XB-ART-55340
Crit Rev Biochem Mol Biol
2018 Dec 01;536:579-595. doi: 10.1080/10409238.2018.1506733.
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Transcriptional quiescence in primordial germ cells.
Lebedeva LA
,
Yakovlev KV
,
Kozlov EN
,
Schedl P
,
Deshpande G
,
Shidlovskii YV
.
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In most animal species, newly formed primordial germ cells (PGCs) acquire the special characteristics that distinguish them from the surrounding somatic cells. Proper fate specification of the PGCs is coupled with transcriptional quiescence, whether they are segregated by determinative or inductive mechanisms. Inappropriate differentiation of PGCs into somatic cells is thought to be prevented due to repression of RNA polymerase (Pol) II-dependent transcription. In the case of a determinative mode of PGC formation (Drosophila, Caenorhabditis elegans, etc.), there is a broad downregulation of Pol II activity. By contrast, PGCs display only gene-specific repression in organisms that rely on inductive signaling-based mechanism (e.g., mice). In addition to the global block of Pol II activity in PGCs, gene expression can be suppressed in other ways, such as chromatin remodeling and Piwi-mediated RNAi. Here, we discuss the mechanisms responsible for the transcriptionally silent state of PGCs in common experimental animals, such as Drosophila, C. elegans, Danio rerio, Xenopus, and mouse. While a PGC-specific downregulation of transcription is a common feature among these organisms, the diverse nature of underlying mechanisms suggests that this functional trait likely evolved independently on several instances. We discuss the possible biological relevance of these silencing mechanisms vis-a-vis fate determination of PGCs.
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Species referenced: Xenopus
Genes referenced: pgc piwil1
GO keywords: germ cell development [+]
References [+] :
Abe,
Loss of heterochromatin protein 1 gamma reduces the number of primordial germ cells via impaired cell cycle progression in mice.
2011, Pubmed
Abe, Loss of heterochromatin protein 1 gamma reduces the number of primordial germ cells via impaired cell cycle progression in mice. 2011, Pubmed
Amikura, Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. 2001, Pubmed
Aravin, Small RNA silencing pathways in germ and stem cells. 2008, Pubmed
Asaoka, Maternal Nanos regulates zygotic gene expression in germline progenitors of Drosophila melanogaster. 1998, Pubmed
Barbash, Genetic and molecular analysis of the autosomal component of the primary sex determination signal of Drosophila melanogaster. 1995, Pubmed
Batista, PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. 2008, Pubmed
Beams, The problem of germ cell determinants. 1974, Pubmed , Xenbase
Bentley, Coupling mRNA processing with transcription in time and space. 2014, Pubmed
Bernstein, A bivalent chromatin structure marks key developmental genes in embryonic stem cells. 2006, Pubmed
Bhandari, Structural basis for the Nanos-mediated recruitment of the CCR4-NOT complex and translational repression. 2014, Pubmed
Breen, Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster. 1986, Pubmed
Brower-Toland, Drosophila PIWI associates with chromatin and interacts directly with HP1a. 2007, Pubmed
Brown, Transcriptional regulation at the nuclear pore complex. 2007, Pubmed
Buckley, A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. 2012, Pubmed
Burton, A Pluripotency Platform for Prdm14. 2016, Pubmed
Butler, Primordial Germ Cell Isolation from Xenopus laevis Embryos. 2017, Pubmed , Xenbase
Campbell, Dynamic visualization of transcription and RNA subcellular localization in zebrafish. 2015, Pubmed
Castel, RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. 2013, Pubmed
Checchi, emb-4 is a conserved gene required for efficient germline-specific chromatin remodeling during Caenorhabditis elegans embryogenesis. 2006, Pubmed
Cinalli, A spindle-independent cleavage pathway controls germ cell formation in Drosophila. 2013, Pubmed
Cline, Vive la différence: males vs females in flies vs worms. 1996, Pubmed
Cox, A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. 1998, Pubmed
Das, Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. 2008, Pubmed
Deshpande, Overlapping mechanisms function to establish transcriptional quiescence in the embryonic Drosophila germline. 2004, Pubmed
Deshpande, Drosophila argonaute-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. 2005, Pubmed
Deshpande, The drosophila fragile X protein dFMR1 is required during early embryogenesis for pole cell formation and rapid nuclear division cycles. 2006, Pubmed
Deshpande, Novel functions of nanos in downregulating mitosis and transcription during the development of the Drosophila germline. 1999, Pubmed
Deshpande, BMP signaling and the maintenance of primordial germ cell identity in Drosophila embryos. 2014, Pubmed
Dimitrov, Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. 1993, Pubmed , Xenbase
Dorafshan, Hierarchical recruitment of Polycomb complexes revisited. 2017, Pubmed
Dorfman, Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. 2001, Pubmed
