XB-ART-57118
Curr Top Dev Biol
2020 Jan 01;140:87-118. doi: 10.1016/bs.ctdb.2020.02.007.
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Organizing the oocyte: RNA localization meets phase separation.
Cabral SE
,
Mowry KL
.
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RNA localization is a key biological strategy for organizing the cytoplasm and generating both cellular and developmental polarity. During RNA localization, RNAs are targeted asymmetrically to specific subcellular destinations, resulting in spatially and temporally restricted gene expression through local protein synthesis. First discovered in oocytes and embryos, RNA localization is now recognized as a significant regulatory strategy for diverse RNAs, both coding and non-coding, in a wide range of cell types. Yet, the highly polarized cytoplasm of the oocyte remains a leading model to understand not only the principles and mechanisms underlying RNA localization, but also links to the formation of biomolecular condensates through phase separation. Here, we discuss both RNA localization and biomolecular condensates in oocytes with a particular focus on the oocyte of the frog, Xenopus laevis.
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R01 GM071049 NIGMS NIH HHS
Species referenced: Xenopus laevis
References [+] :
Alberti,
Are aberrant phase transitions a driver of cellular aging?
2016, Pubmed
Alberti, Are aberrant phase transitions a driver of cellular aging? 2016, Pubmed
Banani, Compositional Control of Phase-Separated Cellular Bodies. 2016, Pubmed
Banani, Biomolecular condensates: organizers of cellular biochemistry. 2017, Pubmed
Bashirullah, Spatial and temporal control of RNA stability. 2001, Pubmed
Berry, RNA transcription modulates phase transition-driven nuclear body assembly. 2015, Pubmed
Birsoy, Vg 1 is an essential signaling molecule in Xenopus development. 2006, Pubmed , Xenbase
Blower, Molecular insights into intracellular RNA localization. 2013, Pubmed
Boke, Amyloid-like Self-Assembly of a Cellular Compartment. 2016, Pubmed , Xenbase
Bovaird, Biological functions, regulatory mechanisms, and disease relevance of RNA localization pathways. 2018, Pubmed
Brangwynne, Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. 2011, Pubmed , Xenbase
Brangwynne, Germline P granules are liquid droplets that localize by controlled dissolution/condensation. 2009, Pubmed
Brendza, A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. 2000, Pubmed
Bubunenko, A consensus RNA signal that directs germ layer determinants to the vegetal cortex of Xenopus oocytes. 2002, Pubmed , Xenbase
Buchan, mRNP granules. Assembly, function, and connections with disease. 2014, Pubmed
Bullock, Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. 2001, Pubmed
Buskila, RNA localization in bacteria. 2014, Pubmed
Buxbaum, In the right place at the right time: visualizing and understanding mRNA localization. 2015, Pubmed
Cabili, Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. 2015, Pubmed
Cajigas, The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. 2012, Pubmed
Cha, Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. 2002, Pubmed
Chan, fatvg encodes a new localized RNA that uses a 25-nucleotide element (FVLE1) to localize to the vegetal cortex of Xenopus oocytes. 1999, Pubmed , Xenbase
Chan, The vegetally localized mRNA fatvg is associated with the germ plasm in the early embryo and is later expressed in the fat body. 2001, Pubmed , Xenbase
Chang, Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. 2004, Pubmed , Xenbase
Chen, Linking Long Noncoding RNA Localization and Function. 2016, Pubmed
Chen, Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein. 2014, Pubmed
Clark, A Dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte. 2007, Pubmed
Clemson, An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. 2009, Pubmed
Cody, The many functions of mRNA localization during normal development and disease: from pillar to post. 2013, Pubmed , Xenbase
Colegrove-Otero, The Xenopus ELAV protein ElrB represses Vg1 mRNA translation during oogenesis. 2005, Pubmed , Xenbase
Cote, A Xenopus protein related to hnRNP I has a role in cytoplasmic RNA localization. 1999, Pubmed , Xenbase
CRICK, On protein synthesis. 1958, Pubmed
Cumberworth, Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. 2013, Pubmed
