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Effects of fetal bovine serum on trophectoderm and primitive endoderm cell allocation of in vitro-produced bovine embryos

Published online by Cambridge University Press:  24 October 2022

Felipe Eduardo Luedke ,
Caroline Pereira da Costa ,
Camilla Mota Mendes ,
Thais Rose dos Santos Hamilton Open the ORCID record for Thais Rose dos Santos Hamilton [Opens in a new window] ,
Marcella Pecora Milazzotto ,
Mayra E. O. A. Assumpção Open the ORCID record for Mayra E. O. A. Assumpção [Opens in a new window]  and
Marcelo Demarchi Goissis Open the ORCID record for Marcelo Demarchi Goissis [Opens in a new window]
Felipe Eduardo Luedke
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
Caroline Pereira da Costa
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
Camilla Mota Mendes
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
Thais Rose dos Santos Hamilton
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
Marcella Pecora Milazzotto
Affiliation:
Center for Natural and Human Sciences, Federal University of ABC, Santo André, SP, Brazil
Mayra E. O. A. Assumpção
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
Marcelo Demarchi Goissis*
Affiliation:
Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil
*
Author for correspondence: Marcelo Demarchi Goissis. Av. Orlando Marques de Paiva, 87, Department of Animal Reproduction, College of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP, Brazil, 05508–270. E-mail: mdgoissis@usp.br
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Summary

Supplementing embryonic culture medium with fetal bovine serum (FBS) renders this medium undefined. Glucose and growth factors present in FBS may affect the results of cell differentiation studies. This study tested the hypothesis that FBS supplementation during in vitro culture (IVC) alters cell differentiation in early bovine embryo development. Bovine embryos were produced in vitro and randomly distributed into three experimental groups at 90 h post insemination (90 hpi): the KSOM-FBS group, which consisted of a 5% (v/v) FBS supplementation; the KSOM33 group, with the renewal of 33% of medium volume; and the KSOM-Zero group, without FBS supplementation nor renewal of the culture medium. The results showed that the blastocyst rate (blastocyst/oocytes) at 210 hpi in the KSOM-FBS group was higher than in the KSOM-Zero group but not different from the KSOM33 group. There were no significant changes in metabolism-related aspects, such as fluorescence intensities of CellROX Green and MitoTracker Red or reduced nicotinamide adenine dinucleotide (NADH) and flavin adenine dinucleotide (FAD+). Immunofluorescence analysis of CDX2 revealed that the lack of FBS or medium supplementation reduced the number of trophectoderm (TE) cells and total cells. Immunofluorescence analysis revealed a reduction of SOX17-positive cell numbers after FBS supplementation compared with the KSOM33 group. Therefore, we concluded that FBS absence reduced blastocyst rates; however, no reduction occurred when there was a 33% volume renewal of the medium at 90 hpi. We also concluded that FBS supplementation altered TE and primitive endoderm cell allocation during early bovine embryo development.

Keywords

BlastocystCDX2DifferentiationInner cell massSOX17
Type
Research Article
Information
Zygote , Volume 31 , Issue 1 , February 2023 , pp. 44 - 50
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Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abe, H., Yamashita, S., Itoh, T., Satoh, T. and Hoshi, H. (1999). Ultrastructure of bovine embryos developed from in vitro-matured and -fertilized oocytes: Comparative morphological evaluation of embryos cultured either in serum-free medium or in serum-supplemented medium. Molecular Reproduction and Development, 53(3), 325–335. doi: 10.1002/(SICI)1098-2795(199907)53:3<325::AID-MRD8>3.0.CO;2-T 3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Barnett, D. K. and Bavister, B. D. (1996). What is the relationship between the metabolism of preimplantation embryos and their developmental competence? Molecular Reproduction and Development, 43(1), 105–133. doi: 10.1002/(SICI)1098-2795(199601)43:1<105::AID-MRD13>3.0.CO;2-4 3.0.CO;2-4>CrossRefGoogle Scholar