Dosch, Next generation mothers: Maternal control of germline development in zebrafish. 2015, Pubmed
Dönertas, Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. 2013, Pubmed
Endoh, Correction: PCGF6-PRC1 suppresses premature differentiation of mouse embryonic stem cells by regulating germ cell-related genes. 2017, Pubmed
Erickson, A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. 1993, Pubmed
Eun, Polycomb Group Gene E(z) Is Required for Spermatogonial Dedifferentiation in Drosophila Adult Testis. 2017, Pubmed
Extavour, Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. 2007, Pubmed
Extavour, Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. 2003, Pubmed
Fang, A PAX5-OCT4-PRDM1 developmental switch specifies human primordial germ cells. 2018, Pubmed
Faunes, Characterization of small RNAs in X. tropicalis gastrulae. 2012, Pubmed , Xenbase
Fedorova, Nuclear architecture and gene regulation. 2008, Pubmed
Frise, Systematic image-driven analysis of the spatial Drosophila embryonic expression landscape. 2010, Pubmed
Ghosh, Inhibition of transcription by the Caenorhabditis elegans germline protein PIE-1: genetic evidence for distinct mechanisms targeting initiation and elongation. 2008, Pubmed
Griesenbeck, Structure and Function of RNA Polymerases and the Transcription Machineries. 2017, Pubmed
Grimaud, RNAi components are required for nuclear clustering of Polycomb group response elements. 2006, Pubmed
Gupta, Zooming in on Transcription Preinitiation. 2016, Pubmed
Guven-Ozkan, Global transcriptional repression in C. elegans germline precursors by regulated sequestration of TAF-4. 2008, Pubmed
Günesdogan, Developmental Competence for Primordial Germ Cell Fate. 2016, Pubmed
Günesdogan, Primordial germ cell specification: a context-dependent cellular differentiation event [corrected]. 2014, Pubmed
Haig, Transposable elements: Self-seekers of the germline, team-players of the soma. 2016, Pubmed
Hampoelz, Pre-assembled Nuclear Pores Insert into the Nuclear Envelope during Early Development. 2016, Pubmed
Hanyu-Nakamura, Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. 2008, Pubmed
Haynie, The maternal and zygotic roles of the gene Polycomb in embryonic determination in Drosophila melanogaster. 1983, Pubmed
Heidemann, Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. 2013, Pubmed
Houwing, Zili is required for germ cell differentiation and meiosis in zebrafish. 2008, Pubmed
Houwing, A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. 2007, Pubmed
Iovino, PRC2 controls Drosophila oocyte cell fate by repressing cell cycle genes. 2013, Pubmed
Irie, SOX17 is a critical specifier of human primordial germ cell fate. 2015, Pubmed
Iwasaki, Piwi Modulates Chromatin Accessibility by Regulating Multiple Factors Including Histone H1 to Repress Transposons. 2016, Pubmed
Jongens, The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. 1992, Pubmed
Jongens, Germ cell-less encodes a cell type-specific nuclear pore-associated protein and functions early in the germ-cell specification pathway of Drosophila. 1994, Pubmed
Kadyrova, Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. 2007, Pubmed
Kahn, Interdependence of PRC1 and PRC2 for recruitment to Polycomb Response Elements. 2016, Pubmed
Kaltenbach, The TBP-like factor CeTLF is required to activate RNA polymerase II transcription during C. elegans embryogenesis. 2000, Pubmed
Kasper, Homeland security in the C. elegans germ line: insights into the biogenesis and function of piRNAs. 2014, Pubmed
Kassis, Polycomb group response elements in Drosophila and vertebrates. 2013, Pubmed
Kawasaki, The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. 2004, Pubmed
Klenov, Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. 2007, Pubmed
Knaut, Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. 2000, Pubmed
Kobayashi, Essential role of the posterior morphogen nanos for germline development in Drosophila. 1996, Pubmed
Kopytova, Two isoforms of Drosophila TRF2 are involved in embryonic development, premeiotic chromatin condensation, and proper differentiation of germ cells of both sexes. 2006, Pubmed
Korf, The Polycomb group in Caenorhabditis elegans and maternal control of germline development. 1998, Pubmed
Kumano, A maternal factor unique to ascidians silences the germline via binding to P-TEFb and RNAP II regulation. 2011, Pubmed
Kwak, Control of transcriptional elongation. 2013, Pubmed
Lai, Xenopus Nanos1 is required to prevent endoderm gene expression and apoptosis in primordial germ cells. 2012, Pubmed , Xenbase
Lamb, Increase in nuclear poly(A)-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. 1976, Pubmed
Lau, Systematic and single cell analysis of Xenopus Piwi-interacting RNAs and Xiwi. 2009, Pubmed , Xenbase
Leatherman, germ cell-less acts to repress transcription during the establishment of the Drosophila germ cell lineage. 2002, Pubmed
Lee, Nanos promotes epigenetic reprograming of the germline by down-regulation of the THAP transcription factor LIN-15B. 2017, Pubmed
Lee, Genome-wide activities of Polycomb complexes control pervasive transcription. 2015, Pubmed
Lerit, Germ Cell-less Promotes Centrosome Segregation to Induce Germ Cell Formation. 2017, Pubmed
