Skip to main content

Multiple Functions of the DEAD-Box Helicase Vasa in Drosophila Oogenesis

  • Chapter
  • First Online:
Oocytes

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 63))

Abstract

The DEAD-box helicase Vasa (Vas) has been most extensively studied in the fruit fly, Drosophila melanogaster, and numerous roles for it in germline development have been discovered. Here, we summarize the present state of knowledge about processes during oogenesis that involve Vas, as well as functions of Vas as a maternal determinant of embryonic spatial patterning and germ cell specification. We review literature that implicates Vas in Piwi-interacting RNA (piRNA) biogenesis in germline cells and in regulating mitosis in germline stem cells (GSCs). We describe the functions of Vas in translational activation of two mRNAs, gurken (grk) and mei-P26, which encode proteins that are important regulators of developmental processes, as Grk specifies both the dorsal-ventral and the anterior-posterior axis of the embryo and Mei-P26 promotes GSC differentiation. The role of Vas in assembly of polar granules, ribonucleoprotein particles that accumulate in the posterior pole plasm of the oocyte and are essential for germ cell specification and posterior embryonic patterning, is also described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdu U, Brodsky M, Schupbach T (2002) Activation of a meiotic checkpoint during Drosophila oogenesis regulates the translation of gurken through Chk2/Mnk. Curr Biol 12:1645–1651

    Article  CAS  PubMed  Google Scholar 

  • Ables ET (2015) Drosophila oocytes as a model for understanding meiosis: an educational primer to accompany “Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila”. Genetics 199:17–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anand A, Kai T (2012) The tudor domain protein Kumo is required to assemble the nuage and to generate germline piRNAs in Drosophila. EMBO J 31:870–882

    Article  CAS  PubMed  Google Scholar 

  • Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K, Kobayashi S (1999) Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1:431–437

    Article  CAS  PubMed  Google Scholar 

  • Assa-Kunik E, Torres IL, Schejter ED, St Johnston D, Shilo BZ (2007) Drosophila follicle cells are patterned by multiple levels of Notch signaling and antagonism between the Notch and JAK/STAT pathways. Development 134:1161–1169

    Article  CAS  PubMed  Google Scholar 

  • Barbosa C, Peixeiro I, Romao L (2013) Gene expression regulation by upstream open reading frames and human disease. PLoS Genet 9:e1003529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastock R, St Johnston D (2008) Drosophila oogenesis. Curr Biol 18:R1082–R1087

    Article  CAS  PubMed  Google Scholar 

  • Becalska AN, Gavis ER (2009) Lighting up mRNA localization in Drosophila oogenesis. Development 136:2493–2503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berg CA (2005) The Drosophila shell game: patterning genes and morphological change. Trends Genet 21:346–355

    Article  CAS  PubMed  Google Scholar 

  • Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nüsslein-Volhard C (1988) The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryos. EMBO J 7:1749–1756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhat MA, Philp AV, Glover DM, Bellen HJ (1996) Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87:1103–1114

    Article  PubMed  Google Scholar 

  • Breitwieser W, Markussen FH, Horstmann H, Ephrussi A (1996) Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev 10:2179–2188

    Article  CAS  PubMed  Google Scholar 

  • Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    Article  CAS  PubMed  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin

    Book  Google Scholar 

  • Carrera P, Johnstone O, Nakamura A, Casanova J, Jäckle H, Lasko P (2000) VASA mediates translation through interaction with a Drosophila yIF2 homolog. Mol Cell 5:181–187

    Article  CAS  PubMed  Google Scholar 

  • Cavaliere V, Taddei C, Gargiulo G (1998). Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster. Dev Genes Evol 208:106–112

    Google Scholar 

  • Chang H, Matzuk MM (2001) Smad5 is required for mouse primordial germ cell development. Mech Dev 104:61–67

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Potratz JP, Tijerina P, Del Campo M, Lambowitz AM, Russell R (2008) DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc Natl Acad Sci USA 105:20203–20208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chuang RY, Weaver PL, Liu Z, Chang TH (1997) Requirement of the DEAD-box protein Ded1p for messenger RNA translation. Science 275:1468–1471

    Article  CAS  PubMed  Google Scholar 

  • Clark A, Meignin C, Davis I (2007) A Dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte. Development 134:1955–1965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clouse KN, Ferguson SB, Schupbach T (2008) Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Dev Biol 313:713–724

    Article  CAS  PubMed  Google Scholar 

  • Cordin O, Banroques J, Tanner NK, Linder P (2006) The DEAD-box protein family of RNA helicases. Gene 367:17–37

    Article  CAS  PubMed  Google Scholar 

  • Dehghani M, Lasko P (2015) In vivo mapping of the functional regions of the DEAD-box helicase Vasa. Biol Open 4:450–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dehghani M, Lasko P (2016) C-terminal residues specific to Vasa among DEAD-box helicases are required for its functions in piRNA biogenesis and embryonic patterning. Dev Genes Evol 226(6):401–412

    Google Scholar 

  • Deng W, Lin HF (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2:819–830

    Article  CAS  PubMed  Google Scholar 

  • Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164:501–509

    CAS  PubMed  PubMed Central  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 

