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Supplementation of culture medium with knockout serum replacement improves the survival of bovine secondary follicles when compared with other protein sources during in vitro culture

Published online by Cambridge University Press:  11 October 2019

D.S. Gomes ,
L.B. Aragão ,
M.F. Lima Neto ,
P.A.A. Barroso ,
L.R.F.M. Paulino ,
B.R. Silva ,
A.L.P. Souza ,
G.L. Vasconcelos ,
A.W.B. Silva  and
J.R.V. Silva Open the ORCID record for J.R.V. Silva [Opens in a new window]
D.S. Gomes
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
L.B. Aragão
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
M.F. Lima Neto
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
P.A.A. Barroso
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
L.R.F.M. Paulino
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
B.R. Silva
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
A.L.P. Souza
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
G.L. Vasconcelos
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
A.W.B. Silva
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
J.R.V. Silva*
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Campus of Sobral, Sobral, CE, Brazil
*
Author for correspondence: JRV Silva. Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36118000. E-mail: [email protected]
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Summary

The present study evaluated the effect of knockout serum replacement (KSR), fetal bovine serum (FBS) and bovine serum albumin (BSA) on the viability and growth of bovine secondary follicles cultured in vitro for 12 days. To this end, secondary follicles were isolated (185–202 μm) and cultured in vitro in TCM-199+ medium supplemented with KSR (5% and 10%), FBS (5% and 10%) or BSA (3 mg/ml) at 38.5°C with 5% CO2 in air. Follicular diameters were evaluated on days 0, 4, 8 and 12. After 12 days of culture, follicular survival analysis was performing by using calcein-AM and ethidium homodimer. Before and after culture, follicles were fixed in paraformaldehyde for histological evaluation. Follicular diameter at different days of culture were compared using the Kruskal–Wallis test, while the percentages of viable follicles were analyzed by chi-squared test (P < 0.05). Results showed that follicles cultured in the presence of KSR at both concentrations presented higher follicular survival rates than those cultured in control medium alone or supplemented with FBS or BSA. Conversely, the presence of KSR, BSA or FBS did not increase follicular diameter after 12 days of culture. Histology analysis showed that, among the tested treatments, follicles cultured in the presence of KSR had preserved rounded oocytes, juxtaposed granulosa cells and intact basal membrane. In conclusion, supplementation of culture medium with KSR increases the follicular survival of bovine secondary follicles cultured in vitro.

Keywords

CowIn vitro cultureKnockout serum replacementOocytesSecondary follicles
Type
Research Article
Information
Zygote , Volume 28 , Issue 1 , February 2020 , pp. 32 - 36
Copyright
© Cambridge University Press 2019 