Lesch, A set of genes critical to development is epigenetically poised in mouse germ cells from fetal stages through completion of meiosis. 2013, Pubmed
Li, Coactivation of STAT and Ras is required for germ cell proliferation and invasive migration in Drosophila. 2003, Pubmed
Li, Germ cell-less expression in zebrafish embryos. 2006, Pubmed
Little, Independent and coordinate trafficking of single Drosophila germ plasm mRNAs. 2015, Pubmed
Lécuyer, Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. 2007, Pubmed
Ma, Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. 2011, Pubmed
Magnúsdóttir, A tripartite transcription factor network regulates primordial germ cell specification in mice. 2013, Pubmed
Manakov, MIWI2 and MILI Have Differential Effects on piRNA Biogenesis and DNA Methylation. 2015, Pubmed
Martinho, A noncoding RNA is required for the repression of RNApolII-dependent transcription in primordial germ cells. 2004, Pubmed
Müller, TBP is not universally required for zygotic RNA polymerase II transcription in zebrafish. 2001, Pubmed
Nakaki, PRDM14: a unique regulator for pluripotency and epigenetic reprogramming. 2014, Pubmed
Nakamura, Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. 1996, Pubmed
Nili, Nuclear membrane protein LAP2beta mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). 2001, Pubmed
Pae, GCL and CUL3 Control the Switch between Cell Lineages by Mediating Localized Degradation of an RTK. 2017, Pubmed
Pan, Role of H1 linker histones in mammalian development and stem cell differentiation. 2016, Pubmed
Panov, Transcription co-activator SAYP mediates the action of STAT activator. 2012, Pubmed
Patel, Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types. 2012, Pubmed
Peng, Piwi maintains germline stem cells and oogenesis in Drosophila through negative regulation of Polycomb group proteins. 2016, Pubmed
Pirrotta, Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression. 1997, Pubmed
Ptak, The multifunctional nuclear pore complex: a platform for controlling gene expression. 2014, Pubmed
Pérez-Montero, The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. 2013, Pubmed
Qi, The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. 2011, Pubmed
Robertson, germ cell-less is required only during the establishment of the germ cell lineage of Drosophila and has activities which are dependent and independent of its localization to the nuclear envelope. 1999, Pubmed
Rudolph, Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3-3. 2007, Pubmed
Schaefer, Epigenetic decisions in mammalian germ cells. 2007, Pubmed
Schaner, A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. 2003, Pubmed
Schwartz, Ruled by ubiquitylation: a new order for polycomb recruitment. 2014, Pubmed
Seki, Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. 2005, Pubmed
Seydoux, Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. 1997, Pubmed
Seydoux, Repression of gene expression in the embryonic germ lineage of C. elegans. 1996, Pubmed
Shpiz, rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus. 2009, Pubmed
Sienski, Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. 2012, Pubmed
Sienski, Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. 2015, Pubmed
Soto, Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. 1995, Pubmed
Su, The cell cycle program in germ cells of the Drosophila embryo. 1998, Pubmed
Surani, Genetic and epigenetic regulators of pluripotency. 2007, Pubmed
Suzuki, Loss of MAX results in meiotic entry in mouse embryonic and germline stem cells. 2016, Pubmed
Suzuki, TBP-like protein (TLP) interferes with Taspase1-mediated processing of TFIIA and represses TATA box gene expression. 2015, Pubmed
Tavares, RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. 2012, Pubmed
Trcek, Drosophila germ granules are structured and contain homotypic mRNA clusters. 2015, Pubmed
Tsuda, Conserved role of nanos proteins in germ cell development. 2003, Pubmed
Tu, Co-repressor CBFA2T2 regulates pluripotency and germline development. 2016, Pubmed
Tóth, The piRNA Pathway Guards the Germline Genome Against Transposable Elements. 2016, Pubmed
Vorobyeva, The novel regulator of metazoan development SAYP organizes a nuclear coactivator supercomplex. 2009, Pubmed
Voronina, RNA granules in germ cells. 2011, Pubmed
Wang, Key Signaling Events for Committing Mouse Pluripotent Stem Cells to the Germline Fate. 2016, Pubmed
Wang, Germ cell specification. 2013, Pubmed
Wei, Transcriptome-wide analysis of small RNA expression in early zebrafish development. 2012, Pubmed
Wilczynska, Two Piwi proteins, Xiwi and Xili, are expressed in the Xenopus female germline. 2009, Pubmed , Xenbase
Wright, TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. 2006, Pubmed
Yamaguchi, Nanog expression in mouse germ cell development. 2005, Pubmed
Yang, Multiple LINEs of retrotransposon silencing mechanisms in the mammalian germline. 2016, Pubmed
Yang, The Xenopus Maternal-to-Zygotic Transition from the Perspective of the Germline. 2015, Pubmed , Xenbase
Yokobayashi, PRC1 coordinates timing of sexual differentiation of female primordial germ cells. 2013, Pubmed
Yuda, Global transcriptional repression: An initial and essential step for Plasmodium sexual development. 2015, Pubmed