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Localization in Oogenesis of Maternal Regulators of Embryonic Development

  • Matias Escobar-Aguirre
  • Yaniv M. Elkouby
  • Mary C. MullinsEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (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.

Keywords

Balbiani body Bucky ball Oocyte polarity Germplasm RNA localization Oogenesis Fertilization Cytoskeleton Axis formation Animal-vegetal axis 

Notes

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.

References

  1. 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 28:698–706PubMedCrossRefGoogle Scholar
  2. 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 32:9143–9158PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amanze D, Iyengar A (1990) The micropyle: a sperm guidance system in teleost fertilization. Development 109:495–500PubMedGoogle Scholar
  4. 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 105:14976–14980PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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 21:1714–1724PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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 77:31–47PubMedCrossRefGoogle Scholar
  7. Barton BR, Hertig AT (1972) Ultrastructure of annulate lamellae in primary oocytes of chimpanzees (Pan troglodytes). Biol Reprod 6:98–108PubMedCrossRefGoogle Scholar
  8. Bateman MJ, Cornell R, d'Alencon C, Sandra A (2004) Expression of the zebrafish Staufen gene in the embryo and adult. Gene Expr Patterns 5:273–278PubMedCrossRefGoogle Scholar
  9. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445PubMedCrossRefGoogle Scholar
  10. Betley JN, Frith MC, Graber JH, Choo S, Deshler JO (2002) A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 12:1756–1761PubMedCrossRefGoogle Scholar
  11. 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 19:414–422PubMedCrossRefGoogle Scholar
  12. 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 126:489–502PubMedCrossRefGoogle Scholar
  13. Bowles J, Koopman P (2007) Retinoic acid, meiosis and germ cell fate in mammals. Development 134:3401–3411PubMedCrossRefGoogle Scholar
  14. 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 216:153–167PubMedCrossRefGoogle Scholar
  15. 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 324:1729–1732PubMedCrossRefGoogle Scholar
  16. Brangwynne CP, Koenderink GH, MacKintosh FC, Weitz DA (2009b) Intracellular transport by active diffusion. Trends Cell Biol 19:423–427PubMedCrossRefGoogle Scholar
  17. 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 289:2120–2122PubMedPubMedCentralCrossRefGoogle Scholar
  18. 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 12:1541–1545PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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 130:5503–5517PubMedCrossRefGoogle Scholar
  20. 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 248:82–92PubMedCrossRefGoogle Scholar
  21. Campbell PD, Chao JA, Singer RH, Marlow FL (2015a) Dynamic visualization of transcription and RNA subcellular localization in zebrafish. Development 142:1368–1374PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 142:2996–3008PubMedPubMedCentralCrossRefGoogle Scholar
  23. Carlson JL, Bakst MR, Ottinger MA (1996) Developmental stages of primary oocytes in turkeys. Poult Sci 75:1569–1578PubMedCrossRefGoogle Scholar
  24. 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 135:3719–3729PubMedCrossRefGoogle Scholar
  25. 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 19:1573–1580PubMedCrossRefGoogle Scholar
  26. 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 15:4669–4681PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cherr GN, Clark WH Jr (1985) An egg envelope component induces the acrosome reaction in sturgeon sperm. J Exp Zool 234:75–85PubMedCrossRefGoogle Scholar
  28. Cherr GN, Yanagimachi R (2014) The fish egg’s micropyle and sperm attraction. Mol Reprod Dev 81:1063PubMedCrossRefGoogle Scholar
  29. 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 278:103–117PubMedCrossRefGoogle Scholar
  30. 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 131:4263–4273PubMedCrossRefGoogle Scholar
  31. 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 266:270–284PubMedCrossRefGoogle Scholar
