Adult Body Weight Is Programmed by a Redox-Regulated and Energy-Dependent Process during the Pronuclear Stage in Mouse

Banrezes, Bernadette; Sainte-Beuve, Thierry; Canon, Eugénie; Schultz, Richard M.; Cancela, José-Manuel; Ozil, Jean-Pierre

doi:10.1371/journal.pone.0029388

Cited by 52 publications

(50 citation statements)

References 44 publications

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“…This highlights the remarkable vulnerability of zygotes to the stresses incurred through the embryo isolation process, which may be related to the timing of zygotic genome activation. Indeed, transfer of mouse zygotes following in vitro exposure to different nutritional milieu during the pronuclear stage alters birth weight in a condition-specific manner (Banrezes, et al 2011). A notable physiological feature that separates the IVC group is that these in vivo -generated embryos are exposed to seminal fluid, which can elicit unique gene expression changes (Schjenken and Robertson 2015).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional signatures throughout development: the effects of mouse embryo manipulation in vitro

Feuer¹,

Liu²,

Donjacour³

et al. 2017

Reproduction

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Stressful environmental exposures incurred early in development can affect postnatal metabolic health and susceptibility to non-communicable diseases in adulthood, although the molecular mechanisms by which this occurs have yet to be elucidated. Here we use a mouse model to investigate how assorted in vitro exposures restricted exclusively to the preimplantation period affect transcription both acutely in embryos and long-term in subsequent offspring adult tissues, to determine if reliable transcriptional markers of in vitro stress are present at specific developmental time points and throughout development. Each in vitro fertilization or embryo culture environment led to a specific and unique blastocyst transcriptional profile, but we identified a common 18-gene and 9-pathway signature of preimplantation embryo manipulation that was present in all in vitro embryos irrespective of culture condition or method of fertilization. This fingerprint did not persist throughout development and there was no clear transcriptional cohesion between adult IVF offspring tissues or compared to their preceding embryos, indicating a tissue-specific impact of in vitro stress on gene expression. However, the transcriptional changes present in each IVF tissue were targeted by the same upstream transcriptional regulators, which provide insight as to how acute transcriptional responses to stressful environmental exposures might be preserved throughout development to influence adult gene expression.

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Section: Discussionmentioning

confidence: 99%

Transcriptional signatures throughout development: the effects of mouse embryo manipulation in vitro

Feuer¹,

Liu²,

Donjacour³

et al. 2017

Reproduction

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“…Poor maternal nutrition in large domestic animals during the PC window also results in increased adult disease risk (Gardner et al, 2004;Sinclair et al, 2007;Torrens et al, 2009). Likewise, in animal ART models, embryo culture and PC treatments cause altered growth rates and increased adult hypertension, metabolic dysfunction and behavioural deficits (Ecker et al, 2004;Fernández-Gonzalez et al, 2004;Watkins et al, 2007;Banrezes et al, 2011). Moreover, in human ART, the selection of commercial embryo culture medium has been shown to change birth weight (Dumoulin et al, 2010) and children born have an increased risk of cardiometabolic disease (Ceelen et al, 2008).…”

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confidence: 99%

Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition

et al. 2014

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Mammalian extra-embryonic lineages perform the crucial role of nutrient provision during gestation to support embryonic and fetal growth. These lineages derive from outer trophectoderm (TE) and internal primitive endoderm (PE) in the blastocyst and subsequently give rise to chorio-allantoic and visceral yolk sac placentae, respectively. We have shown maternal low protein diet exclusively during mouse preimplantation development (Emb-LPD) is sufficient to cause a compensatory increase in fetal and perinatal growth that correlates positively with increased adult-onset cardiovascular, metabolic and behavioural disease. Here, to investigate early mechanisms of compensatory nutrient provision, we assessed the influence of maternal Emb-LPD on endocytosis within extraembryonic lineages using quantitative imaging and expression of markers and proteins involved. Blastocysts collected from Emb-LPD mothers within standard culture medium displayed enhanced TE endocytosis compared with embryos from control mothers with respect to the number and collective volume per cell of vesicles with endocytosed ligand and fluid and lysosomes, plus protein expression of megalin (Lrp2) LDL-family receptor. Endocytosis was also stimulated using similar criteria in the outer PE-like lineage of embryoid bodies formed from embryonic stem cell lines generated from Emb-LPD blastocysts. Using an in vitro model replicating the depleted amino acid (AA) composition found within the Emb-LPD uterine luminal fluid, we show TE endocytosis response is activated through reduced branched-chain AAs (leucine, isoleucine, valine). Moreover, activation appears mediated through RhoA GTPase signalling. Our data indicate early embryos regulate and stabilise endocytosis as a mechanism to compensate for poor maternal nutrient provision.

