Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes

Lepikhov, Konstantin; Zakhartchenko, Valeri; Hao, Ru; Yang, Fan; Wrenzycki, C.; Niemann, Heiner; Wolf, Eckhard; Walter, Joern

doi:10.1186/1756-8935-1-8

Cited by 73 publications

(51 citation statements)

References 42 publications

(50 reference statements)

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“…This indicates that remodelling during early stages of development is of critical importance for resetting the epigenome in preparation for establishment of new programs of differentiation during lineage commitment. Importantly, the kinetics described above for rodents have also been observed in embryos of different domestic animals, including cattle, suggesting that these mechanisms are conserved across mammals (Lepikhov et al 2008;Maalouf et al 2008).…”

Section: Recent Advances In Epigeneticsmentioning

confidence: 78%

Epigenetics and developmental programming of welfare and production traits in farm animals

Sinclair

Rutherford

Wallace

et al. 2016

Reprod. Fertil. Dev.

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Abstract. The concept that postnatal health and development can be influenced by events that occur in utero originated from epidemiological studies in humans supported by numerous mechanistic (including epigenetic) studies in a variety of model species. Referred to as the 'developmental origins of health and disease' or 'DOHaD' hypothesis, the primary focus of large-animal studies until quite recently had been biomedical. Attention has since turned towards traits of commercial importance in farm animals. Herein we review the evidence that prenatal risk factors, including suboptimal parental nutrition, gestational stress, exposure to environmental chemicals and advanced breeding technologies, can determine traits such as postnatal growth, feed efficiency, milk yield, carcass composition, animal welfare and reproductive potential. We consider the role of epigenetic and cytoplasmic mechanisms of inheritance, and discuss implications for livestock production and future research endeavours. We conclude that although the concept is proven for several traits, issues relating to effect size, and hence commercial importance, remain. Studies have also invariably been conducted under controlled experimental conditions, frequently assessing single risk factors, thereby limiting their translational value for livestock production. We propose concerted international research efforts that consider multiple, concurrent stressors to better represent effects of contemporary animal production systems.

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Section: Recent Advances In Epigeneticsmentioning

confidence: 78%

Epigenetics and developmental programming of welfare and production traits in farm animals

Sinclair

Rutherford

Wallace

et al. 2016

Reprod. Fertil. Dev.

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“…It was reported that Histone H3K4 methylation levels correlated with the genome activation (Lepikhov and Walter, 2004;Lepikhov et al, 2008;VerMilyea et al, 2009), while H3K9me3 methylation (Lachner and Jenuwein, 2002;Horn and Peterson, 2006;Grewal and Jia, 2007) correlated with genome inactivation. So we further determined the H3K4me1/2/3 levels and H3K9me2/3 levels.…”

Section: Mutant Zar1l Induced Cell Cycle Arrest In Preimplantation Emmentioning

confidence: 99%

Mouse ZAR1‐like (XM_359149) colocalizes with mRNA processing components and its dominant‐negative mutant caused two‐cell‐stage embryonic arrest

Wang

Zhu

et al. 2010

Developmental Dynamics

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*Maternal effect genes and encoding proteins are necessary for nuclear reprogramming and zygotic genome activation. However, the mechanisms that mediate these functions are largely unknown. Here we identified XM_359149, a Zar1-like gene that is predominantly expressed in oocytes and zygotes, which we designated Zar1-like (Zar1l). ZAR1L-EGFP formed multiple cytoplasmic foci in late two-cell-stage embryos. Expression of the ZAR1L C-terminus induced two-cell-stage embryonic arrest, accompanied with abnormal methylation of histone H3K4me2/3 and H3K9me2/3, and marked down-regulation of a group of chromatin modification factors including Dppa2, Dppa4, and Piwil2. When ectopically expressed in somatic cells, ZAR1L colocalized with P-body components including EIF2C1(AGO1), EIF2C2(AGO2), DDX6 and LSM14A, and germline-specific chromatoid body components including PIWIL1, PIWIL2, and LIN28. ZAR1L colocalized with ZAR1 and interacted with human LIN28. Our data suggest that ZAR1L and ZAR1 may comprise a novel family of processing-body/chromatoid-body components that potentially function as RNA regulators in early embryos.

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“…Most of the knowledge on Dnmt1 functions is based on studies in mice. However studies in other mammals, including cow (Beaujean et al, 2004;Dean et al, 2003;Dean et al, 2001;Lepikhov et al, 2008;Maalouf et al, 2008), revealed that methylation reprogram-…”

Section: Discussionmentioning

confidence: 99%

“…Original Paper ming events occurring in mouse early development do not necessarily reflect those of the other species as the extent and timing of the epigenetic events throughout preimplantation development can be different between mammals (Beaujean et al, 2004;Dean et al, 2003;Dean et al, 2001;Lepikhov et al, 2008;Oswald et al, 2000;Santos et al, 2002). Moreover, in the cow the oocyte specific isoform of Dnmt1 (Dnmt1o) was not found to be expressed in oocytes and embryos (Golding and Westhusin, 2003;Russell and Betts, 2008).…”

mentioning

confidence: 99%

Localization of DNA methyltransferase-1 during oocyte differentiation, in vitro maturation and early embryonic development in cow

Lodde¹,

Modina²,

Franciosi³

et al. 2009

Eur J Histochem

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DNA methyltransferase-1 (Dnmt1) is involved in the maintenance of DNA methylation patterns and is crucial for normal mammalian development. The aim of the present study was to assess the localization of Dnmt1 in cow, during the latest phases of oocyte differentiation and during the early stages of segmentation. Dnmt1 expression and localization were assessed in oocytes according to the chromatin configuration, which in turn provides an important epigenetic mechanism for the control of global gene expression and represents a morphological marker of oocyte differentiation. We found that the initial chromatin condensation was accompanied by a slight increase in the level of global DNA methylation, as assessed by 5-methyl-cytosine immunostaining followed by laser scanning confocal microscopy analysis (LSCM). RT-PCR confirmed the presence of Dnmt1 transcripts throughout this phase of oocyte differentiation. Analogously, Dnmt1 immunodetection and LSCM indicated that the protein was always present and localized in the cytoplasm, regardless the chromatin configuration and the level of global DNA methylation. Moreover, our data indicate that while Dnmt1 is retained in the cytoplasm in metaphase II stage oocytes and zygotes, it enters the nuclei of 8-16 cell stage embryos. As suggested in mouse, the functional meaning of the presence of Dnmt1 in the bovine embryo nuclei could be the maintainement of the methylation pattern of imprinted genes. In conclusion, the present work provides useful elements for the study of Dnmt1 function during the late stage of oocyte differentiation, maturation and early embryonic development in mammals.

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Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes

Cited by 73 publications

References 42 publications

Epigenetics and developmental programming of welfare and production traits in farm animals

Epigenetics and developmental programming of welfare and production traits in farm animals

Mouse ZAR1‐like (XM_359149) colocalizes with mRNA processing components and its dominant‐negative mutant caused two‐cell‐stage embryonic arrest

Localization of DNA methyltransferase-1 during oocyte differentiation, in vitro maturation and early embryonic development in cow

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