Sexually Dimorphic Effect of In Vitro Fertilization (IVF) on Adult Mouse Fat and Liver Metabolomes

Feuer, Sky K.; Donjacour, Annemarie A.; Simbulan, Rhodel; Lin, Wen; Liu, Xiaowei; Maltepe, Emin; Rinaudo, Paolo

doi:10.1210/en.2014-1465

Cited by 42 publications

(52 citation statements)

References 47 publications

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“…The increased ratio of placental/fetal weight observed in this study is similar to that described in human IVF pregnancies, where IVF offspring were associated with hypertension later in life (Barker et al 1990, Moore et al 1996, Koudstaal et al 2000. The reasons for the increased ratio of placental/fetal weight are likely complicated; one possible explanation involves a compensatory process for the depressed fetal growth or the impaired function of the placenta itself (Feuer et al 2014, Chen et al 2015. The placental/fetal weight ratio was higher for IVF males than IVF females.…”

Section: Discussionsupporting

confidence: 82%

“…For example, IVF is associated with higher risks of female-biased Rett syndrome (Arnaud & Feil 2005) and male-biased Autism (Fountain et al 2015), and some IVF-associated birth defects show sexually dimorphic patterns (Michalski et al 2015). Furthermore, sex-specific effects of IVF on postnatal metabolism and growth of IVF-conceived offspring has been confirmed in mouse models (Scott et al 2010, Feuer et al 2014). More importantly, recent studies indicate that IVF results in a skewed sex ratio at birth (Dean et al 2010, Bu et al 2014, Maalouf et al 2014, reflecting sex-biased or even specific disruption of embryonic development.…”

Section: Introductionmentioning

confidence: 88%

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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: Discussionsupporting

confidence: 82%

Section: Introductionmentioning

confidence: 88%

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

Tan¹,

Wang²,

Zhang³

et al. 2016

Reproduction

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“…In mice, long-term effects associated with in vitro fertilization (IVF), intracytoplasmic sperm injection (ICSI) and somatic cell nuclear transfer (SCNT) were found to be sex specific, with females showing altered glucose clearance, higher body weight and adiposity (Scott et al 2010a). In agreement, another study reported sex-specific differences in sterol metabolism, redox state, mobilization and oxidation of fatty acids after IVF in murine offspring, with females being more predisposed to increased fat accumulation (Feuer et al 2014).…”

Section: Sex-specific Long-term Effects Mediated By Assisted Reproducsupporting

confidence: 73%

“…However, in another study in mice produced from IVF, altered postnatal growth and glucose intolerance were only observed in males (Donjacour et al 2014). Additional sexual dimorphic patterns induced by IVF were reported by Tan and coworkers (Tan et al 2016).…”

Section: Sex-specific Long-term Effects Mediated By Assisted Reproducmentioning

confidence: 60%

Early sex-dependent differences in response to environmental stress

et al. 2018

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Developmental plasticity enables the appearance of long-term effects in offspring caused by exposure to environmental stressors during embryonic and foetal life. These long-term effects can be traced to pre-and post-implantation development, and in both cases, the effects are usually sex specific. During preimplantation development, male and female embryos exhibit an extensive transcriptional dimorphism mainly driven by incomplete X chromosome inactivation. These early developmental stages are crucial for the establishment of epigenetic marks that will be conserved throughout development, making it a particularly susceptible period for the appearance of long-term epigenetic-based phenotypes. Later in development, gonadal formation generates hormonal differences between the sexes, and male and female placentae exhibit different responses to environmental stressors. The maternal environment, including hormones and environmental insults during pregnancy, contributes to sex-specific placental development that controls genetic and epigenetic programming during foetal development, regulating sex-specific differences, including sex-specific epigenetic responses to environmental hazards, leading to long-term effects. This review summarizes several human and animal studies examining sex-specific responses to environmental stressors during both the periconception period (caused by differences in sex chromosome dosage) and placental development (caused by both sex chromosomes and hormones). The identification of relevant sex-dependent trajectories caused by sex chromosomes and/or sex hormones is essential to define diagnostic markers and prevention/intervention protocols.Reproduction (2018) 155 R39-R51

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“…They expressed pluripotent markers and had a capacity to generate derivatives representative of all three germ layers in vivo and in vitro. Recently, many groups reported that IVF altered gene methylation mode and metabolic physiology (Feuer et al 2014;Hiura et al 2014;Nelissen et al 2014). This alteration may be arose early in embryogenesis.…”

Section: Resultsmentioning

confidence: 99%

Derivation of embryonic stem cells from Kunming mice IVF blastocyst in feeder- and serum-free condition

Liu

Wei

Zhang

et al. 2015

In Vitro Cell.Dev.Biol.-Animal

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Kunming mice are widely used in China; however, it is difficult to isolate embryonic stem cells (ESCs) in conventional derivation condition containing feeder cells and serum. 6-Bromoindirubin-3'-oxime (BIO), a glycogen synthase kinase 3 (GSK3) inhibitor, could facilitate the maintenance of pluripotency of ESCs. Therefore, BIO could be considered as a candidate to replace feeder cells and serum. On the other hand, in vitro fertilization (IVF) is an important technology in assisted reproduction. It is reported that there was some difference in gene expression between IVF and in vivo developed blastocyst. ESCs derived from IVF blastocyst could provide a valuable tool to research the effect of IVF on differentiation and development. In the present study, we established two novel ESC lines from IVF blastocyst of Kunming mice in a feeder- and serum-free condition containing 2.5 μM BIO. In this condition, expanded IVF blastocyst could spontaneously hatch from zonae pellucidae and attached to the gelatin-coated bottom of dishes. ESC-like outgrowth could be observed without overfull trophoblast cells. After further propagation, two Kunming mice ESC lines, designated as KMES1 and KMES2, were obtained. These two novel ESCs shared common morphological characteristics with other rodent ESCs, showed strong alkaline phosphatase activity, and expressed pluripotent markers, including Oct-4, Nanog, and SSEA-1. Embryoid body (EB) and teratoma test indicated that these ESCs could spontaneously differentiate into cells representative of all three embryonic germ layers.

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Sexually Dimorphic Effect of In Vitro Fertilization (IVF) on Adult Mouse Fat and Liver Metabolomes

Cited by 42 publications

References 47 publications

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

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

Early sex-dependent differences in response to environmental stress

Derivation of embryonic stem cells from Kunming mice IVF blastocyst in feeder- and serum-free condition

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