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Localization in Oogenesis of Maternal Regulators of Embryonic Development

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Vertebrate Development

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 953))

Abstract

Cell polarity generates intracellular asymmetries and functional regionalization in tissues and morphogenetic processes. Cell polarity in development often relies on mechanisms of RNA localization to specific subcellular domains to define the identity of future developing tissues. The totipotent egg of most animals illustrates in a grand way the importance of cell polarity and RNA localization in regulating multiple crucial developmental events. The polarization of the egg arises during its development in oogenesis. RNAs localize asymmetrically in the early oocyte defining its animal-vegetal (AV) axis, which upon further elaboration in mid- and late-oogenesis stages produces a mature egg with specific localized factors along its AV axis. These localized factors will define the future anterior-posterior (AP) and dorsal-ventral (DV) axes of the embryo. Furthermore, AV polarity confines germ cell determinants to the vegetal pole, from where they redistribute to the cleavage furrows of the 2- and 4-cell stage embryo, ultimately specifying the primordial germ cells (PGCs). The sperm entry region during fertilization is also defined by the AV axis. In frogs and fish, sperm enters through the animal pole, similar to the mouse where it enters predominantly in the animal half. Thus, AV polarity establishment and RNA localization are involved in all the major events of early embryonic development. In this chapter, we will review the RNA localization mechanisms in vertebrate oocytes that are key to embryonic patterning, referring to some of the groundbreaking studies in frog oocytes and incorporating the current genetic evidence from the zebrafish.

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References

  • Albamonte MI, Albamonte MS, Stella I, Zuccardi L, Vitullo AD (2013) The infant and pubertal human ovary: Balbiani’s body-associated VASA expression, immunohistochemical detection of apoptosis-related BCL2 and BAX proteins, and DNA fragmentation. Hum Reprod 28:698–706

    Article  CAS  PubMed  Google Scholar 

  • Alves-Silva J, Sanchez-Soriano N, Beaven R, Klein M, Parkin J, Millard TH, Bellen HJ, Venken KJ, Ballestrem C, Kammerer RA et al (2012) Spectraplakins promote microtubule-mediated axonal growth by functioning as structural microtubule-associated proteins and EB1-dependent + TIPs (tip interacting proteins). J Neurosci 32:9143–9158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amanze D, Iyengar A (1990) The micropyle: a sperm guidance system in teleost fertilization. Development 109:495–500

    CAS  PubMed  Google Scholar 

  • Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC (2008) Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A 105:14976–14980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Applewhite DA, Grode KD, Keller D, Zadeh AD, Slep KC, Rogers SL (2010) The spectraplakin Short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol Biol Cell 21:1714–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bally-Cuif L, Schatz WJ, Ho RK (1998) Characterization of the zebrafish Orb/CPEB-related RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech Dev 77:31–47

    Article  CAS  PubMed  Google Scholar 

  • Barton BR, Hertig AT (1972) Ultrastructure of annulate lamellae in primary oocytes of chimpanzees (Pan troglodytes). Biol Reprod 6:98–108

    Article  CAS  PubMed  Google Scholar 

  • Bateman MJ, Cornell R, d'Alencon C, Sandra A (2004) Expression of the zebrafish Staufen gene in the embryo and adult. Gene Expr Patterns 5:273–278

    Article  CAS  PubMed  Google Scholar 

  • Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445

    Article  CAS  PubMed  Google Scholar 

  • Betley JN, Frith MC, Graber JH, Choo S, Deshler JO (2002) A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 12:1756–1761

    Article  CAS  PubMed  Google Scholar 

  • Bontems F, Stein A, Marlow F, Lyautey J, Gupta T, Mullins MC, Dosch R (2009) Bucky ball organizes germ plasm assembly in zebrafish. Curr Biol 19:414–422

    Article  CAS  PubMed  Google Scholar 

  • Bottenberg W, Sanchez-Soriano N, Alves-Silva J, Hahn I, Mende M, Prokop A (2009) Context-specific requirements of functional domains of the Spectraplakin Short stop in vivo. Mech Dev 126:489–502

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Koopman P (2007) Retinoic acid, meiosis and germ cell fate in mammals. Development 134:3401–3411

    Article  CAS  PubMed  Google Scholar 

  • Braat AK, Zandbergen T, van de Water S, Goos HJ, Zivkovic D (1999) Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dyn 216:153–167

    Article  CAS  PubMed  Google Scholar 

  • Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Julicher F, Hyman AA (2009a) Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–1732

    Article  CAS  PubMed  Google Scholar 

  • Brangwynne CP, Koenderink GH, MacKintosh FC, Weitz DA (2009b) Intracellular transport by active diffusion. Trends Cell Biol 19:423–427

    Article  CAS  PubMed  Google Scholar 

  • Brendza RP, Serbus LR, Duffy JB, Saxton WM (2000) A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289:2120–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brendza RP, Serbus LR, Saxton WM, Duffy JB (2002) Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes. Curr Biol 12:1541–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruce AE, Howley C, Zhou Y, Vickers SL, Silver LM, King ML, Ho RK (2003) The maternally expressed zebrafish T-box gene eomesodermin regulates organizer formation. Development 130:5503–5517