Bavister, B. D., Leibfried, M. L. and Lieberman, G. (1983). Development of preimplantation embryos of the golden hamster in a defined culture medium. Biology of Reproduction, 28(1), 235–247. doi: 10.1095/biolreprod28.1.235 CrossRefGoogle Scholar
Behringer, R., Gertsenstein, M., Vintersten, K. and Nagy, A. (2003). Manipulating the Mouse Embryo – A Laboratory Manual. Third Edition. Cold Spring Harbor Laboratory Press.Google Scholar
Canizo, J. R., Ynsaurralde Rivolta, A. E., Vazquez Echegaray, C., Suvá, M., Alberio, V., Aller, J. F., Guberman, A. S., Salamone, D. F., Alberio, R. H. and Alberio, R. (2019). A dose-dependent response to MEK inhibition determines hypoblast fate in bovine embryos. BMC Developmental Biology, 19(1), 13. doi: 10.1186/s12861-019-0193-9 CrossRefGoogle ScholarPubMed
Chi, F., Sharpley, M. S., Nagaraj, R., Roy, S. S., and Banerjee, U. (2020). Glycolysis-independent glucose metabolism distinguishes TE from ICM fate during mammalian embryogenesis. Developmental Cell, 53(1), 9–26.e4. doi: 10.1016/j.devcel.2020.02.015 CrossRefGoogle ScholarPubMed
de Sousa, R. V., da Silva Cardoso, C. R., Butzke, G., Dode, M. A. N., Rumpf, R. and Franco, M. M. (2017). Biopsy of bovine embryos produced in vivo and in vitro does not affect pregnancy rates. Theriogenology, 90, 25–31. doi: 10.1016/j.theriogenology.2016.11.003 CrossRefGoogle Scholar
Dumollard, R., Ward, Z., Carroll, J. and Duchen, M. R. (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development, 134(3) (March), 455–465. doi: 10.1242/dev.02744 CrossRefGoogle ScholarPubMed
Farin, C. E., Farin, P. W. and Piedrahita, J. A. (2004). Development of fetuses from in vitro-produced and cloned bovine embryos. Journal of Animal Science, 82(E Suppl), E53–E62. doi: 10.2527/2004.8213_supplE53x Google ScholarPubMed
Ferré, L. B., Kjelland, M. E., Taiyeb, A. M., Campos-Chillon, F. and Ross, P. J. (2020). Recent progress in bovine in vitro-derived embryo cryotolerance: Impact of in vitro culture systems, advances in cryopreservation and future considerations. Reproduction in Domestic Animals, 55(6), 659–676. doi: 10.1111/rda.13667 CrossRefGoogle ScholarPubMed
Frankenberg, S., Gerbe, F., Bessonnard, S., Belville, C., Pouchin, P., Bardot, O. and Chazaud, C. (2011). Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Developmental Cell, 21(6), 1005–1013. doi: 10.1016/j.devcel.2011.10.019 CrossRefGoogle Scholar
Frankenberg, S. R., de Barros, F. R. O., Rossant, J. and Renfree, M. B. (2016). The mammalian blastocyst. Developmental Biology, 5(2), 210–232. doi: 10.1002/wdev.220 Google ScholarPubMed
Galetic, I., Maira, S. M., Andjelkovic, M. and Hemmings, B. A. (2003). Negative regulation of ERK and Elk by protein kinase B modulates c-fos transcription. Journal of Biological Chemistry, 278(7), 4416–4423. doi: 10.1074/jbc.M210578200 CrossRefGoogle ScholarPubMed
Gardner, D. K. and Lane, M. (1993). Amino acids and ammonium regulate mouse embryo development in culture. Biology of Reproduction, 48(2), 377–385. doi: 10.1095/biolreprod48.2.377 CrossRefGoogle ScholarPubMed
Gómez, E., Rodríguez, A., Muñoz, M., Caamaño, J. N., Hidalgo, C. O., Morán, E., Facal, N. and Díez, C. (2008). Serum free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification. Theriogenology, 69(8), 1013–1021. doi: 10.1016/j.theriogenology.2007.12.015 CrossRefGoogle ScholarPubMed
Gopichandran, N. and Leese, H. J. (2003). Metabolic characterization of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid. Reproduction, 126(3), 299–308. doi: 10.1530/rep.0.1260299 CrossRefGoogle ScholarPubMed
Gordon, I. (2003). Laboratory production of cattle embryos. CABI Publishing. Available online: doi: 10.1079/9780851996660.0000 CrossRefGoogle Scholar
