Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T03:24:57.293Z Has data issue: false hasContentIssue false

Establishment of a protocol for the isolation of ovarian preantral follicles derived from collared peccaries (Pecari tajacu)

Published online by Cambridge University Press:  15 August 2019

Lívia Batista Campos
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Andréia Maria da Silva
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Samara Sandy Jeronimo Moreira
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Caio Sergio Santos
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Carlos Alexandre de Carvalho Apolinário
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Márcia Viviane Alves Saraiva
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Moacir Franco de Oliveira
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
Alexandre Rodrigues Silva*
Affiliation:
Laboratory of Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), Mossoró, RN, Brazil
*
Address for correspondence: A.R. Silva. Departamento de Ciências Animais, Universidade Federal Rural do Semi-Árido (UFERSA), BR 110, Km 47, Bairro Pres. Costa e Silva. CEP: 59.625-900 Mossoró, RN, Brazil. Fax: +55 84 3317 8360. E-mail: [email protected]

Summary

We compare the efficiency of mechanical or enzymatic methods, and their combination, for the isolation of ovarian preantral follicles (PFs) from collared peccaries. The ovaries from six females were subjected to the different methods investigated here. For the enzymatic method, ovary fragments were exposed to collagenase type IV in TCM-HEPES medium; the mechanical procedure was based on ovarian cortex dissociation by using a scalpel blade. The residual solution obtained after the mechanical isolation was subjected to the enzymatic procedure. The number of isolated PFs was quantified and classified as primordial, primary, or secondary; their viability was assessed using trypan blue dye assay. To confirm the results, PFs derived from the most efficient method were evaluated for integrity using scanning electron microscopy (SEM) and subjected to a 24 h in vitro culture for subsequent evaluation of viability by using fluorescent probes. A higher number of PFs (P < 0.05) was obtained from the enzymatic method (961.7 ± 132.9) in comparison with the mechanical method (434.3 ± 88.9), but no difference was observed between the two methods and their combination (743.2 ± 92.8). The trypan blue assay showed that the enzymatic method (98.7 ± 0.6%) provided the highest percentage of viable follicles (P < 0.05). Furthermore, SEM confirmed the ultrastructural integrity of the surface architecture of peccary PFs isolated by the enzymatic procedure; epifluorescence microscopy was used to confirm their viability (86.0%). In conclusion, we suggest that the enzymatic method investigated here is useful for the isolation of viable ovarian PFs from collared peccaries.