  32. 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 8:873–882PubMedCrossRefGoogle Scholar
  33. Clements D, Friday RV, Woodland HR (1999) Mode of action of VegT in mesoderm and endoderm formation. Development 126:4903–4911PubMedGoogle Scholar
  34. Colozza G, De Robertis EM (2014) Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus. Differentiation 88:17–26PubMedCrossRefGoogle Scholar
  35. 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 4:431–437PubMedCrossRefGoogle Scholar
  36. Cox RT, Spradling AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130:1579–1590PubMedCrossRefGoogle Scholar
  37. Cuykendall TN, Houston DW (2010) Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev Dyn 239:1838–1848PubMedPubMedCentralCrossRefGoogle Scholar
  38. De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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 1:171–181PubMedPubMedCentralCrossRefGoogle Scholar
  40. Deshler JO, Highett MI, Abramson T, Schnapp BJ (1998) A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol 8:489–496PubMedCrossRefGoogle Scholar
  41. Deshler JO, Highett MI, Schnapp BJ (1997) Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276:1128–1131PubMedCrossRefGoogle Scholar
  42. 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 12:863–872PubMedCrossRefGoogle Scholar
  43. 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 6:771–780PubMedCrossRefGoogle Scholar
  44. Du S, Draper BW, Mione M, Moens CB, Bruce A (2012) Differential regulation of epiboly initiation and progression by zebrafish Eomesodermin A. Dev Biol 362:11–23PubMedCrossRefGoogle Scholar
  45. Dumont JN (1978) Oogenesis in Xenopus laevis (Daudin): VI. The route of injected tracer transport in the follicle and developing oocyte. J Exp Zool 204:193–217PubMedCrossRefGoogle Scholar
  46. 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:e1002335PubMedPubMedCentralCrossRefGoogle Scholar
  47. Ephrussi A, Dickinson LK, Lehmann R (1991) Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50PubMedCrossRefGoogle Scholar
  48. Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387–392PubMedCrossRefGoogle Scholar
  49. 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 128:3571–3583PubMedGoogle Scholar
  50. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884PubMedCrossRefGoogle Scholar
  51. 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 310:363–378PubMedCrossRefGoogle Scholar
  52. 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 130:859–871PubMedCrossRefGoogle Scholar
  53. Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13:1159–1168PubMedCrossRefGoogle Scholar
  54. 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 121:201–208PubMedGoogle Scholar
  55. Frey S, Richter RP, Gorlich D (2006) FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314:815–817PubMedCrossRefGoogle Scholar
  56. Gagnon JA, Mowry KL (2010) Visualizing RNA localization in Xenopus oocytes. J Vis Exp 35:e1704Google Scholar
  57. Gard DL (1991) Organization, nucleation, and acetylation of microtubules in Xenopus laevis oocytes: a study by confocal immunofluorescence microscopy. Dev Biol 143:346–362PubMedCrossRefGoogle Scholar
  58. Gard DL (1992) Microtubule organization during maturation of Xenopus oocytes: assembly and rotation of the meiotic spindles. Dev Biol 151:516–530PubMedCrossRefGoogle Scholar
  59. Gard DL (1999) Confocal microscopy and 3-D reconstruction of the cytoskeleton of Xenopus oocytes. Microsc Res Tech 44:388–414PubMedCrossRefGoogle Scholar
  60. 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 184:95–114PubMedCrossRefGoogle Scholar
  61. 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 31:383–431PubMedCrossRefGoogle Scholar
  62. 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:e1004422PubMedPubMedCentralCrossRefGoogle Scholar
  63. 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 19:441–449PubMedCrossRefGoogle Scholar
  64. Glotzer JB, Saffrich R, Glotzer M, Ephrussi A (1997) Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Curr Biol 7:326–337PubMedCrossRefGoogle Scholar
  65. 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 438:1030–1035PubMedCrossRefGoogle Scholar
  66. Grey RD, Wolf DP, Hedrick JL (1974) Formation and structure of fertilization envelope in Xenopus laevis. Dev Biol 36:44–61PubMedCrossRefGoogle Scholar
