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Jason G Knott
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Soumen Paul Developmental Epigenetics Laboratory, Department of Pathology and Laboratory Medicine, Department of Animal Science, Michigan State University, East Lansing, Michigan 48824, USA

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Mammalian reproduction is critically dependent on the trophoblast cell lineage, which assures proper establishment of maternal–fetal interactions during pregnancy. Specification of trophoblast cell lineage begins with the development of the trophectoderm (TE) in preimplantation embryos. Subsequently, other trophoblast cell types arise with the progression of pregnancy. Studies with transgenic animal models as well as trophoblast stem/progenitor cells have implicated distinct transcriptional and epigenetic regulators in trophoblast lineage development. This review focuses on our current understanding of transcriptional and epigenetic mechanisms regulating specification, determination, maintenance and differentiation of trophoblast cells.

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Chad S Driscoll Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Jaehwan Kim Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA
Department of Animal Sciences, University of Missouri, Columbia, Missouri, USA

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Mohamed Ashry Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Jason G Knott Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Transcription factor AP2 gamma (TFAP2C) is a well-established regulator of the trophoblast lineage in mice and humans, but a handful of studies indicate that TFAP2C may play an important role in pluripotency. Here, we hypothesize and provide new evidence that TFAP2C functions as an activator of trophoblast and pluripotency genes during preimplantation embryo development.

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Virginia Savy Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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Virgilia Alberio Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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Natalia G Canel Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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Laura D Ratner Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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Maria I Gismondi Instituto de Biotecnología, CICVyA, INTA, Hurlingam, Buenos Aires, Argentina

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Sergio F Ferraris Centro de Ciencias Veterinarias, Universidad Maimónides, CABA, Argentina

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Rafael Fernandez-Martín Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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Jason G Knott Department of Animal Science, Michigan State University, East Lansing, Michigan, USA

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Romina J Bevacqua Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina
Seung Kim Lab, Department of Developmental Biology, Stanford University School of Medicine, Stanford, California, USA

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Daniel F Salamone Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires/INPA CONICET, CABA, Argentina

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CRISPR-mediated transcriptional activation, also known as CRISPR-on, has proven efficient for activation of individual or multiple endogenous gene expression in cultured cells from several species. However, the potential of CRISPR-on technology in preimplantation mammalian embryos remains to be explored. Here, we report for the first time the successful modulation of endogenous gene expression in bovine embryos by using the CRISPR-on system. As a proof of principle, we targeted the promoter region of either SMARCA4 or TFAP2C genes, transcription factors implicated in trophoblast lineage commitment during embryo development. We demonstrate that CRISPR-on provides temporal control of endogenous gene expression in bovine embryos, by simple cytoplasmic injection of CRISPR RNA components into one cell embryos. dCas9VP160 activator was efficiently delivered and accurately translated into protein, being detected in the nucleus of all microinjected blastomeres. Our approach resulted in the activation of SMARCA expression shortly after microinjection, with a consequent effect on downstream differentiation promoting factors, such as TFAP2C and CDX2. Although targeting of TFAP2C gene did not result in a significant increase in TFAP2C expression, there was a profound induction in CDX2 expression on day 2 of development. Finally, we demonstrate that CRISPR-on system is suitable for gene expression modulation during the preimplantation period, since no detrimental effect was observed on microinjected embryo development. This study constitutes a first step toward the application of the CRISPR-on system for the study of early embryo cell fate decisions in cattle and other mammalian embryos, as well as to design novel strategies that may lead to an improved trophectoderm development.

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