Czaplinski, Identification of 40LoVe, a Xenopus hnRNP D family protein involved in localizing a TGF-beta-related mRNA during oogenesis. 2005, Pubmed , Xenbase
Dale, Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis. 1989, Pubmed , Xenbase
Das, The travels of mRNAs in neurons: do they know where they are going? 2019, Pubmed
Davis, Apical localization of pair-rule transcripts requires 3' sequences and limits protein diffusion in the Drosophila blastoderm embryo. 1991, Pubmed
Decker, P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. 2012, Pubmed
Deshler, A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. 1998, Pubmed , Xenbase
Dienstbier, Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motor. 2009, Pubmed
Ding, Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. 1993, Pubmed
Ditlev, Who's In and Who's Out-Compositional Control of Biomolecular Condensates. 2018, Pubmed
Du, Why cells move messages: the biological functions of mRNA localization. 2007, Pubmed
Dumont, Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. 1972, Pubmed , Xenbase
Duncan, The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte. 2002, Pubmed
Elbaum-Garfinkle, The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. 2015, Pubmed
Elbaum-Garfinkle, Liquids, Fibers, and Gels: The Many Phases of Neurodegeneration. 2015, Pubmed
Ephrussi, Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. 1991, Pubmed
Fay, The Role of RNA in Biological Phase Separations. 2018, Pubmed
Feric, Coexisting Liquid Phases Underlie Nucleolar Subcompartments. 2016, Pubmed , Xenbase
Forrest, Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. 2003, Pubmed
Forristall, Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. 1995, Pubmed , Xenbase
Gagnon, Directional transport is mediated by a Dynein-dependent step in an RNA localization pathway. 2013, Pubmed , Xenbase
Gagnon, Molecular motors: directing traffic during RNA localization. 2011, Pubmed , Xenbase
Gáspár, An RNA-binding atypical tropomyosin recruits kinesin-1 dynamically to oskar mRNPs. 2017, Pubmed
Gavis, Localization of nanos RNA controls embryonic polarity. 1992, Pubmed
Han, Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. 2012, Pubmed
Hanazawa, PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans. 2011, Pubmed
Havin, RNA-binding protein conserved in both microtubule- and microfilament-based RNA localization. 1998, Pubmed , Xenbase
Hayes, Dual roles for ATP in the regulation of phase separated protein aggregates in Xenopus oocyte nucleoli. 2018, Pubmed , Xenbase
Heasman, Vegetal localization of maternal mRNAs is disrupted by VegT depletion. 2001, Pubmed , Xenbase
Heasman, The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. 1984, Pubmed , Xenbase
Holt, Subcellular mRNA localization in animal cells and why it matters. 2009, Pubmed
Houston, A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. 1998, Pubmed , Xenbase
Houston, Regulation of cell polarity and RNA localization in vertebrate oocytes. 2013, Pubmed , Xenbase
Hudson, Identification of new localized RNAs in the Xenopus oocyte by differential display PCR. 1996, Pubmed , Xenbase
Hyman, Liquid-liquid phase separation in biology. 2014, Pubmed
Jain, RNA phase transitions in repeat expansion disorders. 2017, Pubmed
Jambhekar, Cis-acting determinants of asymmetric, cytoplasmic RNA transport. 2007, Pubmed
Januschke, Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. 2002, Pubmed
Jeffery, Localization of actin messenger RNA during early ascidian development. 1983, Pubmed
Joseph, Mutant Vg1 ligands disrupt endoderm and mesoderm formation in Xenopus embryos. 1998, Pubmed , Xenbase
Kato, Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. 2012, Pubmed
Kawasaki, PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. 1998, Pubmed
Kedersha, Stress granules and cell signaling: more than just a passing phase? 2013, Pubmed
Kiebler, Neuronal RNA granules: movers and makers. 2006, Pubmed
King, Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. 2005, Pubmed , Xenbase
Kislauskis, beta-Actin messenger RNA localization and protein synthesis augment cell motility. 1997, Pubmed
Kislauskis, Isoform-specific 3'-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. 1993, Pubmed
Kislauskis, Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. 1994, Pubmed
Kistler, Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells. 2018, Pubmed