    Article  CAS  PubMed  Google Scholar 

  • Bubunenko M, Kress TL, Vempati UD, Mowry KL, King ML (2002) A consensus RNA signal that directs germ layer determinants to the vegetal cortex of Xenopus oocytes. Dev Biol 248:82–92

    Article  CAS  PubMed  Google Scholar 

  • Campbell PD, Chao JA, Singer RH, Marlow FL (2015a) Dynamic visualization of transcription and RNA subcellular localization in zebrafish. Development 142:1368–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell PD, Heim AE, Smith MZ, Marlow FL (2015b) Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis. Development 142:2996–3008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson JL, Bakst MR, Ottinger MA (1996) Developmental stages of primary oocytes in turkeys. Poult Sci 75:1569–1578

    Article  CAS  PubMed  Google Scholar 

  • Cha SW, Tadjuidje E, Tao Q, Wylie C, Heasman J (2008) Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. Development 135:3719–3729

    Article  CAS  PubMed  Google Scholar 

  • Cha SW, Tadjuidje E, White J, Wells J, Mayhew C, Wylie C, Heasman J (2009) Wnt11/5a complex formation caused by tyrosine sulfation increases canonical signaling activity. Curr Biol 19:1573–1580

    Article  CAS  PubMed  Google Scholar 

  • Chang P, Torres J, Lewis RA, Mowry KL, Houliston E, King ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15:4669–4681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cherr GN, Clark WH Jr (1985) An egg envelope component induces the acrosome reaction in sturgeon sperm. J Exp Zool 234:75–85

    Article  CAS  PubMed  Google Scholar 

  • Cherr GN, Yanagimachi R (2014) The fish egg’s micropyle and sperm attraction. Mol Reprod Dev 81:1063

    Article  PubMed  Google Scholar 

  • Choo S, Heinrich B, Betley JN, Chen Z, Deshler JO (2005) Evidence for common machinery utilized by the early and late RNA localization pathways in Xenopus oocytes. Dev Biol 278:103–117

    Article  CAS  PubMed  Google Scholar 

  • Claussen M, Horvay K, Pieler T (2004) Evidence for overlapping, but not identical, protein machineries operating in vegetal RNA localization along early and late pathways in Xenopus oocytes. Development 131:4263–4273

    Article  CAS  PubMed  Google Scholar 

  • Claussen M, Pieler T (2004) Xvelo1 uses a novel 75-nucleotide signal sequence that drives vegetal localization along the late pathway in Xenopus oocytes. Dev Biol 266:270–284

    Article  CAS  PubMed  Google Scholar 

  • Claussen M, Tarbashevich K, Pieler T (2011) Functional dissection of the RNA signal sequence responsible for vegetal localization of XGrip2.1 mRNA in Xenopus oocytes. RNA Biol 8:873–882

    Article  CAS  PubMed  Google Scholar 

  • Clements D, Friday RV, Woodland HR (1999) Mode of action of VegT in mesoderm and endoderm formation. Development 126:4903–4911

    CAS  PubMed  Google Scholar 

  • Colozza G, De Robertis EM (2014) Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus. Differentiation 88:17–26

    Article  CAS  PubMed  Google Scholar 

  • Cote CA, Gautreau D, Denegre JM, Kress TL, Terry NA, Mowry KL (1999) A Xenopus protein related to hnRNP I has a role in cytoplasmic RNA localization. Mol Cell 4:431–437

    Article  CAS  PubMed  Google Scholar 

  • Cox RT, Spradling AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130:1579–1590

    Article  CAS  PubMed  Google Scholar 

  • Cuykendall TN, Houston DW (2010) Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev Dyn 239:1838–1848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Robertis EM, Larrain J, Oelgeschlager M, Wessely O (2000) The establishment of Spemann’s organizer and patterning of the vertebrate embryo. Nat Rev Genet 1:171–181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deshler JO, Highett MI, Abramson T, Schnapp BJ (1998) A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol 8:489–496

    Article  CAS  PubMed  Google Scholar 

  • Deshler JO, Highett MI, Schnapp BJ (1997) Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276:1128–1131

    Article  CAS  PubMed  Google Scholar 

  • Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12:863–872

    Article  CAS  PubMed  Google Scholar 

  • Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC (2004) Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell 6:771–780

    Article  CAS  PubMed  Google Scholar 

  • Du S, Draper BW, Mione M, Moens CB, Bruce A (2012) Differential regulation of epiboly initiation and progression by zebrafish Eomesodermin A. Dev Biol 362:11–23

    Article  CAS  PubMed  Google Scholar 

  • Dumont JN (1978) Oogenesis in Xenopus laevis (Daudin): VI. The route of injected tracer transport in the follicle and developing oocyte. J Exp Zool 204:193–217

    Article  CAS  PubMed  Google Scholar 

  • Elkouby YM, Jamieson-Lucy A, Mullins MC (2016) Oocyte polarization is coupled to the chromosomal bouquet, a conserved polarized nuclear configuration in meiosis. PLoS Biol 14:e1002335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ephrussi A, Dickinson LK, Lehmann R (1991) Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50

