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Physical parameters of bovine activated oocytes and zygotes as predictors of development success

Published online by Cambridge University Press:  19 March 2021

Claire L. Timlin ,
Alexa Lynn ,
Lydia K. Wooldridge ,
Kyungjun Uh ,
Alan D. Ealy ,
Robin R. White ,
Kiho Lee  and
Vitor R.G. Mercadante Open the ORCID record for Vitor R.G. Mercadante [Opens in a new window]
Claire L. Timlin
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA
Alexa Lynn
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA
Lydia K. Wooldridge
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA
Kyungjun Uh
Affiliation:
Division of Animal Sciences, University of Columbia, MO65211, USA
Alan D. Ealy
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA
Robin R. White
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA
Kiho Lee
Affiliation:
Division of Animal Sciences, University of Columbia, MO65211, USA
Vitor R.G. Mercadante*
Affiliation:
Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA24061USA Virginia-Maryland College of Veterinary Medicine, Large Animal Clinical Sciences, Blacksburg, VA24061, USA
*
Author for correspondence: Vitor R. G. Mercadante. Department of Animal and Poultry Sciences, 175 W Campus Drive, 364 Litton-Reaves Hall (0306), Blacksburg, VA24061, USA. E-mail: [email protected]
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Summary

The worldwide production of in vitro-produced embryos in livestock species continues to grow. The current gold standard for selecting quality oocytes and embryos is morphologic assessment, yet this method is subjective and varies based on experience. There is a need for a non-invasive, objective method of selecting viable oocytes and embryos. The aim of this study was to determine if ooplasm area, diameter including zona pellucida (ZP), and ZP thickness of artificially activated oocytes and in vitro fertilized (IVF) zygotes are indicative of development success in vitro and correlated with embryo quality, as assessed by total blastomere number. Diameter affected the probability of development to the blastocyst stage in activated oocytes on day 7 (P < 0.01) and day 8 (P < 0.001), and had a tendency to affect IVF zygotes on day 8 (P = 0.08). Zona pellucida thickness affected the probability of development on day 7 (P < 0.01) and day 8 (P < 0.001) in activated oocytes, and day 8 for IVF zygotes (P < 0.05). An interaction between ZP thickness and diameter was observed on days 7 and 8 (P < 0.05) in IVF zygotes. Area did not significantly affect the probability of development, but was positively correlated with blastomere number on day 8 for IVF zygotes (P = 0.01, conditional R2 = 0.09). Physical parameters of bovine zygotes have the potential for use as a non-invasive, objective selection method. Upon further development, methods used in this study could be integrated into embryo production systems to improve IVF success.

Keywords

Artificial activationBovineIn vitro developmentZygote size
Type
Research Article
Information
Zygote , Volume 29 , Issue 5 , October 2021 , pp. 358 - 364
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Báez, F, Camargo, Á and Gastal, G (2019). Ultrastructural imaging analysis of the zona pellucida surface in bovine oocytes. Microsc Microanal 25, 1032–6.CrossRefGoogle ScholarPubMed
Balakier, H, Sojecki, A, Motamedi, G, Bashar, S, Mandel, R and Librach, C (2012). Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels? Fertil Steril 98, 77–83.CrossRefGoogle ScholarPubMed
