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Uterine and Placental KISS1 Regulate Pregnancy: What We Know and The

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Uterine and Placental KISS1 Regulate Pregnancy: What We Know and The REPRODUCTIONREVIEW Transcriptional regulators of the trophoblast lineage in mammals with hemochorial placentation Jason G Knott and Soumen Paul1 Developmental Epigenetics Laboratory, Department of Animal Science, Michigan State University, East Lansing, Michigan 48824, USA and 1Department of Pathology and Laboratory Medicine, Institute of Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, Kansas 66160, USA Correspondence should be addressed to S Paul; Email: [email protected] Abstract 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. Reproduction (2014) 148 R121–R136 Introduction human trophoblast development is restricted due to ethical reasons and lack of proper model systems. Thus, Mammalian reproduction is uniquely characterized the majority of our understanding of transcriptional by the formation of the placenta, a transient extraem- mechanisms that regulate trophoblast development bryonic organ that mediates dynamic interaction comes from studies in rodent models. between embryonic and maternal tissues and ensures Humans possess hemochorial placenta, in which the successful development of the embryo proper. This maternal blood is in direct contact with chorionic intimate relationship between the embryo and mother trophoblast cells, thereby facilitating nutrient exchanges is crucially dependent upon trophoblast cells as they between mother and the fetus. Interestingly, rodents, mediate uterine implantation, initiate the process of such as mouse and rat, also possess hemochorial placentation, and modulate vascular, endocrine and placenta (Rossant & Cross 2001, Soares et al. 2012). immunological properties to support successful preg- Placentation in both rodent and human is associated nancy. Improper trophectoderm (TE) specification results with the invasion of trophoblast cells into the uterine in either arrested preimplantation development or wall and remodeling of uterine spiral arteries with defective embryo implantation (Rossant & Cross 2001, invasive trophoblast cells. Despite several differences Cockburn & Rossant 2010, Roberts & Fisher 2011, Pfeffer between rodent and human placentation (Carter 2007), & Pearton 2012), which are the leading causes of early they share similar regulatory mechanisms controlling pregnancy failure. After embryo implantation, defective placental development (Rossant & Cross 2001, Pfeffer & development and function of trophoblast cells can lead Pearton 2012). Therefore, analyses of mutant mice to pregnancy failure and pregnancy-associated patho- provide opportunities to understand the functional logical conditions such as preeclampsia and intrauterine importance of transcription factors in trophoblast growth restriction (IUGR; Rossant & Cross 2001, development in hemochorial placentation. Successful Redman & Sargent 2005, Myatt 2006, Pfeffer & Pearton derivation of trophoblast stem cells (TSCs) from rodent 2012). Thus, a proper understanding of regulatory blastocysts (Tanaka et al. 1998, Asanoma et al. 2011) has mechanisms that control specification, differentiation also provided the excellent cell-based systems for and function of trophoblast cell types is critical for the biochemical analyses including mechanistic studies on advancement of infertility treatment and the improve- chromatin. The majority of the following discussion ment of reproductive health. However, our scope will be focused on our understanding from studies in for studying molecular mechanisms in the regulation of rodent models. q 2014 Society for Reproduction and Fertility DOI: 10.1530/REP-14-0072 ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org Downloaded from Bioscientifica.com at 10/05/2021 08:14:52AM via free access R122 J G Knott and S Paul Placental development and trophoblast cell types in Rossant & Cross 2001, Simmons & Cross 2005, Watson & rodents and human Cross 2005). In contrast, proliferation and differentiation of polar TE results in the formation of the ectoplacental cone Development of trophoblast cell lineage is a multi-step (EPC) and the chorion (Fig. 1B; Simmons & Cross 2005), process (Fig. 1). Specification of the TE, one of the first which arise during gastrulation (w7.0–7.25 dpc). The EPC two cell lineages within the preimplantation embryo is developed from polar TE-derived extra-embryonic (Kunath et al. 