    Article  CAS  PubMed  Google Scholar 

  • Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387–392

    Article  CAS  PubMed  Google Scholar 

  • Erter CE, Wilm TP, Basler N, Wright CV, Solnica-Krezel L (2001) Wnt8 is required in lateral mesendodermal precursors for neural posteriorization in vivo. Development 128:3571–3583

    CAS  PubMed  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  PubMed  Google Scholar 

  • Fan X, Hagos EG, Xu B, Sias C, Kawakami K, Burdine RD, Dougan ST (2007) Nodal signals mediate interactions between the extra-embryonic and embryonic tissues in zebrafish. Dev Biol 310:363–378

    Article  CAS  PubMed  Google Scholar 

  • Findley SD, Tamanaha M, Clegg NJ, Ruohola-Baker H (2003) Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130:859–871

    Article  CAS  PubMed  Google Scholar 

  • Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13:1159–1168

    Article  CAS  PubMed  Google Scholar 

  • Forristall C, Pondel M, Chen L, King ML (1995) Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development 121:201–208

    CAS  PubMed  Google Scholar 

  • Frey S, Richter RP, Gorlich D (2006) FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314:815–817

    Article  CAS  PubMed  Google Scholar 

  • Gagnon JA, Mowry KL (2010) Visualizing RNA localization in Xenopus oocytes. J Vis Exp 35:e1704

    Google Scholar 

  • Gard DL (1991) Organization, nucleation, and acetylation of microtubules in Xenopus laevis oocytes: a study by confocal immunofluorescence microscopy. Dev Biol 143:346–362

    Article  CAS  PubMed  Google Scholar 

  • Gard DL (1992) Microtubule organization during maturation of Xenopus oocytes: assembly and rotation of the meiotic spindles. Dev Biol 151:516–530

    Article  CAS  PubMed  Google Scholar 

  • Gard DL (1999) Confocal microscopy and 3-D reconstruction of the cytoskeleton of Xenopus oocytes. Microsc Res Tech 44:388–414

    Article  CAS  PubMed  Google Scholar 

  • Gard DL, Cha BJ, King E (1997) The organization and animal-vegetal asymmetry of cytokeratin filaments in stage VI Xenopus oocytes is dependent upon F-actin and microtubules. Dev Biol 184:95–114

    Article  CAS  PubMed  Google Scholar 

  • Gard DL, Cha BJ, Schroeder MM (1995) Confocal immunofluorescence microscopy of microtubules, microtubule-associated proteins, and microtubule-organizing centers during amphibian oogenesis and early development. Curr Top Dev Biol 31:383–431

    Article  CAS  PubMed  Google Scholar 

  • Ge X, Grotjahn D, Welch E, Lyman-Gingerich J, Holguin C, Dimitrova E, Abrams EW, Gupta T, Marlow FL, Yabe T et al (2014) Hecate/Grip2a acts to reorganize the cytoskeleton in the symmetry-breaking event of embryonic axis induction. PLoS Genet 10:e1004422

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghosh S, Marchand V, Gaspar I, Ephrussi A (2012) Control of RNP motility and localization by a splicing-dependent structure in oskar mRNA. Nat Struct Mol Biol 19:441–449

    Article  CAS  PubMed  Google Scholar 

  • Glotzer JB, Saffrich R, Glotzer M, Ephrussi A (1997) Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Curr Biol 7:326–337

    Article  CAS  PubMed  Google Scholar 

  • Gore AV, Maegawa S, Cheong A, Gilligan PC, Weinberg ES, Sampath K (2005) The zebrafish dorsal axis is apparent at the four-cell stage. Nature 438:1030–1035

    Article  CAS  PubMed  Google Scholar 

  • Grey RD, Wolf DP, Hedrick JL (1974) Formation and structure of fertilization envelope in Xenopus laevis. Dev Biol 36:44–61

    Article  CAS  PubMed  Google Scholar 

  • Gupta T, Marlow FL, Ferriola D, Mackiewicz K, Dapprich J, Monos D, Mullins MC (2010) Microtubule actin crosslinking factor 1 regulates the Balbiani body and animal-vegetal polarity of the zebrafish oocyte. PLoS Genet 6:e1001073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han TW, Kato M, Xie S, Wu LC, Mirzaei H, Pei J, Chen M, Xie Y, Allen J, Xiao G et al (2012) Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149:768–779

    Article  CAS  PubMed  Google Scholar 

  • Hart NH, Becker KA, Wolenski JS (1992) The sperm entry site during fertilization of the zebrafish egg: localization of actin. Mol Reprod Dev 32:217–228

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto Y, Maegawa S, Nagai T, Yamaha E, Suzuki H, Yasuda K, Inoue K (2004) Localized maternal factors are required for zebrafish germ cell formation. Dev Biol 268:152–161