Balasubramanian, S, Son, WJ, Kumar, B M, Ock, SA, Yoo, JG, Im, GS, Choe, SY and Rho, GJ (2007). Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology 68, 265–75.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, B and Walker, S (2015). Fitting linear mixed-effects models using lme4. J Stat Softw 67, doi: 10.18637/jss.v067.i01.CrossRefGoogle Scholar
Baxter Bendus, AE, Mayer, JF, Shipley, K and Catherino, WH (2006). Interobserver and intraobserver variation in day 3 embryo grading. Fertil Steril 86, 1608–15.CrossRefGoogle ScholarPubMed
Bertrand, E, Van den Bergh, M and Englert, Y (1995). Does zona pellucida thickness influence the fertilization rate? Hum Reprod 10, 1189–93.CrossRefGoogle ScholarPubMed
Booth, PJ, Viuff, D, Tan, S, Holm, P, Greve, T and Callesen, H (2003). Numerical chromosome errors in day 7 somatic nuclear transfer bovine blastocysts. Biol Reprod 68, 922–8.CrossRefGoogle ScholarPubMed
Choi, BH, Bang, JI, Jin, JI, Kim, SS, Jo, HT, Deb, GK, Ghanem, N, Cho, KW and Kong, IK (2013). Coculturing cumulus–oocyte complexes with denuded oocytes alters zona pellucida ultrastructure in in vitro matured bovine oocytes. Theriogenology 80, 1117–23.CrossRefGoogle ScholarPubMed
Coticchio, G, Mignini Renzini, M, Novara, P V, Lain, M, De Ponti, E, Turchi, D, Fadini, R and Dal Canto, M (2017). Focused time-lapse analysis reveals novel aspects of human fertilization and suggests new parameters of embryo viability. Hum Reprod 33, 23–31.CrossRefGoogle Scholar
Cruz, M, Garrido, N, Herrero, J, Perez-Cano, I, Muñoz, M and Meseguer, M (2012). Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod BioMed Online 25, 371–81.CrossRefGoogle ScholarPubMed
Denicol, AC, Block, J, Kelley, DE, Pohler, KG, Dobbs, KB, Mortensen, CJ, Ortega, MS and Hansen, PJ (2014). The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo. FASEB J 28, 3975–86.CrossRefGoogle ScholarPubMed
Durinzi, KL, Saniga, EM and Lanzendorf, SE (1995). The relationship between size and maturation in vitro in the unstimulated human oocyte. Fertil Steril 63, 404–6.CrossRefGoogle ScholarPubMed
Ealy, AD, Wooldridge, LK and McCoski, SR (2019). Post-transfer consequences of in vitro-produced embryos in cattle. J Anim Sci 97, 2555–68.CrossRefGoogle ScholarPubMed
Fair, T, Hyttel, P and Greve, T (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42, 437–42.CrossRefGoogle ScholarPubMed
Farin, PW, Britt, JH, Shaw, DW and Slenning, BD (1995). Agreement among evaluators of bovine embryos produced in vivo or in vitro . Theriogenology 44, 339–49.CrossRefGoogle ScholarPubMed
Fields, SD, Hansen, PJ and Ealy, AD (2011). Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75, 1466–75.CrossRefGoogle ScholarPubMed
Gardner, DK and Wale, PL (2013). Analysis of metabolism to select viable human embryos for transfer. Fertil Steril 99, 1062–72.CrossRefGoogle ScholarPubMed
Gómez, E, Gutiérrez-Adán, A, Díez, C, Bermejo-Alvarez, P, Muñoz, M, Rodriguez, A, Otero, J, Alvarez-Viejo, M, Martín, D, Carrocera, S and Caamaño, JN (2009). Biological differences between in vitro produced bovine embryos and parthenotes. Reproduction 137, 285–95.CrossRefGoogle ScholarPubMed
Gutiérrez-Adán, A, White, CR, Van Soom, A and Mann, MR (2015). Why we should not select the faster embryo: lessons from mice and cattle. Reprod Fertil Dev 27, 765–75.CrossRefGoogle Scholar
Hasler, JF (2000). In-vitro production of cattle embryos: problems with pregnancies and parturition. Hum Reprod 15 (Suppl 5), 47–58.CrossRefGoogle ScholarPubMed
