Effect of arachidonic acid on pre- and post-hatching in vitro bovine embryo development
L. González-Brusi A , A. Pérez-Gómez A , A. C. Quiroga A , C. Tamargo B , P. Ramos-Ibeas A and P. Bermejo-Álvarez A *A Animal Reproduction Department, INIA, CSIC, Madrid 28040, Spain.
B Department of Animal Selection and Reproduction, SERIDA, Gijón 33394, Spain.
Reproduction, Fertility and Development 35(12) 614-621 https://doi.org/10.1071/RD23053
Published online: 11 July 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: Arachidonic acid (AA) is the precursor of prostaglandins, which may play autocrine roles during early embryo development.
Aims: To test the developmental effects of addition of AA to pre- and post-hatching culture media on in vitro–produced bovine embryos.
Methods: Pre-hatching effects of AA were tested by culturing bovine zygotes in synthetic oviductal fluid (SOF) supplemented with 100 or 333 μM AA. Post-hatching effects of AA were tested by culturing Day 7 blastocysts in N2B27 supplemented with 5, 10, 20 or 100 μM AA up to Day 12.
Key results: Pre-hatching development to blastocyst was completely abrogated at 333 μM AA, whereas blastocyst rates and cell numbers were not altered at 100 μM AA. Impaired post-hatching development was observed at 100 μM AA, whereas no effect on survival rates was noted at 5, 10 and 20 μM AA. However, a significant reduction in Day 12 embryo size was observed at 10 and 20 μM AA. Hypoblast migration, epiblast survival and formation of embryonic-disc-like structures were unaffected at 5–10 μM AA. AA exposure downregulated the genes PTGIS, PPARG, LDHA and SCD in Day 12 embryos.
Conclusions: Pre-hatching embryos are mostly irresponsive to AA, whereas AA was observed to have negative effects during early post-hatching development.
Implications: AA does not improve in vitro bovine embryo development and is not required up to early post-hatching stages.
Keywords: arachidonic, bovine, conceptus, elongation, embryo development, lipids, PPARG, prostaglandin, SCD, trophectoderm.
References
Berg, DK, van Leeuwen, J, Beaumont, S, Berg, M, and Pfeffer, PL (2010). Embryo loss in cattle between Days 7 and 16 of pregnancy. Theriogenology 73, 250–260.| Embryo loss in cattle between Days 7 and 16 of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Bermejo-Alvarez, P, Rizos, D, Rath, D, Lonergan, P, and Gutierrez-Adan, A (2010a). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proceedings of the National Academy of Sciences 107, 3394–3399.
| Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar |
Bermejo-Alvarez, P, Lonergan, P, Rizos, D, and Gutierrez-Adan, A (2010b). Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis. Reproductive BioMedicine Online 20, 341–349.
| Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis.Crossref | GoogleScholarGoogle Scholar |
Bermejo-Alvarez, P, Rizos, D, Lonergan, P, and Gutierrez-Adan, A (2011). Transcriptional sexual dimorphism in elongating bovine embryos: implications for XCI and sex determination genes. Reproduction 141, 801–808.
| Transcriptional sexual dimorphism in elongating bovine embryos: implications for XCI and sex determination genes.Crossref | GoogleScholarGoogle Scholar |
Bermejo-Alvarez, P, Roberts, RM, and Rosenfeld, CS (2012). Effect of glucose concentration during in vitro culture of mouse embryos on development to blastocyst, success of embryo transfer, and litter sex ratio. Molecular Reproduction and Development 79, 329–336.
| Effect of glucose concentration during in vitro culture of mouse embryos on development to blastocyst, success of embryo transfer, and litter sex ratio.Crossref | GoogleScholarGoogle Scholar |
Cammas, L, Reinaud, P, Bordas, N, Dubois, O, Germain, G, and Charpigny, G (2006). Developmental regulation of prostacyclin synthase and prostacyclin receptors in the ovine uterus and conceptus during the peri-implantation period. Reproduction 131, 917–927.