    Article  CAS  PubMed  Google Scholar 

  • Havin L, Git A, Elisha Z, Oberman F, Yaniv K, Schwartz SP, Standart N, Yisraeli JK (1998) RNA-binding protein conserved in both microtubule- and microfilament-based RNA localization. Genes Dev 12:1593–1598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heasman J (2006) Maternal determinants of embryonic cell fate. Semin Cell Dev Biol 17:93–98

    Article  CAS  PubMed  Google Scholar 

  • Heasman J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev Biol 105:458–469

    Article  CAS  PubMed  Google Scholar 

  • Heim AE, Hartung O, Rothhamel S, Ferreira E, Jenny A, Marlow FL (2014) Oocyte polarity requires a Bucky ball-dependent feedback amplification loop. Development 141:842–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrich B, Deshler JO (2009) RNA localization to the Balbiani body in Xenopus oocytes is regulated by the energy state of the cell and is facilitated by kinesin II. RNA 15:524–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertig AT (1968) The primary human oocyte: some observations on the fine structure of Balbiani’s vitelline body and the origin of the annulate lamellae. Am J Anat 122:107–137

    Article  CAS  PubMed  Google Scholar 

  • Hiiragi T, Solter D (2004) First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430:360–364

    Article  CAS  PubMed  Google Scholar 

  • Hong SK, Jang MK, Brown JL, McBride AA, Feldman B (2011) Embryonic mesoderm and endoderm induction requires the actions of non-embryonic Nodal-related ligands and Mxtx2. Development 138:787–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houston DW (2013) Regulation of cell polarity and RNA localization in vertebrate oocytes. Int Rev Cell Mol Biol 306:127–185

    Article  CAS  PubMed  Google Scholar 

  • Houston DW, King ML (2000) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127:447–456

    CAS  PubMed  Google Scholar 

  • Houston DW, Zhang J, Maines JZ, Wasserman SA, King ML (1998) A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development 125:171–180

    CAS  PubMed  Google Scholar 

  • Houwing S, Berezikov E, Ketting RF (2008) Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J 27:2702–2711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB et al (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129:69–82

    Article  CAS  PubMed  Google Scholar 

  • Howley C, Ho RK (2000) mRNA localization patterns in zebrafish oocytes. Mech Dev 92:305–309

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Wang HL, Qi ST, Wang ZB, Tong JS, Zhang QH, Ouyang YC, Hou Y, Schatten H, Qi ZQ et al (2011) DYNLT3 is required for chromosome alignment during mouse oocyte meiotic maturation. Reprod Sci 18:983–989

    Article  CAS  PubMed  Google Scholar 

  • Hulsmann BB, Labokha AA, Gorlich D (2012) The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150:738–751

    Article  PubMed  CAS  Google Scholar 

  • Ikenishi K, Kotani M, Tanabe K (1974) Ultrastructural changes associated with UV irradiation in the “germinal plasm” of Xenopus laevis. Dev Biol 36:155–168

    Article  CAS  PubMed  Google Scholar 

  • Jaglarz MK, Nowak Z, Bilinski SM (2003) The Balbiani body and generation of early asymmetry in the oocyte of a tiger beetle. Differentiation 71:142–151

    Article  PubMed  Google Scholar 

  • Jedrzejowska I, Kubrakiewicz J (2007) The Balbiani body in the oocytes of a common cellar spider, Pholcus phalangioides (Araneae: Pholcidae). Arthropod Struct Dev 36:317–326

    Article  PubMed  Google Scholar 

  • Jenny A, Hachet O, Zavorszky P, Cyrklaff A, Weston MD, Johnston DS, Erdelyi M, Ephrussi A (2006) A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 133:2827–2833

    Article  CAS  PubMed  Google Scholar 

  • Juliano C, Wang J, Lin H (2011) Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet 45:447–469

    Article  CAS  PubMed  Google Scholar 

  • Kamminga LM, Luteijn MJ, den Broeder MJ, Redl S, Kaaij LJ, Roovers EF, Ladurner P, Berezikov E, Ketting RF (2010) Hen1 is required for oocyte development and piRNA stability in zebrafish. EMBO J 29:3688–3700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaneshiro K, Miyauchi M, Tanigawa Y, Ikenishi K, Komiya T (2007) The mRNA coding for Xenopus glutamate receptor interacting protein 2 (XGRIP2) is maternally transcribed, transported through the late pathway and localized to the germ plasm. Biochem Biophys Res Commun 355:902–906

    Article  CAS  PubMed  Google Scholar 

  • Karakesisoglou I, Yang Y, Fuchs E (2000) An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol 149:195–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimelman D (2006) Mesoderm induction: from caps to chips. Nat Rev Genet 7:360–372

    Article  CAS  PubMed  Google Scholar 

  • King ML, Messitt TJ, Mowry KL (2005) Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. Biol Cell 97:19–33

    Article  CAS  PubMed  Google Scholar 

  • Kirilenko P, Weierud FK, Zorn AM, Woodland HR (2008) The efficiency of Xenopus primordial germ cell migration depends on the germplasm mRNA encoding the PDZ domain protein Grip2. Differentiation 76:392–403

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Chan AP, Allen LH, Zearfoss NR, Etkin LD (2001) RNA localization and germ cell determination in Xenopus. Int Rev Cytol 203:63–91

