Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-02T20:10:39.615Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of follicle-stimulating hormone concentrations on the integrity and development of bovine follicles cultured in vitro

Published online by Cambridge University Press:  21 November 2018

C. Bizarro-Silva Open the ORCID record for C. Bizarro-Silva [Opens in a new window] ,
M.M. Santos ,
J.R. Gerez ,
S.M. González ,
L.A. Lisboa  and
M.M. Seneda
C. Bizarro-Silva*
Affiliation:
Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil
M.M. Santos
Affiliation:
Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil
J.R. Gerez
Affiliation:
Department of Veterinary Pathology, University of Londrina, Paraná, 86051-990, Cx. Postal: 10.011, Brazil
S.M. González
Affiliation:
Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil
L.A. Lisboa
Affiliation:
Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil
M.M. Seneda
Affiliation:
Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil
*
Address for correspondence: Camila Bizarro-Silva. Laboratory of Animal Reproduction, University of Londrina (UEL), Paraná, 86051-990, Cx. Postal: 10.011, Brazil E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study investigated the in vitro culture of bovine follicles included in ovarian tissue for 2 or 6 days (D2 or D6), with the addition of different concentrations of follicle-stimulating hormone (FSH) (0, 10, 50, 100 or 200 ng/ml). Data were compared for follicular development, morphological integrity and diameter of follicles and oocytes. Ovaries (n = 10) from Nelore cows (n = 5) were divided into fragments (n = 11 per ovary) and were immediately fixed in Bouin’s solution (D0) or were individually cultured for 2 or 6 days in one of the described concentrations of FSH and then processed for histology. Compared with the rates of follicular development at D2 for minimal essential medium (MEM) (75.0%) and 50 ng/ml of FSH (71.1%), the best rates of follicular development at D2 were obtained with 10 (84.7%), 100 (87.5%) and 200 ng/ml of FSH (85.0%; P<0.05). After 6 days of cultivation, there were no differences among treatments regarding follicular growth. The morphological integrity of preantral follicles was better maintained by 100 ng/ml FSH for 2 and 6 days of cultivation (51.2 and 40.4%, respectively; P<0.05) than that for MEM (D2: 30.9%, D6: 20.8%), 10 (D2: 39.2%, D6: 22.8%), 50 (D2: 30.4%, D6: 28.8%) and 200 ng/ml FSH (D2: 45.2%, D6: 36.8%). FSH at 100 ng/ml provided the highest mean diameter averages: 34.5±10.8 µm at D2 and 33.2±12.5 µm at D6 (P<0.05). We concluded that the medium supplemented with 100 ng/ml FSH during in vitro culture provided appropriate conditions for the development and morphological integrity of preantral follicles in cattle.

Keywords

Bos indicusFollicle-stimulating hormoneFolliculogenesisIn vitro culturePreantral follicles
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 417 - 423
Copyright
© Cambridge University Press 2018 