| Developmental regulation of prostacyclin synthase and prostacyclin receptors in the ovine uterus and conceptus during the peri-implantation period.Crossref | GoogleScholarGoogle Scholar |
Desvergne, B, and Wahli, W (1999). Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocrine Reviews 20, 649–688.
| Peroxisome proliferator-activated receptors: nuclear control of metabolism.Crossref | GoogleScholarGoogle Scholar |
Dieleman, SJ, Hendriksen, PJM, Viuff, D, Thomsen, PD, Hyttel, P, Knijn, HM, Wrenzycki, C, Kruip, TAM, Niemann, H, Gadella, BM, Bevers, MM, and Vos, PLAM (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 5–20.
| Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos.Crossref | GoogleScholarGoogle Scholar |
Diskin, MG, and Morris, DG (2008). Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals 43, 260–267.
| Embryonic and early foetal losses in cattle and other ruminants.Crossref | GoogleScholarGoogle Scholar |
Dorniak, P, Bazer, FW, and Spencer, TE (2011). Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biology of Reproduction 84, 1119–1127.
| Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium.Crossref | GoogleScholarGoogle Scholar |
Dunne, LD, Diskin, MG, and Sreenan, JM (2000). Embryo and foetal loss in beef heifers between day 14 of gestation and full term. Animal Reproduction Science 58, 39–44.
| Embryo and foetal loss in beef heifers between day 14 of gestation and full term.Crossref | GoogleScholarGoogle Scholar |
Forde, N, Carter, F, Spencer, TE, Bazer, FW, Sandra, O, Mansouri-Attia, N, Okumu, LA, McGettigan, PA, Mehta, JP, McBride, R, O’Gaora, P, Roche, JF, and Lonergan, P (2011). Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biology of Reproduction 85, 144–156.
| Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant?Crossref | GoogleScholarGoogle Scholar |
Holm, P, Booth, PJ, Schmidt, MH, Greve, T, and Callesen, H (1999). High bovine blastocyst development in a static in vitro production system using sofaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.
| High bovine blastocyst development in a static in vitro production system using sofaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins.Crossref | GoogleScholarGoogle Scholar |
Hwang, DH, Pool, SH, Rorie, RW, Boudreau, M, and Godke, RA (1988). Transitional changes in arachidonic acid metabolism by bovine embryos at different developmental stages. Prostaglandins 35, 387–402.
| Transitional changes in arachidonic acid metabolism by bovine embryos at different developmental stages.Crossref | GoogleScholarGoogle Scholar |
Lee, J, McCracken, JA, Stanley, JA, Nithy, TK, Banu, SK, and Arosh, JA (2012). Intraluteal prostaglandin biosynthesis and signaling are selectively directed towards PGF2alpha during luteolysis but towards PGE2 during the establishment of pregnancy in sheep. Biology of Reproduction 87, 97.
| Intraluteal prostaglandin biosynthesis and signaling are selectively directed towards PGF2alpha during luteolysis but towards PGE2 during the establishment of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Lewis, GS, Thatcher, WW, Bazer, FW, and Curl, JS (1982). Metabolism of arachidonic acid in vitro by bovine blastocysts and endometrium. Biology of Reproduction 27, 431–439.
| Metabolism of arachidonic acid in vitro by bovine blastocysts and endometrium.Crossref | GoogleScholarGoogle Scholar |
Lim, JM, and Hansel, W (1996). Roles of growth factors in the development of bovine embryos fertilized in vitro and cultured singly in a defined medium. Reproduction, Fertility and Development 8, 1199–1205.
| Roles of growth factors in the development of bovine embryos fertilized in vitro and cultured singly in a defined medium.Crossref | GoogleScholarGoogle Scholar |
Lim, JM, and Hansel, W (2000). Exogeneous substances affecting development of in vitro-derived bovine embryos before and after embryonic genome activation. Theriogenology 53, 1081–1091.