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004a) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266:43–61

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Etkin LD (2004b) The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59:1–36

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287–297

    CAS  PubMed  Google Scholar 

  • Kloc M, Larabell C, Chan AP, Etkin LD (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75:81–93

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Larabell C, Etkin LD (1996) Elaboration of the messenger transport organizer pathway for localization of RNA to the vegetal cortex of Xenopus oocytes. Dev Biol 180:119–130

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108:533–544

    Article  CAS  PubMed  Google Scholar 

  • Knaut H, Pelegri F, Bohmann K, Schwarz H, Nusslein-Volhard C (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J Cell Biol 149:875–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Amikura R, Okada M (1994) Localization of mitochondrial large rRNA in germinal granules and the consequent segregation of germ line. Int J Dev Biol 38:193–199

    CAS  PubMed  Google Scholar 

  • Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E (2003) ACF7: an essential integrator of microtubule dynamics. Cell 115:343–354

    Article  CAS  PubMed  Google Scholar 

  • Kondo T, Yanagawa T, Yoshida N, Yamashita M (1997) Introduction of cyclin B induces activation of the maturation-promoting factor and breakdown of germinal vesicle in growing zebrafish oocytes unresponsive to the maturation-inducing hormone. Dev Biol 190:142–152

    Article  CAS  PubMed  Google Scholar 

  • Kosaka K, Kawakami K, Sakamoto H, Inoue K (2007) Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech Dev 124:279–289

    Article  CAS  PubMed  Google Scholar 

  • Kotani T, Yasuda K, Ota R, Yamashita M (2013) Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules. J Cell Biol 202:1041–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koubova J, Hu YC, Bhattacharyya T, Soh YQ, Gill ME, Goodheart ML, Hogarth CA, Griswold MD, Page DC (2014) Retinoic acid activates two pathways required for meiosis in mice. PLoS Genet 10:e1004541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kress TL, Yoon YJ, Mowry KL (2004) Nuclear RNP complex assembly initiates cytoplasmic RNA localization. J Cell Biol 165:203–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku HY, Lin H (2014) PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression. Nat Sci Rev 1:205–218

    Article  Google Scholar 

  • Ku M, Melton DA (1993) Xwnt-11: a maternally expressed Xenopus wnt gene. Development 119:1161–1173

    CAS  PubMed  Google Scholar 

  • Kwon S, Abramson T, Munro TP, John CM, Kohrmann M, Schnapp BJ (2002) UUCAC- and vera-dependent localization of VegT RNA in Xenopus oocytes. Curr Biol 12:558–564

    Article  CAS  PubMed  Google Scholar 

  • Langdon YG, Mullins MC (2011) Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annu Rev Genet 45:357–377

    Article  CAS  PubMed  Google Scholar 

  • Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, Korving JP, Hogan BL (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lekven AC, Thorpe CJ, Waxman JS, Moon RT (2001) Zebrafish wnt8 encodes two wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning. Dev Cell 1:103–114

    Article  CAS  PubMed  Google Scholar 

  • Lenhart KF, DiNardo S (2015) Somatic cell encystment promotes abscission in germline stem cells following a regulated block in cytokinesis. Dev Cell 34:192–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leu DH, Draper BW (2010) The ziwi promoter drives germline-specific gene expression in zebrafish. Dev Dyn 239:2714–2721

    Article  CAS  PubMed  Google Scholar 

  • Lewis RA, Kress TL, Cote CA, Gautreau D, Rokop ME, Mowry KL (2004) Conserved and clustered RNA recognition sequences are a critical feature of signals directing RNA localization in Xenopus oocytes. Mech Dev 121:101–109

    Article  CAS  PubMed  Google Scholar 

  • Lim S, Wang Y, Yu X, Huang Y, Featherstone MS, Sampath K (2013) A simple strategy for heritable chromosomal deletions in zebrafish via the combinatorial action of targeting nucleases. Genome Biol 14:R69

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin CM, Chen HJ, Leung CL, Parry DA, Liem RK (2005) Microtubule actin crosslinking factor 1b: a novel plakin that localizes to the Golgi complex. J Cell Sci 118:3727–3738

    Article  CAS  PubMed  Google Scholar 

  • Link J, Leubner M, Schmitt J, Gob E, Benavente R, Jeang KT, Xu R, Alsheimer M (2014) Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function. PLoS Genet 10:e1004099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu FI, Thisse C, Thisse B (2011) Identification and mechanism of regulation of the zebrafish dorsal determinant. Proc Natl Acad Sci U S A 108:15876–15880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, Zhu H, Han DY, Harris RA, Coarfa C, Gunaratne PH et al (2009) GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet 5:e1000635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Markussen FH, Michon AM, Breitwieser W, Ephrussi A (1995) Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723–3732

    CAS  PubMed  Google Scholar 

  • Marlow FL, Mullins MC (2008) Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev Biol 321:40–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masui Y (1972) Hormonal and cytoplasmic control of the maturation of frog oocytes. Sov J Dev Biol 3:484–495