Herrick, J. R., Rajput, S., Pasquariello, R., Ermisch, A., Santiquet, N., Schoolcraft, W. B. and Krisher, R. L. (2020). Developmental and molecular response of bovine embryos to reduced nutrients in vitro . Reproduction and Fertility, 1(1), 51–65. doi: 10.1530/RAF-20-0033 CrossRefGoogle ScholarPubMed
Houghton, F. D. (2006). Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation; Research in Biological Diversity, 74(1), 11–18. doi: 10.1111/j.1432-0436.2006.00052.x CrossRefGoogle ScholarPubMed
Jacobsen, H., Schmidt, M., Holm, P., Sangild, P. T., Vajta, G., Greve, T. and Callesen, H. (2000). Body dimensions and birth and organ weights of calves derived from in vitro produced embryos cultured with or without serum and oviduct epithelium cells. Theriogenology, 53(9), 1761–1769. doi: 10.1016/S0093-691X(00)00312-5 CrossRefGoogle ScholarPubMed
Kang, M., Piliszek, A., Artus, J. and Hadjantonakis, A. K. (2013). FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development, 140(2), 267–279. doi: 10.1242/dev.084996 CrossRefGoogle Scholar
Kim, J. Y., Burghardt, R. C., Wu, G., Johnson, G. A., Spencer, T. E. and Bazer, F. W. (2011). Select nutrients in the ovine uterine lumen. VII. Effects of arginine, leucine, glutamine, and glucose on trophectoderm cell signaling, proliferation, and migration. Biology of Reproduction, 84(1), 62–69. doi: 10.1095/biolreprod.110.085738 CrossRefGoogle ScholarPubMed
Kim, J., Song, G., Wu, G. and Bazer, F. W. (2012). Functional roles of fructose. Proceedings of the National Academy of Sciences of the United States of America, 109(25), E1619–E1628. doi: 10.1073/pnas.1204298109 Google ScholarPubMed
Koo, D. B., Kang, Y. K., Choi, Y. H., Park, J. S., Kim, H. N., Oh, K. B., Son, D. S., Park, H., Lee, K. K. and Han, Y. M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biology of Reproduction, 67(2), 487–492. doi: 10.1095/biolreprod67.2.487 CrossRefGoogle ScholarPubMed
Krisher, R. L., Lane, M. and Bavister, B. D. (1999). Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media. Biology of Reproduction, 60(6), 1345–1352. doi: 10.1095/biolreprod60.6.1345 CrossRefGoogle ScholarPubMed
Kuijk, E. W., van Tol, L. T. A., van de Velde, H., Wubbolts, R., Welling, M., Geijsen, N. and Roelen, B. A. J. (2012). The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development, 139(5), 871–882. doi: 10.1242/dev.071688 CrossRefGoogle ScholarPubMed
Lanner, F., Lee, K. L., Sohl, M., Holmborn, K., Yang, H., Wilbertz, J., Poellinger, L., Rossant, J. and Farnebo, F. (2010). Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells, 28(2), 191–200. doi: 10.1002/stem.265 CrossRefGoogle Scholar
Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H. and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biology of Reproduction, 67(3), 767–775. doi: 10.1095/biolreprod.102.004481 CrossRefGoogle Scholar
Lee, E. S., Fukui, Y., Lee, B. C., Lim, J. M. and Hwang, W. S. (2004). Promoting effect of amino acids added to a chemically defined medium on blastocyst formation and blastomere proliferation of bovine embryos cultured in vitro . Animal Reproduction Science, 84(3–4), 257–267. doi: 10.1016/j.anireprosci.2004.02.003 CrossRefGoogle ScholarPubMed
Leese, H. J. (2012). Metabolism of the preimplantation embryo: 40 years on. Reproduction, 143(4), 417–427. doi: 10.1530/REP-11-0484 CrossRefGoogle Scholar
Martin, K. L. and Leese, H. J. (1995). Role of glucose in mouse preimplantation embryo development. Molecular Reproduction and Development, 40(4), 436–443. doi: 10.1002/mrd.1080400407 CrossRefGoogle ScholarPubMed
Mesalam, A., Kong, R., Khan, I., Chowdhury, M., Choi, B. H., Kim, S. W., Cho, K. W., Jin, J. I. and Kong, I. K. (2017). Effect of charcoal:dextran stripped fetal bovine serum on in vitro development of bovine embryos. Reproductive Biology, 17(4), 312–319. doi: 10.1016/j.repbio.2017.09.002 CrossRefGoogle ScholarPubMed