| Exogeneous substances affecting development of in vitro-derived bovine embryos before and after embryonic genome activation.Crossref | GoogleScholarGoogle Scholar |
Liu, T, Li, J, Yu, L, Sun, H-X, Li, J, Dong, G, Hu, Y, Li, Y, Shen, Y, Wu, J, and Gu, Y (2021). Cross-species single-cell transcriptomic analysis reveals pre-gastrulation developmental differences among pigs, monkeys, and humans. Cell Discovery 7, 8.
| Cross-species single-cell transcriptomic analysis reveals pre-gastrulation developmental differences among pigs, monkeys, and humans.Crossref | GoogleScholarGoogle Scholar |
Mamo, S, Mehta, JP, McGettigan, P, Fair, T, Spencer, TE, Bazer, FW, and Lonergan, P (2011). RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biology of Reproduction 85, 1143–1151.
| RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation.Crossref | GoogleScholarGoogle Scholar |
Menezo, Y, Renard, J-P, Delobel, B, and Pageaux, J-F (1982). Kinetic study of fatty acid composition of day 7 to day 14 cow embryos. Biology of Reproduction 26, 787–790.
| Kinetic study of fatty acid composition of day 7 to day 14 cow embryos.Crossref | GoogleScholarGoogle Scholar |
Perez-Gomez, A, Gonzalez-Brusi, L, Bermejo-Alvarez, P, and Ramos-Ibeas, P (2021). Lineage differentiation markers as a proxy for embryo viability in farm ungulates. Frontiers in Veterinary Science 8, 680539.
| Lineage differentiation markers as a proxy for embryo viability in farm ungulates.Crossref | GoogleScholarGoogle Scholar |
Ramos-Ibeas, P, Lamas-Toranzo, I, Martinez-Moro, A, de Frutos, C, Quiroga, AC, Zurita, E, and Bermejo-Alvarez, P (2020). Embryonic disc formation following post-hatching bovine embryo development in vitro. Reproduction 160, 579–589.
| Embryonic disc formation following post-hatching bovine embryo development in vitro.Crossref | GoogleScholarGoogle Scholar |
Ramos-Ibeas, P, Gonzalez-Brusi, L, Used, MT, Cocero, MJ, Marigorta, P, Alberio, R, and Bermejo-Alvarez, P (2022). In vitro culture of ovine embryos up to early gastrulating stages. Development 149, dev199743.
| In vitro culture of ovine embryos up to early gastrulating stages.Crossref | GoogleScholarGoogle Scholar |
Ramos-Ibeas, P, Perez-Gomez, A, Gonzalez-Brusi, L, Quiroga, AC, and Bermejo-Alvarez, P (2023). Pre-hatching exposure to N2B27 medium improves post-hatching development of bovine embryos in vitro. Theriogenology 205, 73–78.
| Pre-hatching exposure to N2B27 medium improves post-hatching development of bovine embryos in vitro.Crossref | GoogleScholarGoogle Scholar |
Reynolds, LP, Robertson, DA, and Ford, SP (1983). Effects of intrauterine infusion of oestradiol-17β and prostaglandin E-2 on luteal function in non-pregnant heifers. Journal of Reproduction and Fertility 69, 703–709.
| Effects of intrauterine infusion of oestradiol-17β and prostaglandin E-2 on luteal function in non-pregnant heifers.Crossref | GoogleScholarGoogle Scholar |
Ribeiro, ES, Santos, JEP, and Thatcher, WW (2016a). Role of lipids on elongation of the preimplantation conceptus in ruminants. Reproduction 152, R115–R126.
| Role of lipids on elongation of the preimplantation conceptus in ruminants.Crossref | GoogleScholarGoogle Scholar |
Ribeiro, ES, Greco, LF, Bisinotto, RS, Lima, FS, Thatcher, WW, and Santos, JE (2016b). Biology of preimplantation conceptus at the onset of elongation in dairy cows. Biology of Reproduction 94, 97.