    CAS  PubMed  Google Scholar 

  • Mei W, Lee KW, Marlow FL, Miller AL, Mullins MC (2009) hnRNP I is required to generate the Ca2+ signal that causes egg activation in zebrafish. Development 136:3007–3017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melton DA (1987) Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328:80–82

    Article  CAS  PubMed  Google Scholar 

  • Mendez R, Richter JD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2:521–529

    Article  CAS  PubMed  Google Scholar 

  • Messitt TJ, Gagnon JA, Kreiling JA, Pratt CA, Yoon YJ, Mowry KL (2008) Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. Dev Cell 15:426–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Micklem DR, Adams J, Grunert S, St Johnston D (2000) Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J 19:1366–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morisawa S (1999) Acrosome reaction in spermatozoa of the hagfish Eptatretus burgeri (Agnatha). Dev Growth Differ 41:109–112

    Article  CAS  PubMed  Google Scholar 

  • Morisawa S, Cherr GN (2002) Acrosome reaction in spermatozoa from hagfish (Agnatha) Eptatretus burgeri and Eptatretus stouti: acrosomal exocytosis and identification of filamentous actin. Dev Growth Differ 44:337–344

    Article  PubMed  Google Scholar 

  • Mosquera L, Forristall C, Zhou Y, King ML (1993) A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain. Development 117:377–386

    CAS  PubMed  Google Scholar 

  • Motosugi N, Dietrich JE, Polanski Z, Solter D, Hiiragi T (2006) Space asymmetry directs preferential sperm entry in the absence of polarity in the mouse oocyte. PLoS Biol 4:e135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mowry KL, Cote CA (1999) RNA sorting in Xenopus oocytes and embryos. FASEB J 13:435–445

    CAS  PubMed  Google Scholar 

  • Mowry KL, Melton DA (1992) Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. Science 255:991–994

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50(Suppl 1):S195–S219

    Article  CAS  PubMed  Google Scholar 

  • Nakahata S, Katsu Y, Mita K, Inoue K, Nagahama Y, Yamashita M (2001) Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J Biol Chem 276:20945–20953

    Article  CAS  PubMed  Google Scholar 

  • Nijjar S, Woodland HR (2013) Protein interactions in Xenopus germ plasm RNP particles. PLoS One 8:e80077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nojima H, Rothhamel S, Shimizu T, Kim CH, Yonemura S, Marlow FL, Hibi M (2010) Syntabulin, a motor protein linker, controls dorsal determination. Development 137:923–933

    Article  CAS  PubMed  Google Scholar 

  • Nojima H, Shimizu T, Kim CH, Yabe T, Bae YK, Muraoka O, Hirata T, Chitnis A, Hirano T, Hibi M (2004) Genetic evidence for involvement of maternally derived Wnt canonical signaling in dorsal determination in zebrafish. Mech Dev 121:371–386

    Article  CAS  PubMed  Google Scholar 

  • Ober EA, Field HA, Stainier DY (2003) From endoderm formation to liver and pancreas development in zebrafish. Mech Dev 120:5–18

    Article  CAS  PubMed  Google Scholar 

  • Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9:257–262

    Article  CAS  PubMed  Google Scholar 

  • Pepling ME, Wilhelm JE, O'Hara AL, Gephardt GW, Spradling AC (2007) Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc Natl Acad Sci U S A 104:187–192

    Article  CAS  PubMed  Google Scholar 

  • Piotrowska K, Zernicka-Goetz M (2001) Role for sperm in spatial patterning of the early mouse embryo. Nature 409:517–521

    Article  CAS  PubMed  Google Scholar 

  • Pique M, Lopez JM, Foissac S, Guigo R, Mendez R (2008) A combinatorial code for CPE-mediated translational control. Cell 132:434–448

    Article  CAS  PubMed  Google Scholar 

  • Ramasamy S, Wang H, Quach HN, Sampath K (2006) Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. Dev Biol 292:393–406

    Article  CAS  PubMed  Google Scholar 

  • Rebagliati MR, Weeks DL, Harvey RP, Melton DA (1985) Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell 42:769–777

    Article  CAS  PubMed  Google Scholar 

  • Riemer S, Bontems F, Krishnakumar P, Gomann J, Dosch R (2015) A functional Bucky ball-GFP transgene visualizes germ plasm in living zebrafish. Gene Expr Patterns 18:44–52

    Article  CAS  PubMed  Google Scholar 

  • Rodler D, Sinowatz F (2013) Expression of intermediate filaments in the Balbiani body and ovarian follicular wall of the Japanese quail (Coturnix japonica). Cells Tissues Organs 197:298–311

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Mari A, Canestro C, BreMiller RA, Catchen JM, Yan YL, Postlethwait JH (2013) Retinoic acid metabolic genes, meiosis, and gonadal sex differentiation in zebrafish. PLoS One 8:e73951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roper K, Brown NH (2004) A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol 14:99–110

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Soriano N, Travis M, Dajas-Bailador F, Goncalves-Pimentel C, Whitmarsh AJ, Prokop A (2009) Mouse ACF7 and drosophila short stop modulate filopodia formation and microtubule organisation during neuronal growth. J Cell Sci 122:2534–2542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, Kasad RA, Dernburg AF (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139:907–919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621–627