  • Fekete CA, Applefield DJ, Blakely SA, Shirokikh N, Pestova T, Lorsch JR, Hinnebusch AG (2005) The eIF1A C-terminal domain promotes initiation complex assembly, scanning and AUG selection in vivo. EMBO J 24:3588–3601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forbes A, Lehmann R (1998) Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125:679–690

    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 

  • Gavis ER, Lehmann R (1992) Localization of nanos RNA controls embryonic polarity. Cell 71:301–313

    Article  CAS  PubMed  Google Scholar 

  • Geigy R (1931) Action de l’ultra-violet sur le pole germinal dans l’oeuf de Drosophila melanogaster. Rev Suisse Zool 38:187–288

    Article  Google Scholar 

  • Ghabrial A, Schupbach T (1999) Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat Cell Biol 1:354–357

    Article  CAS  PubMed  Google Scholar 

  • Goldman CH, Gonsalvez GB (2017) The role of microtubule motors in mRNA localization and patterning within the Drosophila oocyte. In: Kloc M (ed) Oocytes. Springer, Heidelberg

    Google Scholar 

  • González-Reyes A, Elliott H, Stjohnston D (1995) Polarization of both major body axes in Drosophila by Gurken-Torpedo signaling. Nature 375:654–658

    Article  PubMed  Google Scholar 

  • Grieder NC, de Cuevas M, Spradling AC (2000) The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127:4253–4264

    CAS  PubMed  Google Scholar 

  • Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455:1193–1115

    Article  CAS  PubMed  Google Scholar 

  • Haase AD (2016) A small RNA-based immune system defends germ cells against mobile genetic elements. Stem Cells Int 2016:7595791

    Article  PubMed  Google Scholar 

  • Harris AN, Macdonald PM (2001) aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128:2823–2832

    CAS  PubMed  Google Scholar 

  • Harrison RE, Huebner E (1997) Unipolar microtubule array is directly involved in nurse cell-oocyte transport. Cell Motil Cytoskeleton 36:355–362

    Article  CAS  PubMed  Google Scholar 

  • Hay B, Jan LY, Jan YN (1988b) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55:577–587

    Article  CAS  PubMed  Google Scholar 

  • Hay B, Jan LY, Jan YN (1990) Localization of Vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development 109:425–433

    CAS  PubMed  Google Scholar 

  • Hilbert M, Karow AR, Klostermeier D (2009) The mechanism of ATP-dependent RNA unwinding by DEAD-box proteins. Biol Chem 390:1237–1250

    Article  CAS  PubMed  Google Scholar 

  • Hinnebusch AG (2014) The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem 83:779–812

    Article  CAS  PubMed  Google Scholar 

  • Hirakata S, Siomi MC (2016) piRNA biogenesis in the germline: from transcription of piRNA genomic sources to piRNA maturation. Biochim Biophys Acta 1859:82–92

    Article  CAS  PubMed  Google Scholar 

  • Horner VL, Wolfner MF (2008) Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn 237:527–544

    Article  CAS  PubMed  Google Scholar 

  • Huang YZ, Baker RT, Fischervize JA (1995) Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science 270:1828–1831

    Article  CAS  PubMed  Google Scholar 

  • Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H (2013) A major epigenetic programming mechanism guided by piRNAs. Dev Cell 24:502–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu TT, Eisen MB, Thornton KR, Andolfatto P (2013) A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res 23:89–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila – induction of germ cells at anterior pole of egg. Proc Natl Acad Sci USA 71:1016–1020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnstone O, Lasko P (2004) Interaction with eIF513 is essential for Vasa function during development. Development 131:4167–4178

    Article  CAS  PubMed  Google Scholar 

  • Johnstone O, Deuring R, Bock R, Linder P, Fuller MT, Lasko P (2005) Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Dev Biol 277:92–101

    Article  CAS  PubMed  Google Scholar 

  • Jongens TA, Hay B, Jan LY, Jan YN (1992) The germ cell-less gene product – a posterior localized component necessary for germ-cell development in Drosophila. Cell 70:569–584

    Article  CAS  PubMed  Google Scholar 

  • Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SE (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: RESEARCH0084

    Google Scholar 

  • Kawaoka S, Hayashi N, Suzuki Y, Abe H, Sugano S, Tomari Y, Shimada T, Katsuma S (2009) The Bombyx ovary-derived cell line endogenously expresses Piwi/Piwi-interacting RNA complexes. RNA 15:1258–1264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim-Ha J, Kerr K, Macdonald PM (1995) Translational regulation of oskar messenger RNA by Bruno, an ovarian RNA-binding protein, is essential. Cell 81:403–412

    Article  CAS  PubMed  Google Scholar 

  • King RC (1970) Ovarian development in Drosophila melanogaster. Academic Press, New York

    Google Scholar 

  • Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, Zhang F, Schultz N, Koppetsch BS, Nowosielska A et al (2009) The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138:1137–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kugler JM, Woo JS, Oh BH, Lasko P (2010) Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors. Mol Cell Biol 30:1769–1782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W et al (2004) mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131:839–849