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

Adriaens, I, Cortvrindt, R and Smitz, J (2004) Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum Reprod 19, 398–408.Google Scholar
Aguiar, FL, Lunardi, FO, Lima, LF, Rocha, RM, Bruno, JB, Magalhães-Padilha, DM, Cibin, FW, Nunes-Pinheiro, DC, Gastal, MO, Rodrigues, AP, 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, 1106–1112.Google Scholar
Almeida, AP, Saraiva, MVA, Araújo, VR, Magalhães, DM, Duarte, ABG, Frota, IMA, Lopes, CAP, Campello, CC, Silva, JRV and Figueiredo, JR (2011) Expression of growth and differentiation factor 9 (GDF-9) and its effect on the in vitro culture of caprine preantral ovarian follicles. Small Ruminant Res 100, 169–176.Google Scholar
Andrade, ER, van den Hurk, R, Lisboa, LA, Hertel, MF, Melo-Sterza, FA, Moreno, K, APFRL, Bracarense, Landim-Alvarenga, FC, Seneda, MM and Alfieri, AA (2012) Effects of ascorbic acid on in vitro culture of bovine preantral follicles. Zygote 20, 379–388.Google Scholar
Araújo, VR, Gastal, MO, Figueiredo, JR and Gastal, EL (2014) In vitro culture of bovine preantral follicles: a review. Reprod Biol Endocrinol 12, 78–92.Google Scholar
Barros, VR, Cavalcante, AY, Macedo, TJ, Barberino, RS, Lins, TL, Gouveia, BB, Menezes, VG, Queiroz, MA, Araújo, VR, Palheta, RC Jr, Leite, MC and Matos, MH (2013) Immunolocalization of melatonin and follicle-stimulating hormone receptors in caprine ovaries and their effects during in vitro development of isolated pre-antral follicles. Reprod Domest Anim 48, 1025–1033.Google Scholar
Braw-Tal, R and Yossefi, S (1997) Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J Reprod Fertil 109, 165–171.Google Scholar
Búfalo, I, González, SM, 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. Semin-Cienc Agrar 37, 243–250.Google Scholar
Cushman, RA, Wahl, CM and Fortune, JE (2002) Bovine ovarian cortical pieces grafted to chick embryonic membranes: a model for studies on the activation of primordial follicles. Hum Reprod 174, 48–54.Google Scholar
Derrar, N, Price, CA and Sirard, MA (2000) Effects of growth factors and co-culture with ovarian medulla on the activation of primordial in explants of bovine ovarian cortex. Theriogenology 54, 587–598.Google Scholar
Duarte, ABG, Araújo, VR, Chaves, RN, Silva, GM, Luz, VB, Haag, KT, Magalhães-Padilha, DM, Almeida, AP, Lobo, CH, Campello, CC and Figueiredo, JR (2013) Insulin-like growth factor II (IGF-II) and follicle stimulating hormone (FSH) combinations can improve the in vitro development of grown oocytes enclosed in caprine preantral follicles. Growth Horm IGF Res 23, 37–44.Google Scholar
Farin, CE, Rodriguez, KF, Alexander, JE, Hockney, JE, Herrick, JR and Kennedy-Stoskopf, S (2007) The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro . Anim Reprod Sci 98, 97–112.Google Scholar
Fortune, JE, Kito, S, Wandji, SA and Srsen, V (1998) Activation of bovine and baboon primordial follicles in vitro . Theriogenology 49, 441–449.Google Scholar
Fortune, JE (2003) The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci 78, 135–163.Google Scholar
Gomes, RG, Lisboa, LA, Silva, CB, Max, MC, Marino, PC, Oliveira, RL, González, SM, Santos, MM, Barreiros, TRR, Marinho, LSR and Sened, MM (2015) Improvement of development of equine preantral follicles after six days of in vitro culture with ascorbic acid supplementation, Theriogenology 84, 750–755.Google Scholar
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, 169–173.Google Scholar
Gougeon, A (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrin Rev 17, 121–155.Google Scholar
Gutierrez, CG, Ralph, JH, Telfer, EE, Wilmut, I and Webb, R (2000) Growth and antrum formation of bovine preantral follicles in long-term culture in vitro . Biol Reprod 62, 1322–1328.Google Scholar
Hsueh, AJ, Kawamura, K, Cheng, Y and Fauser, BC (2015) Intraovarian control of early folliculogenesis. Endocr Rev 36, 1–24.Google Scholar
Hulshof, SCJ, Figueiredo, JR, Beckers, JF, Bevers, MM, Donk, JA and Van Den Hurk, R (1995) Effect of fetal bovine serum, FSH and 17β-estradiol on the culture of bovine preantral follicles. Theriogenology 44, 217–226.Google Scholar
Hulshof, SCJ, Figueiredo, JR, Bekers, JF, Bevers, MM and van den Hurk, R (1994) Isolation and Characterization of preantral follicles from foetal bovine ovaries. Vet Quart 16, 78–80.Google Scholar
Kreeger, PK, Fernandes, NN, Woodruff, TK and Shea, LD (2005) Regulation of mouse follicle development by follicle stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol Reprod 73, 942–950.Google Scholar
Lima, LF, Rocha, RM, Alves, AM, Saraiva, MV, Araújo, VR, Lima, IM, Lopes, CA, Báo, SN, Campello, CC, Rodrigues, AP and Figueiredo, JR (2013) Dynamized follicle-stimulating hormone affects the development of ovine preantral follicles cultured in vitro . Homeopathy 102, 41–48.Google Scholar