Hazeleger, NL Hill, DJ Stubbing, RB and Walton, JS (1995). Relationship of morphology and follicular fluid environment of bovine oocytes to their developmental potential in vitro . Theriogenology 43, 509–22.CrossRefGoogle ScholarPubMed
Hirao, Y, Nagai, T, Kubo, M, Miyano, T, Miyake, M and Kato, S (1994). In vitro growth and maturation of pig oocytes. J Reprod Fertil 100, 333–9.CrossRefGoogle ScholarPubMed
Hoelker, M, Schmoll, F, Schneider, H, Rings, F, Gilles, M, Tesfaye, D, Jennen, D, Tholen, E, Griese, J and Schellander, K (2006). Bovine blastocyst diameter as a morphological tool to predict embryo cell counts, embryo sex, hatching ability and developmental characteristics after transfer to recipients. Reprod Fertil Dev 18, 551–7.CrossRefGoogle ScholarPubMed
Jiang, H, Wang, W, Lu, K, Gordon, I and Polge, C (1992). Examination of cell numbers of blastocysts derived from IVM, IVF and IVC of bovine follicular oocytes. Theriogenology 37, 229.CrossRefGoogle Scholar
Knijn, HM, Gjørret, JO, Vos, PLAM, Hendriksen, PJM, van der Weijden, BC, Maddox-Hyttel, P and Dieleman, SJ (2003). Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol Reprod 69, 1371–8.CrossRefGoogle ScholarPubMed
Kyogoku, H and Kitajima, TS (2017). Large cytoplasm is linked to the error-prone nature of oocytes. Dev Cell 41, 287–98.e284.CrossRefGoogle ScholarPubMed
Lamb, GC and Mercadante, VR (2014). Selection and management of the embryo recipient herd for embryo transfer. In Hopper, RM (ed.) Bovine Reproduction, pp. 723–732. Wiley Online Library.CrossRefGoogle Scholar
Liang, L, Wang, CT, Sun, X, Liu, L, Li, M, Witz, C, Williams, D, Griffith, J, Skorupski, J, Haddad, G, Gill, J and Wang, WH (2013). Identification of chromosomal errors in human preimplantation embryos with oligonucleotide DNA microarray. PLoS One, 8, e61838.CrossRefGoogle ScholarPubMed
Lundin, K, Bergh, C and Hardarson, T (2001). Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum Reprod 16, 2652–7.CrossRefGoogle ScholarPubMed
Matsuura, K, Hayashi, N, Takiue, C, Hirata, R, Habara, T and Naruse, K (2010). Blastocyst quality scoring based on morphologic grading correlates with cell number. Fertil Steril 94, 1135–7.CrossRefGoogle ScholarPubMed
Mori, M, Otoi, T and Suzuki, T (2002). Correlation between the cell number and diameter in bovine embryos produced in vitro . Reprod Domest Anim 37, 181–4.CrossRefGoogle ScholarPubMed
Nagano, M, Katagiri, S and Takahashi, Y (2006). Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.CrossRefGoogle ScholarPubMed
Nakada, K and Mizuno, J (1998). Intracellular calcium responses in bovine oocytes induced by spermatozoa and by reagents. Theriogenology 50, 269–82.CrossRefGoogle ScholarPubMed
O’Doherty, AM, O’Shea, LC and Fair, T (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol Reprod 86, 67.Google Scholar
Ortega, MS, Moraes, JGN, Patterson, DJ, Smith, MF, Behura, SK, Poock, S and Spencer, TE (2018). Influences of sire conception rate on pregnancy establishment in dairy cattle†. Biol Reprod 99, 1244–54.CrossRefGoogle Scholar
Otoi, T, Yamamoto, K, Koyama, N, Tachikawa, S and Suzuki, T (1997). Bovine oocyte diameter in relation to developmental competence. Theriogenology 48, 769–74.CrossRefGoogle ScholarPubMed
Papaioannou, V and Ebert, K (1988). The preimplantation pig embryo: cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro . Development 102, 793–803.CrossRefGoogle ScholarPubMed
R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Raghu, HM, Nandi, S and Reddy, SM (2002). Follicle size and oocyte diameter in relation to developmental competence of buffalo oocytes in vitro . Reprod Fertil Dev 14, 55–61.CrossRefGoogle ScholarPubMed
