Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T22:24:18.837Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of isolated bovine preantral follicles based on morphology, diameter and cell number

Published online by Cambridge University Press:  14 January 2020

Juliana I. Candelaria  and
Anna C. Denicol Open the ORCID record for Anna C. Denicol [Opens in a new window]
Juliana I. Candelaria
Affiliation:
Department of Animal Science, University of California, Davis, CA, USA
Anna C. Denicol*
Affiliation:
Department of Animal Science, University of California, Davis, CA, USA
*
Author for correspondence: Anna C. Denicol. Department of Animal Science, University of California, 450 Bioletti Way, Davis, CA, 95616, USA. Tel: +1 352 665 1909. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Preantral follicles are a potential reservoir of oocytes to be used in assisted reproductive technologies. With the increasing interest in developing techniques to grow preantral follicles in vitro, and as the bovine emerges as an appropriate model species to understand human folliculogenesis, the establishment of an accurate classification of developmental stages is needed. Classification of bovine preantral follicles has been mostly based on histological analysis and estimation models, which may not translate well to correctly characterize preantral follicles isolated from the ovary. In this study, we classified bovine preantral follicles by morphology upon isolation, determined diameter and number of granulosa cells by direct counting, and compared our results with previous studies reporting bovine preantral follicle classification. Follicles were isolated via homogenization of ovary tissue and classified into primary, early secondary and secondary stage based on morphology and number of layers of granulosa cells. Diameter was individually measured and Hoechst 33342 was used as a nuclear stain to count granulosa cells. We found that follicles classified by morphology into primary, early secondary, and secondary had different mean diameter and cell number (P < 0.01); cell number and diameter were positively correlated, as were cell density and cell number in each developmental stage (P < 0.01). Results obtained here were mostly in agreement with previous classifications based on histological sections and on isolated follicles, with some discrepancies. The present data add accuracy to classification of bovine preantral follicles that is critical to optimize culture conditions to produce developmentally competent oocytes.

Keywords

BovineClassificationFollicle morphologyFolliculogenesisPreantral follicle
Type
Research Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 154 - 159
Copyright
© Cambridge University Press 2020

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

Apolloni, LB, Bruno, JB, Alves, BG, Ferreira, ACA, Paes, VM, Moreno, J, de Aguiar, FL N, Brandao, FZ, Smitz, J, Apgar, G and de Figueiredo, JR (2016) Accelerated follicle growth during the culture of isolated caprine preantral follicles is detrimental to follicular survival and oocyte meiotic resumption. Theriogenology 86, 1530–40.CrossRefGoogle ScholarPubMed
Araujo, 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
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, 165–71.CrossRefGoogle ScholarPubMed
Da 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, 3890–900.CrossRefGoogle ScholarPubMed
De La Fuente, R and Eppig, JJ (2001) Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol 229, 224–36.CrossRefGoogle ScholarPubMed
Fair, T (2010) Mammalian oocyte development: checkpoints for competence. Reprod Fertil Dev 22, 13–20.CrossRefGoogle ScholarPubMed
Fair, T, Hulshof, SC, Hyttel, P, Greve, T and Boland, M (1997a) Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol Reprod Dev 46, 208–15.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Fair, T, Hulshof, SC, Hyttel, P, Greve, T and Boland, M (1997b) Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat Embryol (Berl) 195, 327–36.CrossRefGoogle ScholarPubMed
Figueiredo, JR, Hulshof, SC, Van den Hurk, R, Ectors, FJ, Fontes, RS, Nusgens, B, Bevers, MM and Beckers, JF (1993) Development of a combined new mechanical and enzymatic method for the isolation of intact preantral follicles from fetal, calf and adult bovine ovaries. Theriogenology 40, 789–99.CrossRefGoogle ScholarPubMed
Gougeon, A and Chainy, GB (1987) Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 81, 433–42.CrossRefGoogle ScholarPubMed
Hornick, JE, Duncan, FE, Shea, LD and Woodruff, TK (2012) Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum Reprod 27, 1801–10.CrossRefGoogle ScholarPubMed
Hulshof, SC, Figueiredo, JR, Beckers, JF, Bevers, MM and van den Hurk, R (1994) Isolation and characterization of preantral follicles from foetal bovine ovaries. Vet Q 16, 78–80.CrossRefGoogle ScholarPubMed
Jorssen, EP, Langbeen, A, Marei, WF, Fransen, E, De porte, HF, Leroy, JL and Bols, PE (2015) Morphologic characterization of isolated bovine early preantral follicles during short-term individual in vitro culture. Theriogenology 84, 301–11.CrossRefGoogle ScholarPubMed
Kacinskis, MA, Lucci, CM, Luque, MC and Bao, SN (2005) Morphometric and ultrastructural characterization of Bos indicus preantral follicles. Anim Reprod Sci 87, 45–57.CrossRefGoogle ScholarPubMed
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, 942–50.CrossRefGoogle Scholar
Langbeen, A, Jorssen, EP, Fransen, E, Rodriguez, AP, Garcia, MC, Leroy, JL and Bols, PE (2015) Characterization of freshly retrieved preantral follicles using a low-invasive, mechanical isolation method extended to different ruminant species. Zygote 23, 683–94.CrossRefGoogle ScholarPubMed
Laronda, MM, Rutz, AL, Xiao, S, Whelan, KA, Duncan, FE, Roth, EW, Woodruff, TK and Shah, RN (2017) A bioprosthetic ovary created using 3D printed microporous scaffolds restores ovarian function in sterilized mice. Nat Commun 8, 15261.CrossRefGoogle ScholarPubMed
Lundy, T, Smith, P, O’Connell, A, Hudson, NL and McNatty, KP (1999) Populations of granulosa cells in small follicles of the sheep ovary. J Reprod Fertil 115, 251–262.CrossRefGoogle ScholarPubMed
Lussier, JG, Matton, P and Dufour, JJ (1987) Growth rates of follicles in the ovary of the cow. J Reprod Fertil 81, 301–7.CrossRefGoogle ScholarPubMed
McLaughlin, M and Telfer, EE (2010) Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system. Reproduction 139, 971–8.CrossRefGoogle ScholarPubMed
Rossetto, R, Saraiva, MVA, Bernuci, MP, Silva, GM, Brito, IR, Alves, A, Magalhaes-Padilha, DM, Bao, SN, Campello, CC, Rodrigues, APR 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, 1137–45.CrossRefGoogle ScholarPubMed
Russe, I (1983) Oogenesis in cattle and sheep. Bibl Anat 24, 77–92.Google ScholarPubMed
van Wezel, IL and Rodgers, RJ (1996) Morphological characterization of bovine primordial follicles and their environment in vivo. Biol Reprod 55, 1003–11.CrossRefGoogle ScholarPubMed
Wang, XN, Roy, SK and Greenwald, GS (1991) In vitro DNA synthesis by isolated preantral to preovulatory follicles from the cyclic mouse. Biol Reprod 44, 857–63.CrossRefGoogle ScholarPubMed
Xiao, S, Zhang, J, Romero, MM, Smith, KN, Shea, LD and Woodruff, TK (2015) In vitro follicle growth supports human oocyte meiotic maturation. Sci Rep 5, 17323.CrossRefGoogle ScholarPubMed
Xu, M, West, E, Shea, LD and Woodruff, TK (2006) Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol Reprod 75, 916–23.CrossRefGoogle ScholarPubMed