2004, Rossant 2004), initiates trophoblast ectoderm (ExE) and contributes to the formation of the development. The other earliest lineage is the inner cell junctional zone, a compact layer of cells sandwiched- mass (ICM), which contributes to the embryo proper. between the labyrinth zone and the maternal decidua Studies in rodent models indicate that TE cells, over- (Fig. 1C, a). Development of the labyrinth zone (Fig. 1C, a) laying the ICM (polar TE), contribute to the majority of starts with the attachment of the allantois to the chorion the trophoblast tissue and therefore are considered to be (Fig. 1B, b) at wE8.5 (Simmons & Cross 2005, Cross the TSC population (Rossant 2001). Establishment of et al. 2006). The chorion is a bilayered tissue with a layer bona fide TSC populations from rodent blastocysts of ExE-derived chorionic ectoderm (ChE), which (Tanaka et al. 1998, Asanoma et al.2011) further contains trophoblast stem/progenitor cells. Subsequent supports this concept. to chorio-allantoic attachment, differentiation and Rodent blastocysts implant to the uterus through mural morphogenesis of chorionic trophoblast progenitors and TE cells that are not in contact with the ICM (Fig. 1A). After establishment of vascular network from the allantoic implantation, cells of mural TE differentiate into post- mesoderm (Cross et al.2006) lead to the formation of mitotic primary trophoblast giant cells (primary TGCs; the labyrinth zone, which mediates nutrient exchange between the fetus and mother. Although the gross architecture of a rodent placenta A E3.5 has been known for many years, a more complete Polar TE Epiblast understanding of the hierarchy of the murine trophoblast Hypoblast Development of cell lineage has only been obtained recently (Uy et al. TE in the preimplantation 2002, Simmons et al. 2007, Mould et al. 2012, Ueno Mural embryo One-cell TE et al. 2013). Establishment of FGF4-dependent TSCs embryo Blastocyst from dissociated ExEs/EPCs and ChEs from postim- plantation mouse embryos (Tanaka et al. 1998, Uy B E7.5 E7.5 Primary et al. 2002) confirmed the presence of trophoblast cells EPC TGC EPC (contributes with TSC-potential within those tissues. However, to junctional zone) studies in mice predicted that a bonafide TSC population EPC cavity Development of trophoblast does not persist after the closure of EPC cavity (Uy et al. Chorion progenitors in Alantois extraembryonic tissues during 2002). Rather, recent studies (Simmons et al. 2007, (Contribute to gastrulation labyrinth Mould et al.2012, Ueno et al.2013)inmice zone) a Amnion b have suggested the presence of specific progenitor populations within the junctional and labyrinth zones C Uterine spiral Invasive trophoblasts that could differentiate into specific specialized tropho- artery SpA-TGC Decidual blast cells of the mature placenta. cells Spiral Decidua artery Development of the junctional zone from the EPC is P-TGC associated with the derivation of multiple specialized Juctional zone Development of Arterial differentiated trophoblast cells, namely i) spongiotropblasts, ii) glyco- canal trophoblast Glycogen subtypes with gen cells and iii) secondary TGCs (Fig. 1C, b (top)). Based Spongiotrophoblasts cells specific C-TGC functions on the localization and gene expression patterns in the maturing Matemal placenta (Simmons et al. 2007, Hu & Cross 2010), three subtypes blood sinusoid of secondary TGCs were classified within the junctional S-TGC zone and the decidua. These include the i) maternal SynTB-I arterial canal-associated TGCs (c-TGCs), ii) parietal- SynTB-II Fetal TGCs (p-TGCs) lining the implantation site, and iii) spiral a b vasculature artery-associated TGCs (SpA-TGC), which along with Figure 1 Different stages of mouse trophoblast development. (A) glycogen cells invade the decidua and therefore are Establishment of the TE in preimplantation embryo initiates trophoblast denoted invasive trophoblasts. Some of these invasive development. (B) Location of trophoblast progenitors in E7.5 mouse trophoblasts then associate with the uterine spiral arteries conceptus. (a) EPC in an E7.5 mouse embryo. (b) A cross section of an and remodel the arterial endothelium to establish E7.5 mouse embryo and a cartoon to indicate localization of primary TGCs and trophoblast progenitors. (C) Cartoons indicate different endovascular trophoblast population. Interestingly, line- regions of a mouse placenta (a) and differentiated trophoblast subtypes age-tracing studies indicated that these
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