Endometrium as an early sensor of in vitro embryo manipulation technologies

Mansouri-Attia, N.; Sandra, Olivier; Aubert, Julie; Degrelle, Séverine A.; Everts, Robin E.; Giraud-Delville, Corinne; Heyman, Yvan; Galio, Laurent; Hue, Isabelle; Yang, Xusan; Tian, X. Cindy; Lewin, Harris A.; Renard, Jean‐Paul

doi:10.1073/pnas.0812722106

Cited by 208 publications

(209 citation statements)

References 39 publications

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“…Our group has investigated the effects of SCNT cloning on gene expression and on developmental anomalies at different phases of cattle development and in different tissues, ranging from day (d) 7 blastocysts to placentomes that were collected at the term of pregnancy (14,(17)(18)(19). The resemblance of gene expression profiles between SCNT-derived blastocysts and those derived by artificial insemination (AI) (18) was the first evidence that the effects of cloning by SCNT could be more severe after blastocyst hatching.…”

Section: Significancementioning

confidence: 99%

“…Embryonic and fetal losses substantially reduce the efficiency of SCNT and thus present a significant limitation to the widespread application of the technology for animal improvement. However, the disrupted embryonic and fetal development of cattle clones produced by SCNT has been used as a model to elucidate the mechanisms of embryo loss, the maternal recognition of pregnancy (13,14), and placental development (15)(16)(17). Understanding the mechanism of embryonic and fetal losses in SCNT clones is thus not only practically important but also serves as a window to understanding infertility in cattle and other mammals.…”

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confidence: 99%

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Massive dysregulation of genes involved in cell signaling and placental development in cloned cattle conceptus and maternal endometrium

Biase

Rabel

Guillomot

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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A major unresolved issue in the cloning of mammals by somatic cell nuclear transfer (SCNT) is the mechanism by which the process fails after embryos are transferred to the uterus of recipients before or during the implantation window. We investigated this problem by using RNA sequencing (RNA-seq) to compare the transcriptomes in cattle conceptuses produced by SCNT and artificial insemination (AI) at day (d) 18 (preimplantation) and d 34 (postimplantation) of gestation. In addition, endometrium was profiled to identify the communication pathways that might be affected by the presence of a cloned conceptus, ultimately leading to mortality before or during the implantation window. At d 18, the effects on the transcriptome associated with SCNT were massive, involving more than 5,000 differentially expressed genes (DEGs). Among them are 121 genes that have embryonic lethal phenotypes in mice, cause defects in trophoblast and placental development, and/or affect conceptus survival in mice. In endometria at d 18, <0.4% of expressed genes were affected by the presence of a cloned conceptus, whereas at d 34, ∼36% and <0.7% of genes were differentially expressed in intercaruncular and caruncular tissues, respectively. Functional analysis of DEGs in placental and endometrial tissues suggests a major disruption of signaling between the cloned conceptus and the endometrium, particularly the intercaruncular tissue. Our results support a "bottleneck" model for cloned conceptus survival during the periimplantation period determined by gene expression levels in extraembryonic tissues and the endometrial response to altered signaling from clones. somatic cell nuclear transfer | conceptus | placentation | conceptus-maternal communication I n cattle, as in other mammals, exquisitely orchestrated physiological changes of the conceptus and uterus are necessary for a successful pregnancy. Synchronization of the complex events at the time of implantation relies on the timed release of molecular signals from the conceptus and the endometrium. Embryo-derived IFN-τ (IFNT) is the major signal of pregnancy in cattle, preventing luteolysis and regulating the expression of genes that are responsible for promoting local changes in the endometrium to accommodate the conceptus (1-3). In females, progesterone is the major driver of endometrial changes that prepare the uterus for conceptus implantation (4, 5). In addition to IFNT and progesterone, signaling between the bovine conceptus and the endometrium is bidirectional, and involves several pathways that work concomitantly (6) for the successful establishment of pregnancy.Independent studies have shown that the majority of embryonic losses in cattle occur during the period that spans embryo cleavage until the attachment of the blastocyst to the endometrium (7). The reasons for these losses remain unclear and likely result from several factors, including embryonic lethal genes (8, 9), environmental stressors (7), and endometrial condition (10). Cloning of cattle by somatic cell nuclear transfer ...