Sakatani, M, Alvarez, NV, Takahashi, M and Hansen, PJ (2012). Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J Dairy Sci 95, 3080–91.CrossRefGoogle Scholar
Sanchez, T, Seidler, EA, Gardner, DK, Needleman, D and Sakkas, D (2017). Will noninvasive methods surpass invasive for assessing gametes and embryos? Fertil Steril 108, 730–7.CrossRefGoogle ScholarPubMed
Santos, P, Chaveiro, A, Simoes, N and Moreira da Silva, F (2008). Bovine oocyte quality in relation to ultrastructural characteristics of zona pellucida, polyspermic penetration and developmental competence. Reprod Domest Anim 43, 685–9.CrossRefGoogle ScholarPubMed
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, C, Saalfeld, S, Schmid, B, Tinevez, JY, White, DJ, Hartenstein, V, Eliceiri, K, Tomancak, P and Cardona, A (2012). Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676.CrossRefGoogle ScholarPubMed
Siqueira, AFP, de Castro, LS, de Assis, PM, Bicudo, L d C, Mendes, CM, Nichi, M, Visintin, JA and Assumpção MEODÁ (2018). Sperm traits on in vitro production (IVP) of bovine embryos: Too much of anything is good for nothing. PLoS One 13, e0200273.CrossRefGoogle Scholar
Soloy, E, Srsen, V, Pavlok, A, Hyttel, P, Thomsen, PD, Smith, SD, Prochazka, R, Kubelka, M, Hoier, R, Booth, P, Motlik, J and Greve, T (1997). Establishment of the block against sperm penetration in parthenogenetically activated bovine oocytes matured in vitro . J Reprod Fertil 111, 151–7.CrossRefGoogle ScholarPubMed
Susko-Parrish, JL, Leibfried-Rutledge, ML, Northey, DL, Schutzkus, V and First, NL (1994). Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Dev Biol 166, 729–39.CrossRefGoogle ScholarPubMed
Suzuki, H, Yang, X and Foote, RH (1994). Surface alterations of the bovine oocyte and its investments during and after maturation and fertilization in vitro . Mol Reprod Dev 38, 421–30.CrossRefGoogle ScholarPubMed
Tartia, AP, Rudraraju, N, Richards, T, Hammer, MA, Talbot, P and Baltz, JM (2009). Cell volume regulation is initiated in mouse oocytes after ovulation. Development 136, 2247–54.CrossRefGoogle ScholarPubMed
Tejera, A, Herrero, J, Viloria, T, Romero, JL, Gamiz, P and Meseguer, M (2012). Time-dependent O2 consumption patterns determined optimal time ranges for selecting viable human embryos. Fertil Steril 98, 849–57.e841–3.CrossRefGoogle ScholarPubMed
Vajta, G, Korösi, T, Du, Y, Nakata, K, Ieda, S, Kuwayama, M and Nagy, ZP (2008). The well-of-the-well system: an efficient approach to improve embryo development. Reprod BioMed Online 17, 73–81.CrossRefGoogle ScholarPubMed
Viana, J (2018). 2017 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter 36, 8–25.Google Scholar
Viuff, D, Greve, T, Avery, B, Hyttel, P, Brockhoff, PB and Thomsen, PD (2000). Chromosome aberrations in in vitro-produced bovine embryos at days 2–5 post-insemination. Biol Reprod 63, 1143–8.CrossRefGoogle ScholarPubMed
Walls, ML, Hart, R, Keelan, JA and Ryan, JP (2016). Structural and morphologic differences in human oocytes after in vitro maturation compared with standard in vitro fertilization. Fertil Steril 106, 1392–8.e1395.CrossRefGoogle ScholarPubMed
Wooldridge, LK and Ealy, AD (2019). Interleukin-6 increases inner cell mass numbers in bovine embryos. BMC Dev Biol 19, 2.CrossRefGoogle ScholarPubMed
Xie, M, McCoski, SR, Johnson, SE, Rhoads, ML and Ealy, AD (2017). Combinatorial effects of epidermal growth factor, fibroblast growth factor 2 and insulin-like growth factor 1 on trophoblast cell proliferation and embryogenesis in cattle. Reprod Fertil Dev 29, 419–30.CrossRefGoogle ScholarPubMed