Expression of imprinted genes is aberrant in deceased newborn cloned calves and relatively normal in surviving adult clones

Yang, Lan; Chavatte‐Palmer, Pascale; Kubota, Chikara; O’Neill, Michael; Hoagland, T.A.; Renard, Jean‐Paul; Taneja, M.; Yang, Xiangzhong; Tian, X. Cindy

doi:10.1002/mrd.20311

Cited by 113 publications

(76 citation statements)

References 55 publications

(74 reference statements)

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“…This strongly suggests a correlation between the normality of gene expression and viability of the cloned piglets. Our finding was in accordance with a recent study in which the expression of several imprinted genes were found to be relatively normal in bovine clones that survived to adulthood compared to those that died at/after birth (Yang et al 2005). Interestingly, all the above-mentioned studies, together with ours, reported more variation of gene expression in the cloned group, suggesting the universal random nature of nuclear reprogramming in different species.…”

Section: Discussionsupporting

confidence: 93%

“…In fact, the expression of all but one gene (ARAF1) in organs of individual deceased clones was found to exceed this threshold and was likely abnormal (Table 2). Similar expression abnormalities were found in DNA methylation in cloned pigs and deceased cloned bovine calves (Archer et al 2003;Li et al, 2004;Yang et al, 2005). The same 2SD comparisons in the surviving clones revealed much less dysregulation (Table 2).…”

Section: Discussionsupporting

confidence: 63%

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Expression of X‐linked genes in deceased neonates and surviving cloned female piglets

Jiang

Lai

Samuel

et al. 2007

Molecular Reproduction Devel

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Animal cloning through somatic cell nuclear transfer is very inefficient, probably due to insufficient reprogramming of the donor nuclei, which in turn would cause the dysregulation of gene expression. X-Chromosome inactivation (XCI) is a multi-step epigenetic process utilized by mammals to achieve dosage compensation in females. Our aim was to determine if any dysregulation of X-linked genes, which would be indicative of unfaithful reprogramming of donor nuclei, was present in cloned pigs. Real time reverse transcription polymerase chain reaction (RT-PCR) was performed to quantify the transcript levels of five X-linked genes, XIST, TSIX, HPRT1, G6PD, ARAF1 and one autosomal gene, COL4A1 in major organs of neonatal deceased and surviving female cloned pigs and age-matched control pigs from conventional breeding. Aberrant expression level of these genes was prevalent in the neonatal deceased clones, while it was only moderate in cloned pigs that survived after birth. These results suggest a correlation between the viability of the clones and the normality of their gene expression and provide a possible explanation for the death of a large portion of cloned animals around birth.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 63%

Expression of X‐linked genes in deceased neonates and surviving cloned female piglets

Jiang

Lai

Samuel

et al. 2007

Molecular Reproduction Devel

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“…At d 18, the beginning of the implantation window, developmental asynchrony between the embryonic disk and the extraembryonic tissue (EET) was shown to be one reason for arrest at implantation (19). In addition, relatively few differentially expressed genes are detected in cloned fetuses (20,21), and comparison of gene expression in term placentomes collected from pregnancies produced by SNCT, in vitro fertilization, and AI (17) showed that, at later stages of development and at term, placentomes of SCNT-derived pregnancies had an altered transcriptome, regardless of whether pathological morphology was observed (15,17). These studies demonstrated that the abnormal development of the placenta is the major cause of failure of clones to complete pregnancy after implantation.…”

Section: Significancementioning

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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“…The defect in imprinted genes expression was also observed in cloned embryos and even cloned fetuses (Mann et al 2003;Yang et al 2005). In fact, oocytes have few responsibilities to reprogram imprinted genes in sperm genome, for the reason that appropriate epigenetic modifications have already been established in most of imprinted genes during spermiogenesis.…”

Section: Main Barricades Of Reprogramming Somatic Cells By Oocytesmentioning

confidence: 99%

“…There was a contradiction in the question of whether imprinted genes could normally express in live cloned animals because both faithful and unfaithful expression of imprinted genes were reported (Inoue et al 2002;Yang et al 2005;Wei et al 2010;Shen et al 2012;Okae et al 2014). We considered that the abnormalities in the expression of imprinted genes, as well as aberrant DNA methylation in their DMR, are common phenomena in most of cloned embryos.…”

Section: Main Barricades Of Reprogramming Somatic Cells By Oocytesmentioning

confidence: 99%

Somatic cell reprogrammed by oocyte: process and barricade

Wang

et al. 2014

Animal Cells and Systems

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Somatic cell nuclear transfer (SCNT) is a technology in which a somatic nucleus is transferred into the cytoplasm of a matured oocyte -reconstructed embryos have the capacity to develop to term. Why somatic cells can be reprogrammed by oocytes -the answer for this question must exist in the cytoplasm of matured oocytes. In this review, totipotent characters of matured oocytes were discussed, which may confer matured oocytes with the capacity to reprogram somatic nucleus. Moreover, the procedure of SCNT also makes a possibility for somatic nucleus to be reprogrammed by oocytes. Compared with fertilized embryos, embryos derived from SCNT exhibit low developmental ability; the barricades in reprogramming process and their possible reasons were also discussed. This review maybe can benefit the mechanism research of SCNT technology and can make contribution for improving the efficiency of this technology.

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Expression of imprinted genes is aberrant in deceased newborn cloned calves and relatively normal in surviving adult clones

Cited by 113 publications

References 55 publications

Expression of X‐linked genes in deceased neonates and surviving cloned female piglets

Expression of X‐linked genes in deceased neonates and surviving cloned female piglets

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

Somatic cell reprogrammed by oocyte: process and barricade

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