Consequences of exposure of embryos produced in vitro in a serum-containing medium to dickkopf-related protein 1 and colony stimulating factor 2 on blastocyst yield, pregnancy rate, and birth weight1

Tríbulo, Paula; Ballesteros, Brandon; Ruiz, A.; Tríbulo, A.; Tribulo, R.; Tríbulo, H.; Bó, G. A.; Hansen, Peter J.

doi:10.2527/jas2017.1927

Cited by 28 publications

(30 citation statements)

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“…Indeed, there could be other aspects of development of the blastocyst not studied here, including downstream effects that occur much later in development, that could differ between female and male embryos. Embryokines like CSF2 [ 33 , 34 ] and DKK1 [ 35 ] can act on the preimplantation embryo to affect fetal and postnatal phenotypes. Despite the lack of difference on development to blastocyst stage, the observation that expression of three genes was affected by the IGF1 by sex interaction is indicative that IGF1 might exert sex-dependent actions affecting other aspects of embryo function besides development to the blastocyst stage (e.g., apoptosis, allocation of cells into specific lineages, epigenetic regulation, etc.).…”

Section: Discussionmentioning

confidence: 99%

Effects of sex on response of the bovine preimplantation embryo to insulin-like growth factor 1, activin A, and WNT7A

et al. 2018

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BackgroundAlterations in maternal environment can sometimes affect embryonic development in a sexually-dimorphic manner. The objective was to determine whether preimplantation bovine embryos respond to three maternally-derived cell signaling molecules in a sex-dependent manner.ResultsActions of three embryokines known to increase competence of bovine embryos to develop to the blastocyst stage, insulin-like growth factor 1 (IGF1), activin A, and WNT member 7A (WNT7A), were evaluated for actions on embryos produced in vitro with X- or Y- sorted semen from the same bull. Each embryokine was tested in embryos produced by in vitro fertilization of groups of oocytes with either pooled sperm from two bulls or with sperm from individual bulls. Embryos were treated with IGF1, activin A, or WNT7A on day 5 of culture. All three embryokines increased the proportion of cleaved zygotes that developed to the blastocyst stage and the effect was similar for female and male embryos. As an additional test of sexual dimorphism, effects of IGF1 on blastocyst expression of a total of 127 genes were determined by RT-qPCR using the Fluidigm Delta Gene assay. Expression of 18 genes was affected by sex, expression of 4 genes was affected by IGF1 and expression of 3 genes was affected by the IGF1 by sex interaction.ConclusionSex did not alter how IGF1, activin A or WNT7A altered developmental competence to the blastocyst stage. Thus, sex-dependent differences in regulation of developmental competence of embryos by maternal regulatory signals is not a general phenomenon. The fact that sex altered how IGF1 regulates gene expression is indicative that there could be sexual dimorphism in embryokine regulation of some aspects of embryonic function other than developmental potential to become a blastocyst.Electronic supplementary materialThe online version of this article (10.1186/s12861-018-0176-2) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Effects of sex on response of the bovine preimplantation embryo to insulin-like growth factor 1, activin A, and WNT7A

et al. 2018

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“…Supplementing DKK1 during IVP embryo culture appears beneficial to calving outcomes. Increases in blastocyst development and pregnancy retention occurred in DKK1 treated IVP embryos in one study lacking serum in culture medium (Denicol et al, 2014), but not in another study that utilized a serum-containing medium ( Tríbulo et al, 2017). In the latter study, a reduction in birth weights was observed in calves from DKK1-exposed IVP embryos (Tríbulo et al, 2017).…”

Section: Recent Attempts To Improve Ivp Embryo Competencymentioning

confidence: 87%

“…Increases in blastocyst development and pregnancy retention occurred in DKK1 treated IVP embryos in one study lacking serum in culture medium (Denicol et al, 2014), but not in another study that utilized a serum-containing medium ( Tríbulo et al, 2017). In the latter study, a reduction in birth weights was observed in calves from DKK1-exposed IVP embryos (Tríbulo et al, 2017). The mechanism responsible for this outcome is unclear, but this finding may have important implications for further reducing the incidence of large offspring syndrome in IVP pregnancies.…”

Section: Recent Attempts To Improve Ivp Embryo Competencymentioning

confidence: 91%

“…These large offspring syndrome pregnancies increase the incidence of dystocia and retained placentae (Bonilla et al, 2014), which may compromise future reproductive capacity and milk yield for the dam (Zaborski et al, 2009). The incidence and severity of large offspring syndrome has been reduced, but has not been totally prevented in the past decade by removing serum from embryo culture media formations, by using media formations that replicate the oviduct environment [e.g., synthetic oviductal fluid (SOF)], and by culturing embryos in an oxygen environment similar to that in the oviduct and uterus (van Wagtendonk-de Leeuw et al, 2000;Fischer-Brown et al, 2005;Bonilla et al, 2014;Siqueira et al, 2017;Tríbulo et al, 2017).…”

Section: Calving Outcomes and Performancementioning

confidence: 99%

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BOARD INVITED REVIEW: Post-transfer consequences of in vitro-produced embryos in cattle