Kloc, Translocation of repetitive RNA sequences with the germ plasm in Xenopus oocytes. 1993, Pubmed , Xenbase
Kloc, Organization of cytokeratin cytoskeleton and germ plasm in the vegetal cortex of Xenopus laevis oocytes depends on coding and non-coding RNAs: three-dimensional and ultrastructural analysis. 2007, Pubmed , Xenbase
Kloc, Potential structural role of non-coding and coding RNAs in the organization of the cytoskeleton at the vegetal cortex of Xenopus oocytes. 2005, Pubmed , Xenbase
Kloc, Binary function of mRNA. 2011, Pubmed , Xenbase
Kloc, Balbiani body, nuage and sponge bodies--term plasm pathway players. 2014, Pubmed , Xenbase
Kloc, Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. 1995, Pubmed , Xenbase
Kloc, The Balbiani body and germ cell determinants: 150 years later. 2004, Pubmed
Kofron, Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. 1999, Pubmed , Xenbase
Kugler, Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. 2009, Pubmed
Langdon, mRNA structure determines specificity of a polyQ-driven phase separation. 2018, Pubmed
Langdon, A New Lens for RNA Localization: Liquid-Liquid Phase Separation. 2018, Pubmed
Lawrence, Intracellular localization of messenger RNAs for cytoskeletal proteins. 1986, Pubmed
Lécuyer, Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. 2007, Pubmed
Lewis, PTB/hnRNP I is required for RNP remodeling during RNA localization in Xenopus oocytes. 2008, Pubmed , Xenbase
Lewis, Conserved and clustered RNA recognition sequences are a critical feature of signals directing RNA localization in Xenopus oocytes. 2004, Pubmed , Xenbase
Lin, Formation and Maturation of Phase-Separated Liquid Droplets by RNA-Binding Proteins. 2015, Pubmed
Long, Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. 1997, Pubmed
Macdonald, cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. 1988, Pubmed
Macdonald, Mutational analysis of an RNA recognition element that mediates localization of bicoid mRNA. 1998, Pubmed
MacDougall, Drosophila gurken (TGFalpha) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps. 2003, Pubmed
Maharana, RNA buffers the phase separation behavior of prion-like RNA binding proteins. 2018, Pubmed
Mahowald, Assembly of the Drosophila germ plasm. 2001, Pubmed
Marchand, An intracellular transmission control protocol: assembly and transport of ribonucleoprotein complexes. 2012, Pubmed
Mardakheh, Global Analysis of mRNA, Translation, and Protein Localization: Local Translation Is a Key Regulator of Cell Protrusions. 2015, Pubmed
Martin, mRNA localization: gene expression in the spatial dimension. 2009, Pubmed
Martin, Local protein synthesis and its role in synapse-specific plasticity. 2000, Pubmed
McClintock, RNA-directed activation of cytoplasmic dynein-1 in reconstituted transport RNPs. 2018, Pubmed
Medioni, Principles and roles of mRNA localization in animal development. 2012, Pubmed
Mercer, Noncoding RNAs in Long-Term Memory Formation. 2008, Pubmed
Messitt, Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. 2008, Pubmed , Xenbase
Mingle, Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. 2005, Pubmed
Mittag, Multiple Modes of Protein-Protein Interactions Promote RNP Granule Assembly. 2018, Pubmed
Molliex, Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. 2015, Pubmed
Mosquera, A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain. 1993, Pubmed , Xenbase
Mowry, Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. 1992, Pubmed , Xenbase
Mowry, Complex formation between stage-specific oocyte factors and a Xenopus mRNA localization element. 1996, Pubmed , Xenbase
Murakami, ALS/FTD Mutation-Induced Phase Transition of FUS Liquid Droplets and Reversible Hydrogels into Irreversible Hydrogels Impairs RNP Granule Function. 2015, Pubmed
Niepielko, Stochastic Seeding Coupled with mRNA Self-Recruitment Generates Heterogeneous Drosophila Germ Granules. 2018, Pubmed
Nieuwkoop, The Formation of the Mesoderm in Urodelean Amphibians : II. The origin of the dorso-ventral polarity of the mesoderm. 1969, Pubmed
Noh, Cytoplasmic functions of long noncoding RNAs. 2018, Pubmed
Okita, mRNA localization in plants: targeting to the cell's cortical region and beyond. 2002, Pubmed
Otero, A 250-nucleotide UA-rich element in the 3' untranslated region of Xenopus laevis Vg1 mRNA represses translation both in vivo and in vitro. 2001, Pubmed , Xenbase