    Article  CAS  PubMed  Google Scholar 

  • Schier AF (2003) Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19:589–621

    Article  CAS  PubMed  Google Scholar 

  • Schier AF, Talbot WS (2005) Molecular genetics of axis formation in zebrafish. Annu Rev Genet 39:561–613

    Article  CAS  PubMed  Google Scholar 

  • Schnapp BJ, Arn EA, Deshler JO, Highett MI (1997) RNA localization in Xenopus oocytes. Semin Cell Dev Biol 8:529–540

    Article  CAS  PubMed  Google Scholar 

  • Schroeder KE, Condic ML, Eisenberg LM, Yost HJ (1999) Spatially regulated translation in embryos: asymmetric expression of maternal Wnt-11 along the dorsal-ventral axis in Xenopus. Dev Biol 214:288–297

    Article  CAS  PubMed  Google Scholar 

  • Selman K, Wallace RA, Sarka A, Qi XP (1993) Stages of oocyte development in the zebrafish, brachydanio-rerio. J Morphol 218:203–224

    Article  Google Scholar 

  • Shibuya H, Ishiguro K, Watanabe Y (2014a) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16:145–156

    Article  CAS  PubMed  Google Scholar 

  • Shibuya H, Morimoto A, Watanabe Y (2014b) The dissection of meiotic chromosome movement in mice using an in vivo electroporation technique. PLoS Genet 10:e1004821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith LD (1966) The role of a “germinal plasm” in the formation of primordial germ cells in Rana pipiens. Dev Biol 14:330–347

    Article  CAS  PubMed  Google Scholar 

  • Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28:687–717

    Article  CAS  PubMed  Google Scholar 

  • Song HW, Cauffman K, Chan AP, Zhou Y, King ML, Etkin LD, Kloc M (2007) Hermes RNA-binding protein targets RNAs-encoding proteins involved in meiotic maturation, early cleavage, and germline development. Differentiation 75:519–528

    Article  CAS  PubMed  Google Scholar 

  • Sonnenberg A, Liem RK (2007) Plakins in development and disease. Exp Cell Res 313:2189–2203

    Article  CAS  PubMed  Google Scholar 

  • Staudt N, Molitor A, Somogyi K, Mata J, Curado S, Eulenberg K, Meise M, Siegmund T, Hader T, Hilfiker A et al (2005) Gain-of-function screen for genes that affect Drosophila muscle pattern formation. PLoS Genet 1:e55

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Strasser MJ, Mackenzie NC, Dumstrei K, Nakkrasae LI, Stebler J, Raz E (2008) Control over the morphology and segregation of Zebrafish germ cell granules during embryonic development. BMC Dev Biol 8:58

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tao Q, Yokota C, Puck H, Kofron M, Birsoy B, Yan D, Asashima M, Wylie CC, Lin X, Heasman J (2005) Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120:857–871

    Article  CAS  PubMed  Google Scholar 

  • Tarbashevich K, Koebernick K, Pieler T (2007) XGRIP2.1 is encoded by a vegetally localizing, maternal mRNA and functions in germ cell development and anteroposterior PGC positioning in Xenopus laevis. Dev Biol 311:554–565

    Article  CAS  PubMed  Google Scholar 

  • Toretsky JA, Wright PE (2014) Assemblages: functional units formed by cellular phase separation. J Cell Biol 206:579–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ukeshima A, Fujimoto T (1991) A fine morphological study of germ cells in asymmetrically developing right and left ovaries of the chick. Anat Rec 230:378–386

    Article  CAS  PubMed  Google Scholar 

  • van Boxtel AL, Chesebro JE, Heliot C, Ramel MC, Stone RK, Hill CS (2015) A temporal window for signal activation dictates the dimensions of a nodal signaling domain. Dev Cell 35:175–185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Varga M, Maegawa S, Bellipanni G, Weinberg ES (2007) Chordin expression, mediated by Nodal and FGF signaling, is restricted by redundant function of two beta-catenins in the zebrafish embryo. Mech Dev 124:775–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner DS, Dosch R, Mintzer KA, Wiemelt AP, Mullins MC (2004) Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev Cell 6:781–790

    Article  CAS  PubMed  Google Scholar 

  • Wang JT, Smith J, Chen BC, Schmidt H, Rasoloson D, Paix A, Lambrus BG, Calidas D, Betzig E, Seydoux G (2014) Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically disordered proteins in C. elegans. Elife 3:e04591

    PubMed  PubMed Central  Google Scholar 

  • Weakley BS (1967) “Balbiani’s body” in the oocyte of the golden hamster. Z Zellforsch Mikrosk Anat 83:583–588

    Article  CAS  PubMed  Google Scholar 

  • Weeks DL, Melton DA (1987) A maternal mRNA localized to the animal pole of Xenopus eggs encodes a subunit of mitochondrial ATPase. Proc Natl Acad Sci U S A 84:2798–2802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitington PM, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33:57–74