  67. 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:e1001073PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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 149:768–779PubMedCrossRefGoogle Scholar
  69. Hart NH, Becker KA, Wolenski JS (1992) The sperm entry site during fertilization of the zebrafish egg: localization of actin. Mol Reprod Dev 32:217–228PubMedCrossRefGoogle Scholar
  70. 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 268:152–161PubMedCrossRefGoogle Scholar
  71. 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 12:1593–1598PubMedPubMedCentralCrossRefGoogle Scholar
  72. Heasman J (2006) Maternal determinants of embryonic cell fate. Semin Cell Dev Biol 17:93–98PubMedCrossRefGoogle Scholar
  73. Heasman J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev Biol 105:458–469PubMedCrossRefGoogle Scholar
  74. Heim AE, Hartung O, Rothhamel S, Ferreira E, Jenny A, Marlow FL (2014) Oocyte polarity requires a Bucky ball-dependent feedback amplification loop. Development 141:842–854PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 15:524–536PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 122:107–137PubMedCrossRefGoogle Scholar
  77. 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 430:360–364PubMedCrossRefGoogle Scholar
  78. 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 138:787–795PubMedPubMedCentralCrossRefGoogle Scholar
  79. Houston DW (2013) Regulation of cell polarity and RNA localization in vertebrate oocytes. Int Rev Cell Mol Biol 306:127–185PubMedCrossRefGoogle Scholar
  80. 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 127:447–456PubMedGoogle Scholar
  81. 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 125:171–180PubMedGoogle Scholar
  82. Houwing S, Berezikov E, Ketting RF (2008) Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J 27:2702–2711PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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 129:69–82PubMedCrossRefGoogle Scholar
  84. Howley C, Ho RK (2000) mRNA localization patterns in zebrafish oocytes. Mech Dev 92:305–309PubMedCrossRefGoogle Scholar
  85. 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 18:983–989PubMedCrossRefGoogle Scholar
  86. Hulsmann BB, Labokha AA, Gorlich D (2012) The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150:738–751PubMedCrossRefGoogle Scholar
  87. Ikenishi K, Kotani M, Tanabe K (1974) Ultrastructural changes associated with UV irradiation in the “germinal plasm” of Xenopus laevis. Dev Biol 36:155–168PubMedCrossRefGoogle Scholar
  88. Jaglarz MK, Nowak Z, Bilinski SM (2003) The Balbiani body and generation of early asymmetry in the oocyte of a tiger beetle. Differentiation 71:142–151PubMedCrossRefGoogle Scholar
  89. Jedrzejowska I, Kubrakiewicz J (2007) The Balbiani body in the oocytes of a common cellar spider, Pholcus phalangioides (Araneae: Pholcidae). Arthropod Struct Dev 36:317–326PubMedCrossRefGoogle Scholar
  90. 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 133:2827–2833PubMedCrossRefGoogle Scholar
  91. 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 45:447–469PubMedCrossRefGoogle Scholar
  92. 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 29:3688–3700PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 355:902–906PubMedCrossRefGoogle Scholar
  94. Karakesisoglou I, Yang Y, Fuchs E (2000) An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol 149:195–208PubMedPubMedCentralCrossRefGoogle Scholar
  95. Kimelman D (2006) Mesoderm induction: from caps to chips. Nat Rev Genet 7:360–372PubMedCrossRefGoogle Scholar
  96. 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 97:19–33PubMedCrossRefGoogle Scholar
  97. 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 76:392–403PubMedCrossRefGoogle Scholar
  98. Kloc M, Bilinski S, Chan AP, Allen LH, Zearfoss NR, Etkin LD (2001) RNA localization and germ cell determination in Xenopus. Int Rev Cytol 203:63–91PubMedCrossRefGoogle Scholar
  99. Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004a) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266:43–61PubMedCrossRefGoogle Scholar
  100. Kloc M, Bilinski S, Etkin LD (2004b) The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59:1–36PubMedCrossRefGoogle Scholar
