Maternal organism and embryo biosensoring: insights from ruminants

Sandra, Olivier; Constant, Fabienne; Carvalho, Anais Vitorino; Eozénou, Caroline; Valour, Damien; Mauffré, Vincent; Hue, Isabelle; Charpigny, Gilles

doi:10.1016/j.jri.2014.12.005

Cited by 27 publications

(24 citation statements)

References 94 publications

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“…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)(2)(3). In females, progesterone is the major driver of endometrial changes that prepare the uterus for conceptus implantation (4,5).…”

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.

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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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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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“…The uterine endometrium plays a central role in early conceptus‐maternal communication for establishment and maintenance of pregnancy which involves dynamic changes in the uterine cell types tightly regulated by changes in steroid hormones, cytokines and growth factors and their receptors. Hence, the endometrium has to be considered a critical epigenetic contributor to the embryo trajectory from the very earliest stages of pregnancy (Sandra et al., ).…”

Section: Discussionmentioning

confidence: 99%

Endometrial gene expression in primiparous dairy cows at the end of the voluntary waiting period is affected by nutrition: Total mixed ration vs increasing levels of herbage allowance

Astessiano

Carriquiry

Mattiauda

et al. 2017

Reprod Domestic Animals

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The study postulated that differential nutritional management during the early lactation period would be reflected in endometrial expression of genes related to embryo growth at the end of the voluntary waiting period. Thus, the effect of the combined use of total mixed ration (TMR) and grazing under different herbage allowances during the first 75 days post-partum (DPP) on endometrial gene expression was evaluated in primiparous dairy cows. Cows were blocked by body weight, age and body condition score and randomly assigned to three grazing treatments: high (HA, 30 kg DM per cow per day), medium (MA, 15 kg DM per cow per day) and low (LA, 7.5 kg DM per cow per day) herbage allowance (mixed pasture, 2,600 kg DM per ha) plus 8 kg DM of supplement or TMR (55% forage, 45% concentrate) fed ad libitum (TMR) from calving to 75 DPP. At 57 DPP, cows were synchronized for oestrus (day 0, 68 DPP) and at day 7, endometrial biopsies were obtained. The nutritional treatment did not affect insulin, IGF-1 and leptin concentrations on days 0, 4 or 7. Expression of IGF1, IGFBP3, IGFBP4, ADIPOR1 and ADIPOR2 mRNA was significantly affected by the nutritional treatment. Endometrial IGF1 and IGFBP4 mRNA were twofold greater in TMR and HA than MA and LA cows. Expression of IGFBP3 and ADIPOR1 mRNAs was greater in TMR and HA than MA cows, but did not differ from LA cows. All groups had greater expression of ADIPOR2 mRNA than MA cows. This study provided solid evidence of the importance of nutritional management during early lactation on uterine environment at the end of the voluntary waiting period. The greater expression of genes related to embryo growth and uterine function (IGF system, progesterone and adiponectin receptors) in cows fed diets maximizing energy intake suggests a favourable environment for embryonic growth, which may explain the improved reproductive performance of cows in good energy balance.

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“…It is now widely accepted that ART derived embryos have significantly altered gene expression patterns compared to their in vivo derived counterparts (Clemente et al, 2011;Gad et al, 2012) What is most striking, is that these embryos elicit diverging responses from their recipient maternal endometrium, even though IFNT production levels was found to be similar in these pregnancies (reviewed by Sandra et al, 2015), suggesting that other pathways than IFNT-mediated, are involved in recognition of pregnancy. Comparing endometrial transcriptomes of cows that were recipients of in vivo, IVF-derived or SCNT -embryos revealed distinct patterns of gene expression among the three groups (Bauersachs et al, 2009;Mansouri-Attia et al, 2009b).…”

Section: Molecular Response Of Maternal Endometrium To the Embryomentioning

confidence: 99%

“…In addition to the local uterine immune response, extra-uterine tissues, including peripheral blood cells (PBL) and the corpus luteum, respond to conceptus secretions (Sandra et al, 2015). The systemic effect of the conceptus has also been investigated with regard to IFNT and the expression of ISG in peripheral blood leucocytes (PBL; Oliveira and Hansen, 2008) and (Ott and Gifford, 2010).…”

Section: Peripheral Response Of the Maternal Immune System To Early Pmentioning

confidence: 99%

Embryo maternal immune interactions in cattle

Fair¹

2016

Anim Reprod

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Mammalian embryo implantation requires the priming of the maternal immune system, but, not the provocation. There are many examples of conditions where a disturbed or aberrant immune profile during embryo implantation leads to pregnancy loss. However, these studies are primarily associated with human and mouse species; data is generally limited for cattle and livestock. Most available information centres on the endometrial response to interferon tau (IFNT), a type I antiviral cytokine, which is the maternal recognition factor for cattle and sheep. Interferon tau secretion by the embryo and detection by the dam is critical to corpus luteum (CL) maintenance and pregnancy retention. However, the large volume of bovine endometrial and conceptual transcriptomic data highlights a broader more integral role of the maternal immune system in the establishment of pregnancy in cattle. When taken together with available immunohistochemistry and flow cytometry data from livestock, mouse, and human, a profile of immune cell involvement from ovulation to conception and placentation emerges. The key events of pregnancy establishment in cattle and the involvement of the maternal immune system will be discussed.

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Maternal organism and embryo biosensoring: insights from ruminants

Cited by 27 publications

References 94 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

Endometrial gene expression in primiparous dairy cows at the end of the voluntary waiting period is affected by nutrition: Total mixed ration vs increasing levels of herbage allowance

Embryo maternal immune interactions in cattle

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