Type
Research Article
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

Ahn, JI, Lee, ST, Park, JH, Kim, JY, Park, JH, Choi, JK and Lim, JM (2012) In vitro-growth and gene expression of porcine preantral follicles retrieved by different protocols. Asian-Australasian J Anim Sci 25, 950–5.CrossRefGoogle ScholarPubMed
Alves, BG, Alves, KA, Araújo, VR, Beletti, ME, Gambarini, ML and Jacomini, JO (2012) Quantitative and morphological study of preantral follicles from prepubertal gilts. Acta Sci Vet 40, 1079.Google Scholar
Bustos-Obregon, E and Fléchon, JE (1975) Comparative scanning electron microscope study of boar, bull and ram spermatozoa. Cell Tissue Res 161 329–41.CrossRefGoogle ScholarPubMed
Cavalcante-Filho, MF, Miglino, MA, Machado, GV, Bevilacqua, EMAF and Neves, WC (1998) Comparative study of the morphology of the stomach of White lipped peccary (Tayassu pecari) and of the collared peccary (Tayassu tajacu). Braz J Morphol Sci 15, 203–7.Google Scholar
Choi, MH, Seung, PG and Jeong, ML (2008) Retrieval of porcine ovarian follicles by different methods. Asian-Australasian J Anim Sci 21, 353–7.CrossRefGoogle Scholar
Demeestere, I, Delbaere, A, Gervy, C, Van Den Bergh, M, Devreker, F and Englert, Y (2002) Effect of preantral follicle isolation technique on in vitro follicular growth, oocyte maturation and embryo development in mice. Hum Reprod 17, 2152–9.CrossRefGoogle ScholarPubMed
Dong, FL, Ma, L, Shi, SL, Dai, SJ, Liu, XG, Su, YC, Guo, YH, Wang, F and Sun, YP (2014) A research on the isolation methods of frozen–thawed human ovarian preantral follicles. Int J Clin Exp Med 15, 2298–303.Google Scholar
Figueiredo, JR, Hulshof, SCJ and Van Den Hurk, R (1993) Development of a combined new mechanical and enzymatic method for the isolation of intact follicles from fetal, calf and adult bovine ovaries. Theriogenology 40, 789–99.CrossRefGoogle ScholarPubMed
Gongora, J, Reyna-Hurtado, R, Beck, H, Taber, A, Altrichter, M and Keuroghlian, A (2011) Pecari tajacu. The IUCN Red List of Threatened Species 2011: e.T41777A10562361. Available: http://dx.doi.org/10.2305/IUCN.UK.2011-2.RLTS.T41777A10562361.en CrossRefGoogle Scholar
Gosden, RG and Telfer, E (1987) Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool 211, 169–75.CrossRefGoogle Scholar
Greenwald, GS and Moor, RM (1989) Isolation and preliminary characterization of pig primordial follicles. J Reprod Fertil 87, 561–71.CrossRefGoogle ScholarPubMed
Hulshof, SCJ, Figueiredo, JR, Beckers, JF, Bevers, MM and Van Den Hurk, R (1994) Isolation and characterization of preantral follicles from fetal bovine ovaries. Vet Q 16, 7880.CrossRefGoogle Scholar
Kerong, S, Xuefeng, Y, Liying, D, Dengke, PAN, Yunhai, Z, Yonghui, Z, Xuemei, D, Xiaoxiang, H, Changxin, W and Ning, L (2007) Advanced methods of isolation and identification of porcine primordial follicles. Anim Reprod Sci 101, 163–71.Google Scholar
Klein, T, Buhr, E and Frase, CG (2012) TSEM: a review of scanning electron microscopy in transmission mode and its applications. In: Hawkes, P (ed.). Adv Imaging Electron Phys 171, 297356.CrossRefGoogle Scholar
Lakshminarayana, BNV, Praveen Chakravarthi, V, Brahmaiahb, KV and Rao, VH (2014) Quantification of P450 aromatase gene expression in cultured and in vivo grown ovarian follicles in sheep. Small Rumin Res 117, 6672 CrossRefGoogle Scholar
Lierman, S, Tilleman, K, Cornelissen, M, De Vos, WH, Weyers, S, T’Sjoen, G, Cuvelier, CA and De Sutter, P (2014) Follicles of various maturation stages react differently to enzymatic isolation: a comparison of different isolation protocols. Reprod BioMed Online 30, 181–90.CrossRefGoogle ScholarPubMed
Lima, LF, Rubessa, M, Rocha, RMP, Winters, R, Milner, DJ, Campello, CC, Figueiredo, JR and Wheeler, MB (2017) High diluted and dynamized follicle stimulating hormone modulates steroid production in isolated porcine preantral follicles cultured in vitro . Homeopathy 106, 8792.Google Scholar
Lima, GL, Luz, VB, Lima, LF, Rocha, R, Castro, SV, Castelo, TS, Rodrigues, A, Figueiredo, JR and Silva, AR (2018) Interactions between different media and FSH supplementation on in vitro culture of preantral follicles enclosed in ovarian tissue derived from collared peccaries (Pecari tajacu Linnaeus, 1758). Reprod Domest Anim 53, 880–8.CrossRefGoogle Scholar
Lima, GL, Santos, EAA, Luz, VB, Rodrigues, APR and Silva, AR (2013) Morphological characterization of the ovarian preantral follicle population of collared peccaries (Tayassu tajacu Linnaeus, 1758). Anat Histol Embryol 42, 304–11.CrossRefGoogle Scholar