  101. Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287–297PubMedGoogle Scholar
  102. 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 75:81–93PubMedCrossRefGoogle Scholar
  103. 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 180:119–130PubMedCrossRefGoogle Scholar
  104. Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108:533–544PubMedCrossRefGoogle Scholar
  105. 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 149:875–888PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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 38:193–199PubMedGoogle Scholar
  107. Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E (2003) ACF7: an essential integrator of microtubule dynamics. Cell 115:343–354PubMedCrossRefGoogle Scholar
  108. 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 190:142–152PubMedCrossRefGoogle Scholar
  109. Kosaka K, Kawakami K, Sakamoto H, Inoue K (2007) Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech Dev 124:279–289PubMedCrossRefGoogle Scholar
  110. 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 202:1041–1055PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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:e1004541PubMedPubMedCentralCrossRefGoogle Scholar
  112. Kress TL, Yoon YJ, Mowry KL (2004) Nuclear RNP complex assembly initiates cytoplasmic RNA localization. J Cell Biol 165:203–211PubMedPubMedCentralCrossRefGoogle Scholar
  113. Ku HY, Lin H (2014) PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression. Nat Sci Rev 1:205–218CrossRefGoogle Scholar
  114. Ku M, Melton DA (1993) Xwnt-11: a maternally expressed Xenopus wnt gene. Development 119:1161–1173PubMedGoogle Scholar
  115. 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 12:558–564PubMedCrossRefGoogle Scholar
  116. Langdon YG, Mullins MC (2011) Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annu Rev Genet 45:357–377PubMedCrossRefGoogle Scholar
  117. 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 13:424–436PubMedPubMedCentralCrossRefGoogle Scholar
  118. 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 1:103–114PubMedCrossRefGoogle Scholar
  119. Lenhart KF, DiNardo S (2015) Somatic cell encystment promotes abscission in germline stem cells following a regulated block in cytokinesis. Dev Cell 34:192–205PubMedPubMedCentralCrossRefGoogle Scholar
  120. Leu DH, Draper BW (2010) The ziwi promoter drives germline-specific gene expression in zebrafish. Dev Dyn 239:2714–2721PubMedCrossRefGoogle Scholar
  121. 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 121:101–109PubMedCrossRefGoogle Scholar
  122. 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:R69PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 118:3727–3738PubMedCrossRefGoogle Scholar
  124. 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:e1004099PubMedPubMedCentralCrossRefGoogle Scholar
  125. Lu FI, Thisse C, Thisse B (2011) Identification and mechanism of regulation of the zebrafish dorsal determinant. Proc Natl Acad Sci U S A 108:15876–15880PubMedPubMedCentralCrossRefGoogle Scholar
  126. 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:e1000635PubMedPubMedCentralCrossRefGoogle Scholar
  127. Markussen FH, Michon AM, Breitwieser W, Ephrussi A (1995) Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723–3732PubMedGoogle Scholar
  128. 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 321:40–50PubMedPubMedCentralCrossRefGoogle Scholar
  129. Masui Y (1972) Hormonal and cytoplasmic control of the maturation of frog oocytes. Sov J Dev Biol 3:484–495PubMedGoogle Scholar
  130. 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 136:3007–3017PubMedPubMedCentralCrossRefGoogle Scholar
  131. Melton DA (1987) Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328:80–82PubMedCrossRefGoogle Scholar
  132. Mendez R, Richter JD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2:521–529PubMedCrossRefGoogle Scholar
  133. 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 15:426–436PubMedPubMedCentralCrossRefGoogle Scholar
  134. 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 19:1366–1377PubMedPubMedCentralCrossRefGoogle Scholar
  135. Morisawa S (1999) Acrosome reaction in spermatozoa of the hagfish Eptatretus burgeri (Agnatha). Dev Growth Differ 41:109–112PubMedCrossRefGoogle Scholar