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Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

Massive dysregulation of genes involved in cell signaling and placental development in cloned cattle conceptus and maternal endometrium

Biase

Rabel

Guillomot

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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“…Indeed, evidence that the endometrium can act a sensor of the quality of the embryo was recently provided by two elegant studies examining the endometrial transcriptomic response elicited by conceptuses of differeing developmental fates (Bauersachs et al, 2009;Mansouri-Attia et al, 2009; reviewed by Sandra et al (2011)). Some, but not all, of the differentially expressed genes were involved in the classical IFNT response of the endometrium MX2, BST2, IFIT1 (Bauersachs et al, 2009); radical S-adenosyl RSAD2, OAS1 (Mansouri-Attia et al, 2009).…”

Section: Maternal-embryonic Interaction In Early Pregnancymentioning

confidence: 99%

Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle

Lonergan¹,

Forde²

2014

Animal

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Early embryo development following fertilization occurs in the oviduct. However, despite being the site of fertilization in cattle, it is possible to by-pass the oviduct by producing embryos in vitro and/or by transferring blastocysts recovered from one female into the uterus of another. While there is substantial evidence for the oviduct having an influence on the quality of the developing embryo, manifested in altered morphology, gene expression and cryotolerance, evidence for a two-way dialogue is weak. In contrast, successful growth and development of the post-hatching blastocyst and pregnancy establishment are a result of the two-way interaction between a competent embryo and a receptive uterine environment. Progesterone (P4) plays a key role in reproductive events associated with establishment and maintenance of pregnancy through its action on the uterine endometrium. Elevated concentrations of circulating P4 in the immediate post-conception period have been associated with an advancement of conceptus elongation, an increase in interferon-tau production and, in some studies, higher pregnancy rates in cattle. This review summarizes current knowledge on the communication between the developing embryo and the maternal reproductive tract.

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“…Moreover, these changes in endometrial gene expression can be affected by the quality of the conceptus present (Bauersachs et al 2009;Mansouri-Attia et al 2009). In addition, systemic factors such as elevated concentrations of serum progesterone (Forde et al 2009a), disease (Gabler et al 2009;Herath et al 2009) as well as dietary status (Coyne et al 2008;Wathes et al 2009) all alter gene expression in the uterine endometrium.…”

Section: Introductionmentioning

confidence: 99%

Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination

Beltman

Forde

Furney

et al. 2010

Reprod. Fertil. Dev.

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Abridged title: Endometrial gene expression and metabolic parameters in subfertile beef heifers. AbstractThe objective of this study was to compare the hormonal, metabolic characteristics and endometrial gene expression profiles in beef heifers yielding either a viable or a degenerate embryo on Day 7 after insemination as a means to explain differences in embryo survival.Oestrus was synchronised in cross bred beef heifers (n=145) using a CIDR-prostaglandin protocol and heifers (n=102) detected in standing oestrus (within 24-48 h post CIDR removal) were inseminated 12-18 h after detection of oestrus (Day 0) with frozen-thawed semen from a single ejaculate of a bull with proven fertility. Blood samples were collected from Day 4 to Day 7 post oestrus to measure progesterone (on Days 4, 5 and 7), insulin and IGF-I (on Days 4 and 6) and urea concentrations (on Day 7). All animals were slaughtered on Day 7. Uterine pH was also determined. Animals from which an embryo was recovered were classified as either having a viable embryo (morula/blastocyst stage); n=32, or a retarded embryo (arrested at 2-to 16-cell stage); n=19. The overall recovery rate was 64%. There was no significant difference in blood parameters measured or uterine pH at slaughter between the heifers with either a viable or retarded embryo. The relative abundance of 9 transcripts out of 53 tested from the endometrial tissue was different between heifers with a viable embryo or retarded embryo: MOGAT1, PFKB2, LYZ2, SVS8, UHRF1, PTGES, AGPAT4, DGKA and HGPD. Both LYZ2 and UHRF1 are associated with regulation of the immune system. PFKFB2 is a mediator in glycolysis and MOGAT, AGPAT4 and DGKA belong to the triglyceride synthesis pathway. PTGES and HGPD belong to the prostaglandin pathway.Both of these metabolic pathways are important for early embryonic development. In conclusion, retarded embryo development in this study was not related to serum progesterone, IGF-I, insulin or urea concentrations nor to uterine pH at slaughter. However, altered expression of genes involved in the prostaglandin and triglyceride pathways, as well as 2 genes that are closely associated with the regulation of immunity in the endometrium may indicate a uterine component to the retardation of the embryos in these beef heifers.

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Endometrium as an early sensor of in vitro embryo manipulation technologies

Cited by 208 publications

References 39 publications

Massive dysregulation of genes involved in cell signaling and placental development in cloned cattle conceptus and maternal endometrium

Massive dysregulation of genes involved in cell signaling and placental development in cloned cattle conceptus and maternal endometrium

Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle

Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination

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