Lima, GL, Luz, VB, Alves, AMCV, Lunardi, FO, Souza, ALP, Peixoto, GCX, Rodrigues, AP R, Oliveira, MF and Silva, AR (2012) Vitrification of collared peccaries (Tayassu tajacu) ovarian tissue using various. In: IV International Symposium on Animal Biology of Reproduction, Campinas, Anais Campinas.Google Scholar
Lopes, CAP, Santos, RR, Celestino, JJH, Melo, MA, Chaves, RN, Campello, CC, Silva, JR, Báo, SN, Jewgenow, K and Figueiredo, JR (2009) Short term preservation of canine preantral follicles: effects of temperature, medium and time. Anim Reprod Sci 115, 201–14.CrossRefGoogle Scholar
Machado, VP, Rodrigues, APR, Brasil, AF, Amorim, CA, Matos, MHT, Santos, RR and Figueiredo, JR (2002) Mechanical and enzymatic isolation of preantral ovarian follicles in goat fetuses. Ci Anim 12, 8391.Google Scholar
Mandl, I, Zipper, H and Ferguson, LT (1958) Clostridium histolyticum collagenase. Its purification and properties. Arch Biochem Biophys 74, 465–75.CrossRefGoogle ScholarPubMed
Mayor, P, Fenech, M, Bodmer, MF and Lopez-Bejar, M (2006) Ovarian features of the wild collared peccary (Tayassu tajacu) from the northeastern Peruvian Amazon. Gen Comp Endocrinol 147, 268–75.CrossRefGoogle ScholarPubMed
Moreira, SSJ, Campos, LB, Silva, AM, Praxedes, ECG, Bezerra, LGP, Apolinário, CAC and Silva, AR (2017) Comparison between solid surface and ovarian tissue cryosystem for vitrification of collared peccaries (Pecari tajacu) ovarian tissue. In: Encontro de Biotecnologia do Nordeste, Natal, Anais Natal.Google Scholar
Nottola, SA, Cecconi, S, Bianchi, S, Motta, C, Rossi, G, Continenza, MA and Macchiarelli, G (2011) Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod Biol Endocrinol 9, 112.CrossRefGoogle ScholarPubMed
Nicosia, SV, Evangelista, I and Batta, SK (1975) Rabbit ovarian follicles. I. Isolation technique and characterization at different stages of development. Biol Reprod 13, 423–47.CrossRefGoogle ScholarPubMed
Rossetto, R, Lima, IMT, Saraiva, MVA, Lima-Verde, IB, Sales, ET and Figueiredo, JR (2011) Advances in isolation and culture systems of preantral follicles. Acta Vet Brasilica 5, 1523.Google Scholar
Runge, KE, Evans, JE, He, ZY, Gupta, S, McDonald, KL, Stahlberg, H, Primakoff, P and Myles, DG (2007) Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 7, 317–25.CrossRefGoogle Scholar
Sadeghnia, S, Akhondi, MM, Hossein, G, Mobini, S, Hosseini, L, Naderi, MM and Shirazi, A (2016) Development of sheep primordial follicles encapsulated in alginate or in ovarian tissue in fresh and vitrified samples. Cryobiology 72, 100–5.CrossRefGoogle ScholarPubMed
Santos, SS, Biondi, FC, Cordeiro, MS, Miranda, MS, Dantas, JK, Figueiredo, JR and Ohashi, OM (2006) Isolation, follicular density, and culture of preantral follicles of buffalo fetuses of different ages. Anim Reprod Sci 95,115.CrossRefGoogle ScholarPubMed
Santos, DO, Mendes, A, Nogueira, SS and Nogueira-Filho, SLG (2009) Collared peccary (‘Pecari tajacu’) farming as alternative for agribusiness. Rev Bras Saúde Prod An 10, 110.Google Scholar
Shuttleworth, G, Pipkin, FB and Hunter, MG (2002) In vitro development of pig preantral follicles cultured in a serum-free medium and the effect of angiotensin II. Reproduction 123, 807–18.CrossRefGoogle Scholar
Silva, AR, Campos, LB, Maia, KM and Borges, AA (2017) Reproductive biotechniques applied to collared peccaries (Pecari tajacu Linnaeus, 1758) – an experimental strategy. Ver Bras Reprod Anim 41, 110–5.Google Scholar
Sirotkin, AV, Florkovičová (Koničková), I, Schaeffer, H-J, Laurincik, J and Harrath, AH (2017) Interrelationships between ovarian follicles grown in culture and possible mediators. Reprod Biol 17, 97104.CrossRefGoogle ScholarPubMed
Telfer, EE and Watson, ED (2000) Method for isolating preantral follicles from mare ovaries. J Reprod Fertil Suppl 56, 447−53.Google Scholar
Vanhoutte, L, Cortvrindt, R, Nogueira, D and Smitz, J (2004) Effects of chilling on structural aspects of early preantral mouse follicles. Biol Reprod 70, 1041–8.CrossRefGoogle ScholarPubMed
Young, F, Drummond, J, Akers, E, Bartle, L, Kennedy, D and Asaduzzaman, M (2017) Effects of ovarian disaggregation on adult murine follicle yield and viability. Reprod Fertil Dev 29, 2400–10.CrossRefGoogle ScholarPubMed
Zhang, S, Wu, Y, Weng, Y, Xu, Z, Chen, W, Zheng, D, Lin, W, Liu, J and Zhou, Y (2017) In vitro growth of mouse preantral follicles under simulated microgravity. J Vis Exp 130, 55641.Google Scholar