  136. 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 44:337–344PubMedCrossRefGoogle Scholar
  137. 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 117:377–386PubMedGoogle Scholar
  138. 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:e135PubMedPubMedCentralCrossRefGoogle Scholar
  139. Mowry KL, Cote CA (1999) RNA sorting in Xenopus oocytes and embryos. FASEB J 13:435–445PubMedGoogle Scholar
  140. Mowry KL, Melton DA (1992) Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. Science 255:991–994PubMedCrossRefGoogle Scholar
  141. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50(Suppl 1):S195–S219PubMedCrossRefGoogle Scholar
  142. 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 276:20945–20953PubMedCrossRefGoogle Scholar
  143. Nijjar S, Woodland HR (2013) Protein interactions in Xenopus germ plasm RNP particles. PLoS One 8:e80077PubMedPubMedCentralCrossRefGoogle Scholar
  144. Nojima H, Rothhamel S, Shimizu T, Kim CH, Yonemura S, Marlow FL, Hibi M (2010) Syntabulin, a motor protein linker, controls dorsal determination. Development 137:923–933PubMedCrossRefGoogle Scholar
  145. 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 121:371–386PubMedCrossRefGoogle Scholar
  146. Ober EA, Field HA, Stainier DY (2003) From endoderm formation to liver and pancreas development in zebrafish. Mech Dev 120:5–18PubMedCrossRefGoogle Scholar
  147. Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9:257–262PubMedCrossRefGoogle Scholar
  148. 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 104:187–192PubMedCrossRefGoogle Scholar
  149. Piotrowska K, Zernicka-Goetz M (2001) Role for sperm in spatial patterning of the early mouse embryo. Nature 409:517–521PubMedCrossRefGoogle Scholar
  150. Pique M, Lopez JM, Foissac S, Guigo R, Mendez R (2008) A combinatorial code for CPE-mediated translational control. Cell 132:434–448PubMedCrossRefGoogle Scholar
  151. 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 292:393–406PubMedCrossRefGoogle Scholar
  152. Rebagliati MR, Weeks DL, Harvey RP, Melton DA (1985) Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell 42:769–777PubMedCrossRefGoogle Scholar
  153. 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 18:44–52PubMedCrossRefGoogle Scholar
  154. 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 197:298–311PubMedCrossRefGoogle Scholar
  155. 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:e73951PubMedPubMedCentralCrossRefGoogle Scholar
  156. Roper K, Brown NH (2004) A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol 14:99–110PubMedCrossRefGoogle Scholar
  157. 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 122:2534–2542PubMedPubMedCentralCrossRefGoogle Scholar
  158. 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 139:907–919PubMedPubMedCentralCrossRefGoogle Scholar
  159. Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621–627PubMedCrossRefGoogle Scholar
  160. Schier AF (2003) Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19:589–621PubMedCrossRefGoogle Scholar
  161. Schier AF, Talbot WS (2005) Molecular genetics of axis formation in zebrafish. Annu Rev Genet 39:561–613PubMedCrossRefGoogle Scholar
  162. Schnapp BJ, Arn EA, Deshler JO, Highett MI (1997) RNA localization in Xenopus oocytes. Semin Cell Dev Biol 8:529–540PubMedCrossRefGoogle Scholar
  163. 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 214:288–297PubMedCrossRefGoogle Scholar
  164. Selman K, Wallace RA, Sarka A, Qi XP (1993) Stages of oocyte development in the zebrafish, brachydanio-rerio. J Morphol 218:203–224CrossRefGoogle Scholar
  165. Shibuya H, Ishiguro K, Watanabe Y (2014a) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16:145–156PubMedCrossRefGoogle Scholar
  166. Shibuya H, Morimoto A, Watanabe Y (2014b) The dissection of meiotic chromosome movement in mice using an in vivo electroporation technique. PLoS Genet 10:e1004821PubMedPubMedCentralCrossRefGoogle Scholar
  167. Smith LD (1966) The role of a “germinal plasm” in the formation of primordial germ cells in Rana pipiens. Dev Biol 14:330–347PubMedCrossRefGoogle Scholar
  168. Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28:687–717PubMedCrossRefGoogle Scholar
  169. 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 75:519–528PubMedCrossRefGoogle Scholar