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References

Almeida, AP, Magalhães-Padilha, DDM, Araújo, VR, Costa, SLD, Chaves, RN, Lopes, C AP, Donato, MA, Peixoto, CA, Campello, CC, Junior, JB and Figueiredo, JR (2015) Effect of sequential medium with fibroblast growth factor-10 and follicle stimulating hormone on in vitro development of goat preantral follicles. Anim Reprod Sci 152, 32–8.CrossRefGoogle ScholarPubMed
Aoshima, K, Baba, A, Makino, Y and Okada, Y (2013) Establishment of alternative culture method for spermatogonial stem cells using knockout serum replacement. PLoS One 8, 77715.CrossRefGoogle 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
Beck, K, Singh, J, Dar, MA and Anzar, M (2018) Short-term culture of adult bovine ovarian tissues: chorioallantoic membrane (CAM) vs. traditional in vitro culture systems. Reprod Biol Endocrinol 16, 1–10.CrossRefGoogle ScholarPubMed
Bernuci, MP, Rosa-e-Silva, ACJS, Batista, L, Garcia, C, Campos, JO and Sá, MFS (2013) Effect of fetal calf serum and bovine serum albumin on in vitro development of bovine preantral follicles during three-dimensional culture. Fertil Steril 100, 168–9.CrossRefGoogle Scholar
Brunner, D, Frank, J, Appl, H, Schoffl, H, Pfaller, W and Gstraunthaler, G (2010) Serum-free cell culture: the serum-free media interactive online database. Altex 27, 53–62.CrossRefGoogle ScholarPubMed
Cadoret, V, Frapsauce, C, Jarrier, O, Maillard, V, Bonnet, A, Locatelli, Y, Royère, D, Monniaux, D, Guérif, F and Monget, P (2017) Molecular evidence that follicle development is accelerated in vitro compared with in vivo. Reproduction 153, 493–508.CrossRefGoogle ScholarPubMed
Cho, H, Lee, A and Kim, K (2018) The effect of serum types on chondrogenic differentiation of adipose-derived stem cells. Biomater Res 22, 6.CrossRefGoogle ScholarPubMed
Del Collado, M, Saraiva, NZ, Lopes, FL, Cruz, MH, Gaspar, RC, Oliveira, CS, Perecin, F and Garcia, JM (2014) Effects of reduction or replacement of fetal calf serum by other compounds during in vitro maturation of bovine oocytes. Pesq Vet Bras 34, 689–94.CrossRefGoogle Scholar
Del Collado, M, Saraiva, NZ, Lopes, FL, Gaspar, RC, Padilha, LC, Costa, RR, Rossi, GF, Vantini, R and Garcia, JM (2015) Influence of bovine serum albumin and fetal bovine serum supplementation during in vitro maturation on lipid and mitochondrial behaviour in oocytes and lipid accumulation in bovine embryos. Reprod Fert Dev 28, 689–94.Google Scholar
Fujihara, M, Comizzoli, P, Wildt, DE and Songsasen, N (2012) Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium. Reprod Domest Anim 47, 102–8.CrossRefGoogle Scholar
Garcia-Gonzalo, FR and Belmonte, JCL (2008) Albumin-associated lipids regulate human embryonic stem cell self-renewal. PLoS One 3, 1384.CrossRefGoogle ScholarPubMed
Gougeon, A (2010) Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endocrinol (Paris) 71, 132–43.CrossRefGoogle ScholarPubMed
Heger, IJ, Froehlich, K, Pastuscheck, J, Schmidt, A, Baer, C, Mmrowka, R, Backsch, C, Schleuβner, E, Markert, UR and Schmidt, A (2018) Human serum alters cell culture behavior and improves spheroid formation in comparison to fetal bovine serum. Exp Cell Res 365, 57–65.CrossRefGoogle ScholarPubMed
Hulshof, SCJ, Figueiredo, JR, Beckers, JF, Bevers, MM, van der Donk, JA and van den Hurk, R (1995) Effects of fetal bovine serum, FSH and 17β–estradiol on the culture of bovine preantral follicles. Theriogenology 44, 217–26.CrossRefGoogle ScholarPubMed
Jin, JX, Lee, S, Setyawan, EMN, Taweechaipaisankul, A, Kim, GA, Han, HJ, Ahn, C and Lee, BC (2018) A potential role of knockout serum replacement as a porcine follicular fluid substitute for in vitro maturation: lipid metabolism approach. J Cell Physiol 233, 6984–95.CrossRefGoogle ScholarPubMed