Magalhães, DM, Fernandes, DD, Araújo, VR, Almeida, AP, Matos, MHT and Figueiredo, JR (2009) Papel do hormônio folículo estimulante na foliculogênese in vivo e in vitro . Rev Bras Reprod Anim 33, 171–182.Google Scholar
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, 182–188.Google Scholar
Matos, MHT, Lima-Verde, IB, Luque, MCA, Maia, JE Jr, Silva, JRV, Celestino, JJH, Martins, FS, Báo, SN, Lucci, CM and Figueiredo, JR (2007) Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro . Zygote 15, 173–182.Google Scholar
Max, MC, Silva, CB, González, SM, Lindquist, AG, Búfalo, I, Gomes, RG, Morotti, F, Costa, CB, Barreiros, T, Lisboa, LA and Seneda, MM (2017) The development and integrity of equine pre-antral follicles cultured in vitro with follicle-stimulating hormone (FSH) supplementation. Reprod Domest Anim 52, 899–904.Google Scholar
McLaughlin, M, Bromfield, JJ, Albertini, DF and Telfer, EE (2010) Activin promotes follicular integrity and oogenesis in cultured preantral bovine follicles. Mol Hum Reprod 16, 644–653.Google Scholar
Médure, G, Charnaux, N, Driancourt, MA, Combettes, L, Granet, P, Vannier, B, Lossfelt, H and Milgrom, E (2002) Follicle-stimulating hormone receptors in oocytes? J Clin Endocr Metab 87, 2266–2276.Google Scholar
Nilsson, EE and Skinner, MK (2001) Cellular interactions that control primordial follicle development and folliculogenesis. J Soc Gynecol Invest 8, 17–20.Google Scholar
Oktay, K, Briggs, D and Gosden, RG (1997) Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocr Metab 82, 3748–3751.Google Scholar
Rodrigues, GQ, Silva, CMG, Faustino, LR, Bruno, JB, Pinto, LC, Lopes, CAP, Campello, CC and Figueiredo, JR (2010) Efeito de diferentes concentrações de hormônio folículo-estimulante recombinante sobre o desenvolvimento in vitro de folículos pré-antrais caprinos e ovinos isolados. Acta Vet Bras 4, 144–152.Google Scholar
Rossetto, R, Santos, RR, Silva, GM, Duarte, ABG, Silva, CMG, Campello, CC and Figueiredo, JR (2013) Comparative study on the in vitro development of caprine and bovine preantral follicles. Small Ruminant Res 113, 167–170.Google Scholar
Rossetto, R, Saraiva, MV, Bernuci, MP, Silva, GM, Brito, IR, Alves, AM, Magalhães-Padilha, DM, Báo, SN, Campello, CC, Rodrigues, AP and Figueiredo, JR (2016) Impact of insulin concentration and mode of FSH addition on the in vitro survival and development of isolated bovine preantral follicles. Theriogenology 86, 1137–1145.Google Scholar
Roy, SK and Albee, L (2000) Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. Endocrinology 141, 4449–4456.Google Scholar
Salomon, AK, Leon, K, Campbell, MM and Young, KA (2018) Folliculogenic factors in photoregressed ovaries: Differences in mRNA expression in early compared to late follicle development. Gen Comp Endocr 260, 90–99.Google Scholar
Saraiva, MVA, Rossetto, R, Brito, IR, Celestino, JJH, Silva, CMG, Faustino, LR, Almeida, AP, Bruno, JB, Magalhães, MS, Matos, MHT, Campello, CC and Figueiredo, JR (2010) Dynamic medium produces caprine embryo from preantral follicles grown in vitro . Reprod Sci 17, 1135–1143.Google Scholar
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, 85–89.Google Scholar
Silva, JRV, van den Hurk, R and Figueiredo, JR (2016) Ovarian follicle development in vitro and oocyte competence: advances and challenges for farm animals. Domest Anim Endocrin 55, 123–135.Google Scholar
Silva-Buttkus, P, Jayasooriya, GS, Mora, JM, Mobberley, M, Ryder, TA, Baithun, M, Stark, J, Franks, S and Hardy, K (2008) Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci 121, 3890–3900.Google Scholar
Souza, DK, Salles, LP, Camargo, R, Gulart, LVM, Costa e Silva, S, Lima, BD, FAG, Torres and Silva, AAMR (2017) Effects of PI3K and FSH on steroidogenesis, viability and embryo development of the cumulus–oocyte complex after in vitro culture. Zygote 26, 50–61.Google Scholar
Thomas, FH, Armstrong, DG and Telfer, EE (2003) Activin promotes oocyte development in ovine preantral follicles in vitro . Reprod Biol Endocrinol 76, 1–7.Google Scholar
Thomas, FH, Ethier, JF, Shimasaki, S and Vanderhyden, BC (2005) Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 146, 941–949.Google Scholar
Vasconcelos, GL, Saraiva, MV, Costa, JJ, Passos, MJ, Silva, AW, Rossi, RO, Portela, AM, Duarte, AB, Magalhães-Padilha, DM, Campelo, CC, Figueiredo, JR, van den Hurk, R and Silva, JR (2013) Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles. Reprod Fert Dev 25, 1194–1203.Google Scholar
Wandji, SA, Eppig, JJ and Fortune, JE (1996) FSH and growth factor affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–832.Google Scholar
Wright, CS, Hovatta, O, Margara, R, Trew, G, Winston, RM, Franks, S and Hardy, K (1999) Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Hum Reprod 14, 1555–1562.Google Scholar
Wu, J, Xu, B and Wang, W (2007) Effects of luteinizing hormone and follicle stimulating hormone on the developmental competence of porcine preantral follicle oocytes grown in vitro. J Assist Reprod Gen 24, 419–424.Google Scholar