  170. Sonnenberg A, Liem RK (2007) Plakins in development and disease. Exp Cell Res 313:2189–2203PubMedCrossRefGoogle Scholar
  171. 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:e55PubMedPubMedCentralCrossRefGoogle Scholar
  172. 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 8:58PubMedPubMedCentralCrossRefGoogle Scholar
  173. 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 120:857–871PubMedCrossRefGoogle Scholar
  174. 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 311:554–565PubMedCrossRefGoogle Scholar
  175. Toretsky JA, Wright PE (2014) Assemblages: functional units formed by cellular phase separation. J Cell Biol 206:579–588PubMedPubMedCentralCrossRefGoogle Scholar
  176. Ukeshima A, Fujimoto T (1991) A fine morphological study of germ cells in asymmetrically developing right and left ovaries of the chick. Anat Rec 230:378–386PubMedCrossRefGoogle Scholar
  177. 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 35:175–185PubMedPubMedCentralCrossRefGoogle Scholar
  178. 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 124:775–791PubMedPubMedCentralCrossRefGoogle Scholar
  179. 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 6:781–790PubMedCrossRefGoogle Scholar
  180. 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:e04591PubMedPubMedCentralGoogle Scholar
  181. Weakley BS (1967) “Balbiani’s body” in the oocyte of the golden hamster. Z Zellforsch Mikrosk Anat 83:583–588PubMedCrossRefGoogle Scholar
  182. 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 84:2798–2802PubMedPubMedCentralCrossRefGoogle Scholar
  183. Whitington PM, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33:57–74PubMedGoogle Scholar
  184. 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 49:17–21PubMedCrossRefGoogle Scholar
  185. Wu X, Kodama A, Fuchs E (2008) ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135:137–148PubMedPubMedCentralCrossRefGoogle Scholar
  186. 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 144:341–352PubMedPubMedCentralCrossRefGoogle Scholar
  187. Xanthos JB, Kofron M, Wylie C, Heasman J (2001) Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128:167–180PubMedGoogle Scholar
  188. 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 157:1698–1711PubMedCrossRefGoogle Scholar
  189. 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 6:272–285PubMedCrossRefGoogle Scholar
  190. Yan W, Ma L, Zilinski CA, Matzuk MM (2004) Identification and characterization of evolutionarily conserved pufferfish, zebrafish, and frog orthologs of GASZ. Biol Reprod 70:1619–1625PubMedCrossRefGoogle Scholar
  191. 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 6:637–648PubMedCrossRefGoogle Scholar
  192. 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 348:76–86PubMedCrossRefGoogle Scholar
  193. 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 382:517–529PubMedCrossRefGoogle Scholar
  194. Yisraeli JK, Melton DA (1988) The material mRNA Vg1 is correctly localized following injection into Xenopus oocytes. Nature 336:592–595PubMedCrossRefGoogle Scholar
  195. Yisraeli JK, Sokol S, Melton DA (1989) The process of localizing a maternal messenger RNA in Xenopus oocytes. Development 107(Suppl):31–36PubMedGoogle Scholar
  196. 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 108:289–298PubMedGoogle Scholar
  197. 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 124:3157–3165PubMedGoogle Scholar
  198. Yoon YJ, Mowry KL (2004) Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin. Development 131:3035–3045PubMedCrossRefGoogle Scholar
  199. 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 267:60–71PubMedCrossRefGoogle Scholar
  200. 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 122:2947–2953PubMedGoogle Scholar
  201. Zhou Y, King ML (1996b) RNA transport to the vegetal cortex of Xenopus oocytes. Dev Biol 179:173–183PubMedCrossRefGoogle Scholar
  202. 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 34:209–220PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Matias Escobar-Aguirre
    • 1
  • Yaniv M. Elkouby
    • 1
  • Mary C. Mullins
    • 1
    Email author
  1. 1.Department of Cell and Developmental BiologyUniversity of Pennsylvania Perelman School of MedicinePhiladelphiaUSA

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