Effect of the method of conception and embryo transfer procedure on mid-gestation placenta and fetal development in an IVF mouse model

Piane, Luisa Delle; Lin, Wen; Liu, X.; Donjacour, Annemarie A.; Minasi, Petros; Revelli, Alberto; Maltepe, Emin; Rinaudo, Paolo

doi:10.1093/humrep/deq165

Cited by 104 publications

(94 citation statements)

References 40 publications

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“…However, the long-term effect of this IVF-induced female-specific epigenetic error should be further investigated. During the mid-gestation stage, E13.5 was selected for sampling based on developmental considerations, as the placental architecture and function is well established and spongiotrophoblast and labyrinthine areas can be clearly distinguished at this time (Delle Piane et al 2010). Although the implantation ability of IVF embryos was comparable with that of IVO embryos, we found that the abortion rate of IVF embryos is significantly higher than that of IVO embryos.…”

Section: Discussionmentioning

confidence: 91%

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IVF affects embryonic development in a sex-biased manner in mice

Tan¹,

Wang²,

Zhang³

et al. 2016

Reproduction

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Increasing evidence indicates that IVF (IVF includes in vitro fertilization and culture) embryos and babies are associated with a series of health complications, and some of them show sex-dimorphic patterns. Therefore, we hypothesized that IVF procedures have sex-biased or even sex-specific effects on embryonic and fetal development. Here, we demonstrate that IVF-induced side effects show significant sexual dimorphic patterns from the pre-implantation to the prenatal stage. During the pre-implantation stage, female IVF embryos appear to be more vulnerable to IVF-induced effects, including an increased percentage of apoptosis (7.22G1.94 vs 0.71G0.76, P!0.01), and dysregulated expression of representative sex-dimorphic genes (Xist, Hprt, Pgk1 and Hsp70). During the mid-gestation stage, IVF males had a higher survival rate than IVF females at E13.5 (male:femaleZ1.33:1), accompanied with a female-biased pregnancy loss. In addition, while both IVF males and females had reduced placental vasculogenesis/angiogenesis, the compensatory placental overgrowth was more evident in IVF males. During the late-gestation period, IVF fetuses had a higher sex ratio (male:femaleZ1.48:1) at E19.5, and both male and female IVF placentas showed overgrowth. After birth, IVF males grew faster than their in vivo (IVO) counterparts, while IVF females showed a similar growth pattern with IVO females. The present study provides a new insight into understanding IVF-induced health complications during embryonic and fetal development. By understanding and minimizing these sex-biased effects of the IVF process, the health of IVF-conceived babies may be improved in the future.

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Section: Discussionmentioning

confidence: 91%

“…We used a well-established experimental design (Delle Piane et al 2010, Fauque et al 2010, Tan et al 2015 to test the sex-biased or sex-specific effects of the IVF process from pre-implantation to the prenatal stage (Fig. 1).…”

Section: Experimental Designmentioning

confidence: 99%

IVF affects embryonic development in a sex-biased manner in mice

Tan¹,

Wang²,

Zhang³

et al. 2016

Reproduction

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“…Low birth weight has also been linked to predisposition to cardiovascular diseases, diabetes, and stroke. A previous in vitro study of mouse embryos supported that in vitro embryo culture affects both fetal and placental weight during development [Delle Piane et al 2010]. In vitro culture of sheep or cattle embryos has been associated with abnormal skeletal and organ development [Walker et al 2000].…”

Section: Various Methods Are Needed To Monitor Genome Integrity Durinmentioning

confidence: 99%

Genome constraint through sexual reproduction: application of 4D-Genomics in reproductive biology

Horne¹,

Abdallah²,

Stevens³

et al. 2013

Systems Biology in Reproductive Medicine

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“…Oocytes were obtained from superovulated C57Bl/ 6J female mice as described previously. 14,25 Briefly, female mice were injected with 5 IU of pregnant mare serum gonadotropin and 46 to 48 hours later with 5 IU of human chorionic gonadotropin (hCG). The following morning, oocytes were collected from the ampullae.…”

Section: Preimplantation Embryo Productionmentioning

confidence: 99%

Behavior and Brain Gene Expression Changes in Mice Exposed to Preimplantation and Prenatal Stress

et al. 2015

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Preimplantation culture of mouse embryos has been suggested to result in reduced anxiety-like behavior in adulthood. Here, we investigated the effects of in vitro fertilization (IVF), embryo culture, and different diets on anxiety-like behavior using the elevated plus maze (EPM). We hypothesized that exposure to suboptimal conditions during the preimplantation stage would interact with the suboptimal diet to alter behavior. The expression of genes related to anxiety was then assessed by quantitative real-time polymerase chain reaction in various brain regions. When fed a normal diet during gestation and a moderately high-fat Western diet (WD) postnatally, naturally conceived (NC) and IVF mice showed similar anxiety-like behavior on the EPM. However, when fed a low-protein diet prenatally and a high-fat diet postnatally (LP/HF), NC mice showed a modest increase in anxiety-like behavior, whereas IVF mice showed the opposite: a strongly reduced anxiety-like behavior on the EPM. The robust reduction in anxiety-like behavior in IVF males fed the LP/HF diets was, intriguingly, associated with reduced expression of MAO-A, CRFR2, and GABA markers in the hypothalamus and cortex. These findings are discussed in relation to the developmental origin of health and disease hypothesis and the 2-hit model, which suggests that 2 events, occurring at different times in development, can act synergistically with long-term consequences observed during adulthood.

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Effect of the method of conception and embryo transfer procedure on mid-gestation placenta and fetal development in an IVF mouse model

Abstract: In vitro embryo culture affects fetal and placental development; this could explain the lower birthweight in IVF offspring.

Cited by 104 publications

References 40 publications

IVF affects embryonic development in a sex-biased manner in mice

IVF affects embryonic development in a sex-biased manner in mice

Genome constraint through sexual reproduction: application of 4D-Genomics in reproductive biology

Behavior and Brain Gene Expression Changes in Mice Exposed to Preimplantation and Prenatal Stress

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