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“…Some of the associations seen were not in agreement for the two genes, raising some question about their relevance. However, it is noted that the zygotic REDOX state can affect postnatal phenotype (Banrezes et al 2011). Participation of Txndc9 in such regulation could contribute to SCNT development.…”

Section: Discussionmentioning

confidence: 99%

“…Ooplasmic components that repair the cytoskeleton and cellular architecture, repair the plasma membrane, promote proper pmSCC formation, enable correct mitoses, initiate correct cell cycle transit, and suppress apoptosis may be key for cloned embryogenesis, with parallel roles in the normal embryo. Because the oxidative state of the cell can be compromised by in vitro manipulation and this can lead to long-term phenotypic change (Banrezes et al 2011), ooplasmic factors that regulate the oxidative state in clones may also be key. With so many processes potentially contributing to cloned embryogenesis, and the fundamental interest in understanding these processes in normal embryos, there is clear value in pursuing a systematic approach to identify genes that enable successful cloned embryo development.…”

mentioning

confidence: 99%

Systems Genetics Implicates Cytoskeletal Genes in Oocyte Control of Cloned Embryo Quality

Cheng¹,

Gaughan

Midic³

et al. 2013

Genetics

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Cloning by somatic cell nuclear transfer is an important technology, but remains limited due to poor rates of success. Identifying genes supporting clone development would enhance our understanding of basic embryology, improve applications of the technology, support greater understanding of establishing pluripotent stem cells, and provide new insight into clinically important determinants of oocyte quality. For the first time, a systems genetics approach was taken to discover genes contributing to the ability of an oocyte to support early cloned embryo development. This identified a primary locus on mouse chromosome 17 and potential loci on chromosomes 1 and 4. A combination of oocyte transcriptome profiling data, expression correlation analysis, and functional and network analyses yielded a short list of likely candidate genes in two categories. The major category-including two genes with the strongest genetic associations with the traits (Epb4.1l3 and Dlgap1)-encodes proteins associated with the subcortical cytoskeleton and other cytoskeletal elements such as the spindle. The second category encodes chromatin and transcription regulators (Runx1t1, Smchd1, and Chd7). Smchd1 promotes X chromosome inactivation, whereas Chd7 regulates expression of pluripotency genes. Runx1t1 has not been associated with these processes, but acts as a transcriptional repressor. The finding that cytoskeleton-associated proteins may be key determinants of early clone development highlights potential roles for cytoplasmic components of the oocyte in supporting nuclear reprogramming. The transcriptional regulators identified may contribute to the overall process as downstream effectors.T HE oocyte is a remarkable cell. It harbors essential stored mRNAs, proteins, and other macromolecules to sustain and direct normal development until embryonic gene expression commences and until external nutrient supplies become available. The oocyte also has the unique ability to reprogram somatic cell nuclei to a totipotent state, a capacity that reflects its unique role during normal embryogenesis of uniting the two gamete genomes and converting them into an embryonic genome. A variety of approaches since the late 1800s investigated the nuclear reprogramming capacity of oocytes by manipulating the ooplasm-nucleus dialog, using blastomere ligature experiments, embryo splitting, embryonic cell nuclear transfer, and ultimately somatic cell nuclear transfer (SCNT). These methodologies have also been useful in determining the timing and mechanisms underlying other processes such as cell-fate restriction and lineage determination in the early embryo. Cloning studies can thus provide unique insight into the early formative processes that are essential to creating each new individual.Ooplasmic components must mediate a myriad of key events to make cloned embryogenesis possible, and observing the execution of these events in cloned embryos can reveal previously unappreciated aspects of normal development. The first step of the cloning process entai...

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Adult Body Weight Is Programmed by a Redox-Regulated and Energy-Dependent Process during the Pronuclear Stage in Mouse

Cited by 52 publications

References 44 publications

Transcriptional signatures throughout development: the effects of mouse embryo manipulation in vitro

Transcriptional signatures throughout development: the effects of mouse embryo manipulation in vitro

Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition

Systems Genetics Implicates Cytoskeletal Genes in Oocyte Control of Cloned Embryo Quality

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