    CAS  PubMed  Google Scholar 

  • Wilk K, Bilinski S, Dougherty MT, Kloc M (2005) Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. Int J Dev Biol 49:17–21

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Kodama A, Fuchs E (2008) ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135:137–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X, Shen QT, Oristian DS, Lu CP, Zheng Q, Wang HW, Fuchs E (2011) Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta. Cell 144:341–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xanthos JB, Kofron M, Wylie C, Heasman J (2001) Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128:167–180

    CAS  PubMed  Google Scholar 

  • Xiol J, Spinelli P, Laussmann MA, Homolka D, Yang Z, Cora E, Coute Y, Conn S, Kadlec J, Sachidanandam R et al (2014) RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 157:1698–1711

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Zhu G, Wang Y, Sun J, Liu X, Chen YG, Meng A (2014) Maternal Eomesodermin regulates zygotic nodal gene expression for mesendoderm induction in zebrafish embryos. J Mol Cell Biol 6:272–285

    Article  CAS  PubMed  Google Scholar 

  • Yan W, Ma L, Zilinski CA, Matzuk MM (2004) Identification and characterization of evolutionarily conserved pufferfish, zebrafish, and frog orthologs of GASZ. Biol Reprod 70:1619–1625

    Article  CAS  PubMed  Google Scholar 

  • Yano T, Lopez de Quinto S, Matsui Y, Shevchenko A, Shevchenko A, Ephrussi A (2004) Hrp48, a Drosophila hnRNPA/B homolog, binds and regulates translation of oskar mRNA. Dev Cell 6:637–648

    Article  CAS  PubMed  Google Scholar 

  • Yasuda K, Kotani T, Ota R, Yamashita M (2010) Transgenic zebrafish reveals novel mechanisms of translational control of cyclin B1 mRNA in oocytes. Dev Biol 348:76–86

    Article  CAS  PubMed  Google Scholar 

  • Yasuda K, Kotani T, Yamashita M (2013) A cis-acting element in the coding region of cyclin B1 mRNA couples subcellular localization to translational timing. Dev Biol 382:517–529

    Article  CAS  PubMed  Google Scholar 

  • Yisraeli JK, Melton DA (1988) The material mRNA Vg1 is correctly localized following injection into Xenopus oocytes. Nature 336:592–595

    Article  CAS  PubMed  Google Scholar 

  • Yisraeli JK, Sokol S, Melton DA (1989) The process of localizing a maternal messenger RNA in Xenopus oocytes. Development 107(Suppl):31–36

    CAS  PubMed  Google Scholar 

  • Yisraeli JK, Sokol S, Melton DA (1990) 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. Development 108:289–298

    CAS  PubMed  Google Scholar 

  • Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3165

    CAS  PubMed  Google Scholar 

  • Yoon YJ, Mowry KL (2004) Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin. Development 131:3035–3045

    Article  CAS  PubMed  Google Scholar 

  • Zearfoss NR, Chan AP, Wu CF, Kloc M, Etkin LD (2004) Hermes is a localized factor regulating cleavage of vegetal blastomeres in Xenopus laevis. Dev Biol 267:60–71

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, King ML (1996a) Localization of Xcat-2 RNA, a putative germ plasm component, to the mitochondrial cloud in Xenopus stage I oocytes. Development 122:2947–2953

    CAS  PubMed  Google Scholar 

  • Zhou Y, King ML (1996b) RNA transport to the vegetal cortex of Xenopus oocytes. Dev Biol 179:173–183

    Article  CAS  PubMed  Google Scholar 

  • Zust B, Dixon KE (1975) The effect of u.v. irradiation of the vegetal pole of Xenopus laevis eggs on the presumptive primordial germ cells. J Embryol Exp Morphol 34:209–220

    CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to acknowledge grants from the National Institutes of Health R01GM056326 and R01GM117981 to M.C.M. and “BECAS CHILE DE DOCTORADO EN EL EXTRANJERO” to M.E.A.

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  1. Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1152 BRBII/III, 421 Curie Boulevard, Philadelphia, PA, 19104-6058, USA

    Matias Escobar-Aguirre, Yaniv M. Elkouby & Mary C. Mullins

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  1. Matias Escobar-Aguirre
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  2. Yaniv M. Elkouby
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  3. Mary C. Mullins
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Correspondence to Mary C. Mullins .

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  1. Laboratory of Genetics, University of Wisconsin—Madison, Madison, Wisconsin, USA

    Francisco Pelegri

  2. Department of Integrative Biosciences, Oregon Health & Science University, Portland, Oregon, USA

    Michael Danilchik

  3. Department of Cell Biology, University of Virginia Health System, Charlottesville, Virginia, USA

    Ann Sutherland

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Escobar-Aguirre, M., Elkouby, Y.M., Mullins, M.C. (2017). Localization in Oogenesis of Maternal Regulators of Embryonic Development. In: Pelegri, F., Danilchik, M., Sutherland, A. (eds) Vertebrate Development. Advances in Experimental Medicine and Biology, vol 953. Springer, Cham. https://doi.org/10.1007/978-3-319-46095-6_5

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