| Biology of preimplantation conceptus at the onset of elongation in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Rizos, D, Ward, F, Duffy, P, Boland, MP, and Lonergan, P (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Molecular Reproduction and Development 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar |
Sergeant, S, Rahbar, E, and Chilton, FH (2016). Gamma-linolenic acid, dihommo-gamma linolenic, eicosanoids and inflammatory processes. European Journal of Pharmacology 785, 77–86.
| Gamma-linolenic acid, dihommo-gamma linolenic, eicosanoids and inflammatory processes.Crossref | GoogleScholarGoogle Scholar |
Simintiras, CA, Sanchez, JM, McDonald, M, and Lonergan, P (2019). Progesterone alters the bovine uterine fluid lipidome during the period of elongation. Reproduction 157, 399–411.
| Progesterone alters the bovine uterine fluid lipidome during the period of elongation.Crossref | GoogleScholarGoogle Scholar |
Simmons, DL, Botting, RM, and Hla, T (2004). Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacological Reviews 56, 387–437.
| Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition.Crossref | GoogleScholarGoogle Scholar |
Song, B-S, Kim, J-S, Kim, C-H, Han, Y-M, Lee, D-S, Lee, K-K, and Koo, D-B (2009). Prostacyclin stimulates embryonic development via regulation of the cAMP response element-binding protein–cyclo-oxygenase-2 signalling pathway in cattle. Reproduction, Fertility and Development 21, 400–407.
| Prostacyclin stimulates embryonic development via regulation of the cAMP response element-binding protein–cyclo-oxygenase-2 signalling pathway in cattle.Crossref | GoogleScholarGoogle Scholar |
Ulbrich, SE, Schulke, K, Groebner, AE, Reichenbach, HD, Angioni, C, Geisslinger, G, and Meyer, HHD (2009). Quantitative characterization of prostaglandins in the uterus of early pregnant cattle. Reproduction 138, 371–382.
| Quantitative characterization of prostaglandins in the uterus of early pregnant cattle.Crossref | GoogleScholarGoogle Scholar |
van de Leemput, EE, Vos, PLAM, Zeinstra, EC, Severs, MM, van der Weijden, GC, and Dieleman, SJ (1999). Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory lh surge. Theriogenology 52, 335–349.
| Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory lh surge.Crossref | GoogleScholarGoogle Scholar |
Weems, YS, Kim, L, Humphreys, V, Tsuda, V, and Weems, CW (2003). Effect of luteinizing hormone (LH), pregnancy specific protein B (PSPB), or arachidonic acid (AA) on ovine endometrium of the estrous cycle or placental secretion of prostaglandins E2 (PGE2) and F2α (PGF2α) and progesterone in vitro. Prostaglandins & Other Lipid Mediators 71, 55–73.
| Effect of luteinizing hormone (LH), pregnancy specific protein B (PSPB), or arachidonic acid (AA) on ovine endometrium of the estrous cycle or placental secretion of prostaglandins E2 (PGE2) and F2α (PGF2α) and progesterone in vitro.Crossref | GoogleScholarGoogle Scholar |
Ying, Q-L, and Smith, AG (2003). Defined conditions for neural commitment and differentiation. Methods in Enzymology 365, 327–341.
| Defined conditions for neural commitment and differentiation.Crossref | GoogleScholarGoogle Scholar |
Zhao, Z-A, Zhang, Z-R, Xu, X, Deng, W-B, Li, M, Leng, J-Y, Liang, X-H, and Yang, Z-M (2012). Arachidonic acid regulation of the cytosolic phospholipase A2α/cyclooxygenase-2 pathway in mouse endometrial stromal cells. Fertility and Sterility 97, 1199–1205.e9.
| Arachidonic acid regulation of the cytosolic phospholipase A2α/cyclooxygenase-2 pathway in mouse endometrial stromal cells.Crossref | GoogleScholarGoogle Scholar |