Leibfried-Rutledge, ML, Critser, ES and First, NL (1986) Effects of fetal calf serum and bovine serum albumin on in vitro maturation and fertilization of bovine and hamster cumulus–oocyte complexes. Biol Reprod 35, 850–7.CrossRefGoogle ScholarPubMed
Magalhães, DM, Duarte, AB, Araújo, VR, Brito, IR, Soares, TG, Lima, IM, Lopes, CA, Campello, CC, Rodrigues, AP 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
Majorek, K, Porebski, PJ, Dayal, A, Zimmermman, MT, Jablonska, K, Stewart, AJ, Chruszcz, M and Minor, W (2012) Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Mol Immunol 52, 174–82.CrossRefGoogle ScholarPubMed
Meng, L, Jan, SZ, Hamer, G, van Pelt, AM, van der Stelt, I, Keijer, J and Teerds, KJ (2018) Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostly through apoptosis. Biol Reprod 99, 853–63.Google ScholarPubMed
Motohashi, HH, Taniguchi, R, Sakamoto, J, Sankai, T and Kada, H (2017) Live, full-term mouse pups from oocytes grown and matured in vitro with serum substitutes. Reprod Biol 17, 180–4.CrossRefGoogle ScholarPubMed
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, YH, Gong, SP, Kim, HY, Kim, GA, Choi, JH, Ahn, JY and Lim, JM (2013) Development of a serum-free defined system employing growth factors for preantral follicle culture. Mol Reprod Dev 80, 725–33.Google ScholarPubMed
Paulino, LRFM, Cunha, EV, Silva, AWB, Souza, GB, Lopes, EPF, Donato, MAM, Peixoto, CA, Matos-Brito, BG, van den Hurk, R and Silva, JRV (2018) Effects of tumour necrosis factor-alpha and interleukin-1 beta on in vitro development of bovine secondary follicles. Reprod Dom Anim 53, 997–1005.CrossRefGoogle ScholarPubMed
Price, PJ, Goldsborough, MD and Tilkins, ML. Embryonic stem cell serum replacement: U.S. Patent, 1998, International Publication Number: WO/1998/30679 (International Application Number: PCT/US1998/ 000467).Google Scholar
Rossetto, R, Saraiva, MV, Dos santos, RR, Da Silva, CM, Faustino, LR, Chaves, RN, Brito, IR, Rodrigues, GQ, Lima, IM, Donato, MA, Peixoto, CA and De Figuereido, JR (2013) Effect of medium composition on the in vitro culture of bovine pre-antral follicles: morphology and viability do not guarantee functionality. Zygote 21, 125–8.CrossRefGoogle Scholar
Sakurai, M, Suzuki, C and Yoshioka, K (2015) Effect of knockout serum replacement supplementation to culture medium on porcine blastocyst development and piglet production. Theriogenology 83, 679–86.CrossRefGoogle ScholarPubMed
Silva, JRV, Ferreira, LAM, Costa, SHF and Figueiredo, JR (2002) Morphological features and control of follicular growth during folliculogenesis in domestic ruminants. Cienc Anim 12, 105–17.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 Endocrinol 55, 123–35.CrossRefGoogle ScholarPubMed
Thomas, FH, Leask, R, Srsen, V, Riley, SC, Spears, N and Telfer, EE (2001) Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture. Reproduction 122, 487–95.CrossRefGoogle ScholarPubMed
van den Hurk, R., Spek, ER, Hage, WJ, Fair, T, Ralph, JH and Schotanus, K (1998) Ultrastructure and viability of isolated bovine preantral follicles. Hum Reprod 4, 833–41.Google ScholarPubMed
van der Valk, J, Mellor, D, Brands, R, Fischer, R, Gruber, F, Gstraunthaler, G, Hellebrekers, L, Hyllner, J, Jonker, FH, Prieto, P, Thalen, M and Baumans, V (2004) The humane collection of fetal bovine serum and possibilities for serum-free cell and tissue culture. Toxicol In Vitro 18, 1–12.CrossRefGoogle ScholarPubMed
Vasconcelos, GL, Saraiva, MVA, Costa, JJN, Passos, MJ, Silva, AWB, Rossi, RODS, Portela, AMLR, Duarte, ABG, Magalhães-Padilha, DM, Campelo, CC, Figueiredo, JR, van den Hurk, R and Silva, JRV (2013) Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles. Reprod Fertil Dev 25, 1194–203.CrossRefGoogle ScholarPubMed
Zampolla, T, Rawson, DM and Zhang, T (2012) The use of fetal bovine serum for cryopreservation of stage III zebrafish (Danio rerio) ovarian follicles. Cryo Lett 33, 435–42.Google ScholarPubMed