Navarrete Santos, A., Ramin, N., Tonack, S. and Fischer, B. (2008). Cell lineage-specific signaling of insulin and insulin-like growth factor I in rabbit blastocysts. Endocrinology, 149(2), 515–524. doi: 10.1210/en.2007-0821 CrossRefGoogle ScholarPubMed
Parrish, J. J., Susko-Parrish, J., Winer, M. A. and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biology of Reproduction, 38(5), 1171–1180. doi: 10.1095/biolreprod38.5.1171 CrossRefGoogle ScholarPubMed
Rizos, D., Fair, T., Papadopoulos, S., Boland, M. P. and Lonergan, P. (2002). Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro . Molecular Reproduction and Development, 62(3), 320–327. doi: 10.1002/mrd.10138 CrossRefGoogle ScholarPubMed
Saeki, K., Hoshi, M., Leibfried-Rutledge, M. L. and First, N. L. (1991). In vitro fertilization and development of bovine oocytes matured in serum-free medium. Biology of Reproduction, 44(2), 256–260. doi: 10.1095/biolreprod44.2.256 CrossRefGoogle ScholarPubMed
Saiz, N., Kang, M., Schrode, N., Lou, X. and Hadjantonakis, A. K. (2016a). Quantitative analysis of protein expression to study lineage specification in mouse preimplantation embryos. Journal of Visualized Experiments: JoVE, 108(108), 53654. doi: 10.3791/53654 Google Scholar
Saiz, N., Williams, K. M., Seshan, V. E. and Hadjantonakis, A. K. (2016b). Asynchronous fate decisions by single cells collectively ensure consistent lineage composition in the mouse blastocyst. Nature Communications, 7, 13463. doi: 10.1038/ncomms13463 CrossRefGoogle ScholarPubMed
Santos, É., Fonseca Junior, A., Lima, C. B., Ispada, J., Silva, J. and Milazzotto, M. P. (2021) Less is more: Reduced nutrient concentration during in vitro culture improves embryo production rates and morphophysiology of bovine embryos. Theriogenology, 173, 37–47. doi: 10.1016/j.theriogenology.2021.07.010 CrossRefGoogle ScholarPubMed
Steeves, T. E. and Gardner, D. K. (1999). Temporal and differential effects of amino acids on bovine embryo development in culture. Biology of Reproduction, 61(3), 731–740. doi: 10.1095/biolreprod61.3.731 CrossRefGoogle ScholarPubMed
Stringfellow, D. A., Givens, M. D. and Waldrop, J. G. (2004). Biosecurity issues associated with current and emerging embryo technologies. Reproduction, Fertility, and Development, 16(1–2), 93–102. doi: 10.10371/RD03082 CrossRefGoogle ScholarPubMed
Thompson, J. G. (2000). In vitro culture and embryo metabolism of cattle and sheep embryos — A decade of achievement. Animal Reproduction Science, 60–61, 263–275. doi: 10.1016/s0378-4320(00)00096-8 CrossRefGoogle ScholarPubMed
Van Langendonckt, A., Donnay, I., Schuurbiers, N., Auquier, P., Carolan, C., Massip, A. and Dessy, F. (1997). Effects of supplementation with fetal calf serum on development of bovine embryos in synthetic oviduct fluid medium. Journal of Reproduction and Fertility, 109(1), 87–93. doi: 10.1530/jrf.0.1090087 CrossRefGoogle ScholarPubMed
van Wagtendonk-de Leeuw, A. M., Mullaart, E., de Roos, A. P. W., Merton, J. S., den Daas, J. H., Kemp, B. and de Ruigh, L. (2000). Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring. Theriogenology, 53(2), 575–597. doi: 10.1016/s0093-691x(99)00259-9 CrossRefGoogle ScholarPubMed
Wang, H., Cao, W., Hu, H., Zhou, C., Wang, Z., Alam, N., Qu, P. and Liu, E. (2022). Effects of changing culture medium on preimplantation embryo development in rabbit. Zygote, 30(3), 338–343. doi: 10.1017/S0967199421000721 CrossRefGoogle ScholarPubMed
Yamanaka, Y., Lanner, F. and Rossant, J. (2010). FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development, 137(5), 715–724. doi: 10.1242/dev.043471 CrossRefGoogle ScholarPubMed
Zheng, X., Baker, H., Hancock, W. S., Fawaz, F., McCaman, M. and Pungor, E. (2006). Proteomic analysis for the assessment of different lots of fetal bovine serum as a raw material for cell culture. Part IV. Application of proteomics to the manufacture of biological drugs. Biotechnology Progress, 22(5), 1294–1300. doi: 10.1021/bp060121o CrossRefGoogle Scholar