Patel, A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation. 2015, Pubmed
Pederson, The nucleolus. 2011, Pubmed
Puthanveettil, RNA transport and long-term memory storage. 2013, Pubmed
Putnam, A gel phase promotes condensation of liquid P granules in Caenorhabditis elegans embryos. 2019, Pubmed
Rebagliati, Identification and cloning of localized maternal RNAs from Xenopus eggs. 1985, Pubmed , Xenbase
Rodriguez, Mechanisms and cellular roles of local protein synthesis in mammalian cells. 2008, Pubmed
Saha, Polar Positioning of Phase-Separated Liquid Compartments in Cells Regulated by an mRNA Competition Mechanism. 2016, Pubmed
Semotok, Drosophila maternal Hsp83 mRNA destabilization is directed by multiple SMAUG recognition elements in the open reading frame. 2008, Pubmed
Seydoux, The P Granules of C. elegans: A Genetic Model for the Study of RNA-Protein Condensates. 2018, Pubmed
Singer-Krüger, Here, there, everywhere. mRNA localization in budding yeast. 2014, Pubmed
Singh, The Clothes Make the mRNA: Past and Present Trends in mRNP Fashion. 2015, Pubmed
Smith, Spatial patterning of P granules by RNA-induced phase separation of the intrinsically-disordered protein MEG-3. 2016, Pubmed
St Johnston, Moving messages: the intracellular localization of mRNAs. 2005, Pubmed
Strome, Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. 1982, Pubmed
Sudarwati, Mesoderm formation in the anuranXenopus laevis (Daudin). 1971, Pubmed
Sundell, Requirement of microfilaments in sorting of actin messenger RNA. 1991, Pubmed
Tadros, SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. 2007, Pubmed
Takizawa, The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p. 2000, Pubmed
Tannahill, Localized synthesis of the Vg1 protein during early Xenopus development. 1989, Pubmed , Xenbase
Thiry, Birth of a nucleolus: the evolution of nucleolar compartments. 2005, Pubmed
Thomsen, Processed Vg1 protein is an axial mesoderm inducer in Xenopus. 1993, Pubmed , Xenbase
Trcek, Germ granules in Drosophila. 2019, Pubmed
Updike, P granule assembly and function in Caenorhabditis elegans germ cells. 2010, Pubmed
Van de Bor, mRNA localisation gets more complex. 2004, Pubmed
Van Treeck, Emerging Roles for Intermolecular RNA-RNA Interactions in RNP Assemblies. 2018, Pubmed
Van Treeck, RNA self-assembly contributes to stress granule formation and defining the stress granule transcriptome. 2018, Pubmed
Voronina, RNA granules in germ cells. 2011, Pubmed
Wallace, The induced synthesis and transport of yolk proteins and their accumulation by the oocyte in Xenopus laevis. 1968, Pubmed , Xenbase
Weatheritt, Asymmetric mRNA localization contributes to fidelity and sensitivity of spatially localized systems. 2014, Pubmed
Weber, Inverse size scaling of the nucleolus by a concentration-dependent phase transition. 2015, Pubmed
Weil, mRNA localization in the Drosophila germline. 2014, Pubmed
Weiss, Non-coding mechanisms of local mRNA translation in neuronal dendrites. 2015, Pubmed
White, Maternal control of pattern formation in Xenopus laevis. 2008, Pubmed , Xenbase
Wilk, Diverse and pervasive subcellular distributions for both coding and long noncoding RNAs. 2016, Pubmed
Wilkie, Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. 2001, Pubmed
Xiang, The LC Domain of hnRNPA2 Adopts Similar Conformations in Hydrogel Polymers, Liquid-like Droplets, and Nuclei. 2015, Pubmed
Yisraeli, A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. 1990, Pubmed , Xenbase
Yoon, Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin. 2004, Pubmed , Xenbase
Zaessinger, Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. 2006, Pubmed
Zearfoss, Hermes is a localized factor regulating cleavage of vegetal blastomeres in Xenopus laevis. 2004, Pubmed , Xenbase
Zearfoss, Identification of new Xlsirt family members in the Xenopus laevis oocyte. 2003, Pubmed , Xenbase
Zhang, The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. 1998, Pubmed , Xenbase
Zhang, RNA Controls PolyQ Protein Phase Transitions. 2015, Pubmed
Zhang, Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. 1996, Pubmed , Xenbase
Zhang, Neurotrophin regulation of beta-actin mRNA and protein localization within growth cones. 1999, Pubmed
Zimyanin, In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. 2008, Pubmed