Reprogramming the genome to totipotency in mouse embryos

Zhou, Li-Quan; Dean, Jurrien

doi:10.1016/j.tcb.2014.09.006

Cited by 93 publications

(76 citation statements)

References 102 publications

(107 reference statements)

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“…It is known that, if conveniently directed, reprogramming can change cell identity (56). Further, epigenetic reprogramming is essential during vertebrate gonadogenesis and early development (57). Although targeting the stem cell microenvironment is believed to be important for proper tissue reprogramming (reviewed in ref.…”

Section: Discussionmentioning

confidence: 99%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

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

119

136

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Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

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Section: Discussionmentioning

confidence: 99%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

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

119

136

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“…During the MZT, the previously silenced zygotic genome starts transcription to activate the new genetic program (M. T. Lee et al, 2014), the chromatin is remodeled to stabilize the pluripotent state (Zhou & Dean, 2015), and maternal instructions in the form of mRNAs and proteins are actively cleared to remove the previous cellular identify (Giraldez, 2010; Tadros & Lipshitz, 2009; Walser & Lipshitz, 2011). Likewise, reprogramming to pluripotency in vitro requires activation of the pluripotency program (Takahashi & Yamanaka, 2006; Yu et al, 2007), chromatin remodeling (Apostolou & Hochedlinger, 2013), and less-well understood post-transcriptional mechanisms to erase the differentiated gene expression program.…”

Section: Introductionmentioning

confidence: 99%

The Maternal-to-Zygotic Transition During Vertebrate Development

Yartseva

Giráldez

2015

Current Topics in Developmental Biology

106

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Cellular transitions occur at all stages of organismal life from conception to adult regeneration. Changing cellular state involves three main features: activating gene expression necessary to install the new cellular state, modifying the chromatin status to stabilize the new gene expression program, and removing existing gene products to clear out the previous cellular program. The maternal-to-zygotic transition (MZT) is one of the most profound changes in the life of an organism. It involves gene expression remodeling at all levels, including the active clearance of the maternal oocyte program to adopt the embryonic totipotency. In this chapter we provide an overview of molecular mechanisms driving maternal mRNA clearance during the MZT, describe the developmental consequences of losing components of this gene regulation, and illustrate how remodeling of gene expression during the MZT is common to other cellular transitions with parallels to cellular reprogramming.

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“…In the mouse, zygotic genome activation (ZGA) is detectable in 1-cell stage embryos but occurs mostly at the 2-cell stage. MZT and ZGA are essential for continued development and establishment of totipotency34. The second event is embryo compaction, which initiates at 8-cell stage in mouse embryos.…”

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confidence: 99%

Towards Functional Annotation of the Preimplantation Transcriptome: An RNAi Screen in Mammalian Embryos

Cui

Dai

Marcho

et al. 2016

Sci Rep

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With readily available transcriptome-wide data, understanding the role of each expressed gene is an essential next step. Although RNAi technologies allow for genome-wide screens in cell culture, these approaches cannot replace strategies for discovery in the embryo. Here we present, for the first time, a knockdown screen in mouse preimplantation embryos. Early mammalian development encompasses dynamic cellular, molecular and epigenetic events that are largely conserved from mouse to man. We assayed 712 genes for requirements during preimplantation. We identified 59 genes required for successful development or outgrowth and implantation. We have characterized each phenotype and revealed cellular, molecular, and lineage specific defects following knockdown of transcript. Induced network analyses demonstrate this as a valid approach to identify networks of genes that play important roles during preimplantation. Our approach provides a robust and efficient strategy towards identification of novel phenotypes during mouse preimplantation and facilitates functional annotation of the mammalian transcriptome.

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Reprogramming the genome to totipotency in mouse embryos

Cited by 93 publications

References 102 publications

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

The Maternal-to-Zygotic Transition During Vertebrate Development

Towards Functional Annotation of the Preimplantation Transcriptome: An RNAi Screen in Mammalian Embryos

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