Conceptus elongation in cattle: Genes, models and questions

Hue, Isabelle; Degrelle, Séverine A.; Turenne, Nicolas

doi:10.1016/j.anireprosci.2012.08.007

Cited by 53 publications

(36 citation statements)

References 88 publications

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“…A considerable reduction in elongation size was observed in SCNT embryos (93.3 mm) compared with AI embryos (196.3 mm), and this was related to alterations in the expression of genes involved in glycolysis, arginine, proline, pyruvate, and glutathione metabolism (4 pathways among the 11 top canonical pathways affected in SCNT embryos), as seen earlier in D14 and D16 AI embryos (54). Moreover, lipid metabolism is a top function frequently identified by Ingenuity Pathway Analysis (IPA) and cited as differentially expressed between SNCT, in vitro (IVP), and in vivo (IA) produced elongated embryos (33). Lipids and fatty acids are precursors for prostaglandin and steroid hormone biosynthesis.…”

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confidence: 88%

“…Although molecularly true, dissecting the discs to define the developmental stages of elongating conceptuses provides an advantage: knowing whether the conceptus is fully developed (elongation and gastrulation) or not. So far, molecular studies on bovine elongating conceptuses have identified gene clusters involved in cell growth and differentiation, connective tissue development, lipid metabolism, signaling pathways involving growth factors or cytokines and their receptors, as well as transcription factors (33,48,68,69).…”

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Energy and lipid metabolism gene expression of D18 embryos in dairy cows is related to dam physiological status

Valour

Degrelle

Ponter

et al. 2014

Physiological Genomics

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We analyzed the change in gene expression related to dam physiological status in day (D)18 embryos from growing heifers (GH), early lactating cows (ELC), and late lactating cows (LLC). Dam energy metabolism was characterized by measurement of circulating concentrations of insulin, glucose, IGF-1, nonesterified fatty acids, ␤-hydroxybutyrate, and urea before embryo flush. The metabolic parameters were related to differential gene expression in the extraembryonic tissues by correlation analysis. Embryo development estimated by measuring the length of the conceptuses and the proportion of expected D18 gastrulating stages was not different between the three groups of females. However, embryo metabolism was greatly affected by dam physiological status when we compared GH with ELC and GH with LLC but to a lesser extent when ELC was compared with LLC. Genes involved in glucose, pyruvate, and acetate utilization were upregulated in GH vs. ELC conceptuses (e.g., SLC2A1, PC, ACSS2, ACSS3). This was also true for the pentose pathway (PGD, TKT), which is involved in synthesis of ribose precursors of RNA and DNA. The pathways involved in lipid synthesis were also upregulated in GH vs. ELC. Despite similar morphological development, the molecular characteristics of the heifers' embryos were consistently different from those of the cows. Most of these differences were strongly related to metabolic/hormone patterns before insemination and during conceptus free-life. Many biosynthetic pathways appeared to be more active in heifer embryos than in cow embryos, and consequently they seemed to be healthier, and this may be more conducive to continue development. dairy cow; fertility; energy balance; energy metabolism; conceptus development; gene expression; correlations IN THE MODERN HOLSTEIN cow, calving rates are close to 55-60% in heifers and 35-40% in lactating cows (39,73). Most pregnancy losses occur prior to the period of maternal recognition and maintenance of the corpus luteum, i.e., before days 15-17 (D15-D17) after artificial insemination (AI), and are due to nonfertilization-early embryonic loss (NF-EEL, Refs. 22,35,73). NF-EEL can be estimated in field trials by measuring plasma or milk progesterone concentrations the day of AI and 21-24 days later. The frequency of NF-EEL has been reported to be between 25 and 45% in lactating Holstein cows (26,32,35,52), and it has increased from the 1980s (22).Age/parity, uterine health (nulliparous heifers vs. postpartum cows), and metabolic and endocrine environment are factors that can explain differences in reproductive efficiency. Maternal metabolism is known to influence fertility. Milk production, body condition score (BCS), postpartum BCS variations, negative energy balance (NEB), and quantity and quality of dietary protein supply are related to pregnancy rate (reviews Refs. 15,40,45,65,73,76). This effect might be explained partly by the clearance of progesterone in highproducing dairy cows (22) and by poor oocyte quality (43), which impair fertilization ability and early e...

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confidence: 88%

mentioning

confidence: 99%

Energy and lipid metabolism gene expression of D18 embryos in dairy cows is related to dam physiological status

Valour

Degrelle

Ponter

et al. 2014

Physiological Genomics

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“…Progesterone acts on the uterus to indirectly stimulate preimplantation blastocyst growth and elongation by stimulating the production of embryotrophic factors from the endometrium (Garrett et al 1988b ;Mann and Lamming 2001 ;Mann et al 2006 ;Satterfi eld et al 2006 ). Conceptus elongation involves exponential increases in length and weight of the trophectoderm (Wales and Cuneo 1989 ) and onset of extraembryonic membrane differentiation, including gastrulation of the embryo and formation of the yolk sac and allantois that are vital for embryonic survival and formation of a functional placenta (Guillomot 1995 ;Hue et al 2012 ). The increase in conceptus length is not due to the geometrical change of trophoblast cell shape, but is likely primarily driven by cell proliferation associated with peculiar plans of cell division or intercalation (Wang et al 2009 ).…”

Section: Overview Of Peri-implantation Conceptus-endometrial Interactmentioning

confidence: 99%

Implantation and Establishment of Pregnancy in Ruminants

Spencer

Hansen

2015

Advances in Anatomy, Embryology and Cell Biology

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The establishment of pregnancy in ruminants occurs during the peri-implantation period and involves the suppression of the endometrial luteolytic mechanism to maintain progesterone production by the corpus luteum (CL). Reciprocal interactions between the elongating conceptus (embryo/fetus and associated extraembryonic membranes) and endometrium culminate in implantation. Antiluteolytic effects of the conceptus are due to the production of interferon tau (IFNT) by the trophoblast that has a paracrine effect to inhibit the upregulation of oxytocin receptors in the endometrial epithelia, thereby disrupting uterine release of luteolytic prostaglandin F2 alpha (PGF) pulses. Additionally, IFNT is released into the uterine vein and has endocrine actions to induce ISGs in peripheral tissues. For example, IFNT may induce luteal resistance to PGF, thereby ensuring survival of the CL and maintenance of pregnancy. Survival of the blastocyst and elongation of the conceptus requires embryotrophic factors from the epithelia of the uterus, and those embryotrophic factors are regulated by ovarian progesterone as well as conceptus-derived factors including IFNT and prostaglandins. This review provides new concepts on mechanisms of the establishment of pregnancy and implantation in ruminants with emphasis on conceptus-maternal signaling associated with elongation of the blastocyst and endometrial responses to the presence of a conceptus.

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“…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 (SCNT) induces perturbations in conceptus development and greatly increases the probability of developmental arrest before and after implantation (11,12). 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.…”

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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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Conceptus elongation in cattle: Genes, models and questions

Cited by 53 publications

References 88 publications

Energy and lipid metabolism gene expression of D18 embryos in dairy cows is related to dam physiological status

Energy and lipid metabolism gene expression of D18 embryos in dairy cows is related to dam physiological status

Implantation and Establishment of Pregnancy in Ruminants

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

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