi-Mahani, SN, Pouya, F and Nematollahi-Mahani, A (2011) Antioxidants rescue stressed embryos at a rate comparable with co-culturing of embryos with human umbilical cord mesenchymal cells. J Assist Reprod Genet 28, 343–9.CrossRefGoogle Scholar
O’Brien, MJ, Pendola, JK and Eppig, JJ (2003) A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 68, 1682–6.CrossRefGoogle ScholarPubMed
Park, SE, Lee, J, Chang, EH, Kim, JH, Sung, JH, Na, DL and Chang, JW (2016) Activin A secreted by human mesenchymal stem cells induces neuronal development and neurite outgrowth in an in vitro model of Alzheimer’s disease: neurogenesis induced by MSCs via activin A. Arch Pharm Res 39, 1171–9.CrossRefGoogle Scholar
Park, SG, Kim, JH, Xia, Y and Sung, JH (2011) Generation of reactive oxygen species in adipose-derived stem cells: friend or foe? Expert Opin Ther Targets 15, 1297–306.CrossRefGoogle ScholarPubMed
Parte, S, Bhartiya, D, Manjramkar, DD, Chauhan, A and Joshi, A (2013) Stimulation of ovarian stem cells by follicle stimulating hormone and basic fibroblast growth factor during cortical tissue culture. J Ovarian Res 6, 20.CrossRefGoogle ScholarPubMed
Persani, L, Rossetti, R, Di Pasquale, E, Cacciatore, C and Fabre, S (2014) The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum Reprod Update 20, 869–83.CrossRefGoogle ScholarPubMed
Rodrigues, GQ, Lima, IMT, Chaves, RN, Rossetto, R, Costa, SL, Castro, SV, Barros, VRP, Matos, MHT, Lopes, CAP, Báo, SN, Campello, CC and Figueiredo, JR (2014) Transforming growth factor-β (TGF-β) maintains follicular ultrastructure and stimulates preantral follicle growth in caprine ovarian tissue cultured in vitro . Arq Bras Med Vet e Zootec. 66, 411–6.CrossRefGoogle Scholar
Rossetto, R, Matos, MHT, Celestino, JJH, Bruno, JB, Silva, CMG and Faustino, LR (2010) Androstenedione and follicle stimulating hormone involvement in the viability and development of goat preantral follicles in vitro. Anim Reprod 7, 80–9.Google Scholar
Saraiva, MVA, Rossetto, R, Brito, IR, Celestino, JJH, Silva, CMG, Faustino, LR, Almeida, AP, Bruno, JB, Magalhães, DM, Matos, MHT, Campello, CC and Figueiredo, JR (2010) Dynamic medium produces caprine embryo from preantral follicles grown in vitro . Reprod Sci 17, 1135–43.CrossRefGoogle ScholarPubMed
Sedlak, J and Lindsay, RH (1968) Estimation of total, protein-bound and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25, 192–205.CrossRefGoogle ScholarPubMed
Serafim, MKB, Duarte, ABG, Silva, GM, Souza, CEA, Magalhães-Padilha, DM, Moura, AAA, Silva, LDM, Campello, CC and Figueiredo, JR (2015) Impact of growth hormone (GH) and follicle stimulating hormone (FSH) on in vitro canine preantral follicle development and estradiol production. Growth Horm IGF Res 25, 85–9.CrossRefGoogle ScholarPubMed
Telfer, EE, McLaughlin, M, Ding, C and Thong, KJ (2008) A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod 23, 1151–8.CrossRefGoogle ScholarPubMed
Wang, X, Catt, S, Pangestu, M and Temple-Smith, P (2011) Successful in vitro culture of pre-antral follicles derived from vitrified murine ovarian tissue: oocyte maturation, fertilization and live births. Reproduction 141, 183–91.CrossRefGoogle ScholarPubMed
Xia, X, Wang, T, Yin, T, Yan, L, Yan, J, Lu, C, Zhao, L, Li, M, Zhang, Y, Jin, H, Zhu, X, Liu, P, Li, R and Qiao, J (2015) Mesenchymal stem cells facilitate in vitro development of human preantral follicle. Reprod Sci 22, 1367–76.CrossRefGoogle ScholarPubMed