Ealy

Wooldridge

McCoski

2019

Journal of Animal Science

127

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In vitro embryo production (IVP) in cattle has gained worldwide interest in recent years, but the efficiency of using IVP embryos for calf production is far from optimal. This review will examine the pregnancy retention rates of IVP embryos and explore causes for pregnancy failures. Based on work completed over the past 25 yr, only 27% of cattle receiving IVP embryos will produce a live calf. Approximately 60% of these pregnancies fail during the first 6 wk of gestation. When compared with embryos generated by superovulation, pregnancy rates are 10% to 40% lower for cattle carrying IVP embryos, exemplifying that IVP embryos are consistently less competent than in vivo-generated embryos. Several abnormalities have been observed in the morphology of IVP conceptuses. After transfer, IVP embryos are less likely to undergo conceptus elongation, have reduced embryonic disk diameter, and have compromised yolk sac development. Marginal binucleate cell development, cotyledon development, and placental vascularization have also been documented, and these abnormalities are associated with altered fetal growth trajectories. Additionally, in vitro culture conditions increase the risk of large offspring syndrome. Further work is needed to decipher how the embryo culture environment alters post-transfer embryo development and survival. The risk of these neonatal disorders has been reduced by the use of serum-free synthetic oviductal fluid media formations and culture in low oxygen tension. However, alterations are still evident in IVP oocyte and embryo transcript abundances, timing of embryonic cleavage events and blastulation, incidence of aneuploidy, and embryonic methylation status. The inclusion of oviductal and uterine-derived embryokines in culture media is being examined as one way to improve the competency of IVP embryos. To conclude, the evidence presented herein clearly shows that bovine IVP systems still must be refined to make it an economical technology in cattle production systems. However, the current shortcomings do not negate its current value for certain embryo production needs and for investigating early embryonic development in cattle.

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“…One possible mediator of the effects of progesterone on embryonic elongation in the ruminant is DKK1, an endogenous modulator of WNT signaling produced by the endometrium 22 . Addition of DKK1 to culture medium improves the ability of bovine embryos to establish and maintain pregnancy after transfer 23 and affects birthweight of offspring 24 . Endometrial expression of DKK1 is induced by progesterone in the cow 3 , sheep 25 and human 26,27 .…”

Section: Introductionmentioning

confidence: 99%

Dickkopf-related protein 1 is a progestomedin acting on the bovine embryo during the morula-to-blastocyst transition to program trophoblast elongation

Tríbulo

Rabaglino

Bo³

et al. 2019

Sci Rep

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Progesterone regulates the endometrium to support pregnancy establishment and maintenance. In the ruminant, one action of progesterone early in pregnancy is to alter embryonic development and hasten the process of trophoblast elongation around day 14–15 of pregnancy, which is required for maternal recognition of pregnancy. Here we demonstrate that the WNT antagonist DKK1, whose expression is increased by progesterone treatment, can act on the bovine embryo during day 5 to 7.5 of development (the morula to blastocyst stage) to promote embryonic elongation on day 15 of pregnancy. Embryos were produced in vitro and exposed to 0 or 100 ng/ml recombinant human DKK1 from day 5 to 7.5 of culture. Blastocysts were transferred into synchronized recipient cows on day 7.5 (n = 23 for control and 17 for DKK1). On day 15, cows were slaughtered and embryos recovered by flushing the uterus. Embryo recovery was n = 11 for controls (48% recovery) and n = 11 for DKK1 (65% recovery). Except for two DKK1 embryos, all embryos were filamentous. Treatment with DKK1 increased (P = 0.007) the length of filamentous embryos from 43.9 mm to 117.4 mm and the intrauterine content of the maternal recognition of pregnancy signal IFNT (P = 0.01) from 4.9 µg to 16.6 µg. Determination of differentially expressed genes (DEG), using the R environment, revealed 473 DEG at p < 0.05 but none at FDR < 0.05, suggesting that DKK1 did not strongly modify the embryo transcriptome at the time it was measured. However, samples clustered apart in a multidimensional scaling analyisis. Weighted gene co-expression analysis of the transcriptome of filamentous embryos revealed a subset of genes that were related to embryo length, with identification of a significant module of genes in the DKK1 group only. Thus, several of the differences between DKK1 and control groups in gene expression were due to differences in embryo length. In conclusion, DKK1 can act on the morula-to-blastocyst stage embryo to modify subsequent trophoblast elongation. Higher pregnancy rates associated with transfer of DKK1-treated embryos may be due in part to enhancements of trophoblast growth and antiluteolytic signaling through IFNT secretion. Given that progesterone can regulate both timing of trophoblast elongation and DKK1 expression, DKK1 may be a mediator of progesterone effects on embryonic development.

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Consequences of exposure of embryos produced in vitro in a serum-containing medium to dickkopf-related protein 1 and colony stimulating factor 2 on blastocyst yield, pregnancy rate, and birth weight1

Cited by 28 publications

References 20 publications

Effects of sex on response of the bovine preimplantation embryo to insulin-like growth factor 1, activin A, and WNT7A

Effects of sex on response of the bovine preimplantation embryo to insulin-like growth factor 1, activin A, and WNT7A

BOARD INVITED REVIEW: Post-transfer consequences of in vitro-produced embryos in cattle

Dickkopf-related protein 1 is a progestomedin acting on the bovine embryo during the morula-to-blastocyst transition to program trophoblast elongation

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