    Article  CAS  PubMed  Google Scholar 

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, Kojima-Kita K, Shiromoto Y, Asada N, Toyoda A, Fujiyama A et al (2010) MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 24:887–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lasko PF (2012) mRNA localization and translational control in Drosophila oogenesis. Cold Spring Harb Perspect Biol 4:pii: a012294

    Google Scholar 

  • Lasko PF, Ashburner M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335:611–617

    Article  CAS  PubMed  Google Scholar 

  • Lasko PF, Ashburner M (1990) Posterior localization of Vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4:905–921

    Article  CAS  PubMed  Google Scholar 

  • Lehmann R, Nüsslein-Volhard C (1987) hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev Biol 119:402–417

    Article  CAS  PubMed  Google Scholar 

  • Lehmann R (2012) Germline stem cells: origin and destiny. Cell Stem Cell 10:729–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerit DA, Gavis ER (2011) Transport of germ plasm on astral microtubules directs germ cell development in Drosophila. Curr Biol 21:439–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lesch BJ, Page DC (2012) Genetics of germ cell development. Nat Rev Genetics 13:781–794

    Article  CAS  PubMed  Google Scholar 

  • Li W, Klovstad M, Schuepbach T (2014) Repression of Gurken translation by a meiotic checkpoint in Drosophila oogenesis is suppressed by a reduction in the dose of eIF1A. Development 141:3910–3921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang L, Diehljones W, Lasko P (1994) Localization of Vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120:1201–1211

    CAS  PubMed  Google Scholar 

  • Linder P, Fuller-Pace FV (2013) Looking back on the birth of DEAD-box RNA helicases. Biochim Biophys Acta 1829:750–755

    Article  CAS  PubMed  Google Scholar 

  • Linder P, Jankowsky E (2011) From unwinding to clamping – the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12:505–516

    Article  CAS  PubMed  Google Scholar 

  • Linder P, Lasko PF, Ashburner M, Leroy P, Nielsen PJ, Nishi K, Schnier J, Slonimski PP (1989) Birth of the D-E-A-D box. Nature 337:121–122

    Article  CAS  PubMed  Google Scholar 

  • Liu NK, Dansereau DA, Lasko P (2003) Fat facets interacts with Vasa in the Drosophila pole plasm and protects it from degradation. Curr Biol 13:1905–1909

    Article  CAS  PubMed  Google Scholar 

  • Liu NK, Han H, Lasko P (2009) Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3′ UTR. Genes Dev 23:2742–2752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mach JM, Lehmann R (1997) An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev 11:423–435

    Article  CAS  PubMed  Google Scholar 

  • Mahowald AP (1968) Polar granules in Drosophila: II. Ultrastructural changes during early embryogenesis. J Exp Zool 167:237–261

    Article  CAS  PubMed  Google Scholar 

  • Mahowald AP, Goralski TJ, Caulton JH (1983) In vitro activation of Drosophila eggs. Dev Biol 98:437–445

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin JM, Bratu DP (2015) Drosophila melanogaster oogenesis: an overview. Methods Mol Biol 1328:1–20

    Article  CAS  PubMed  Google Scholar 

  • Meignin C, Davis I (2010) Transmitting the message: intracellular mRNA localization. Curr Opin Cell Biol 22:112–119

    Article  CAS  PubMed  Google Scholar 

  • Meister G (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14:447–459

    Article  CAS  PubMed  Google Scholar 

  • Mills RE, Bennett EA, Iskow RC, Devine SE (2007) Which transposable elements are active in the human genome? Trends Genet 23:183–191

    Article  CAS  PubMed  Google Scholar 

  • Mohn F, Sienski G, Handler D, Brennecke J (2014) The Rhino-Deadlock-Cutoff complex Licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157:1364–1379

    Article  CAS  PubMed  Google Scholar 

  • Murata Y, Wharton RP (1995) Binding of Pumilio to maternal Hunchback messenger RNA is required for posterior patterning in Drosophila embryos. Cell 80:747–756

    Article  CAS  PubMed  Google Scholar 

  • Nakamura A, Amikura R, Mukai M, Kobayashi S, Lasko PF (1996) Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science 274:2075–2079

    Article  CAS  PubMed  Google Scholar 

  • Neuman-Silberberg FS, Schupbach T (1993) The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF-alpha-like protein. Cell 75:165–174

    Article  CAS  PubMed  Google Scholar 

  • Neuman-Silberberg FS, Schupbach T (1996) The Drosophila TGF-alpha-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech Dev 59:105–113

    Article  CAS  PubMed  Google Scholar 

  • Neumuller RA, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K, Cohen SM, Knoblich JA (2008) Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454:241–245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishida KM, Iwasaki YW, Murota Y, Nagao A, Mannen T, Kato Y, Siomi H, Siomi MC (2015) Respective functions of two distinct Siwi complexes assembled during Piwi-interacting RNA biogenesis in Bombyx germ cells. Cell Rep. 10:193–203

    Article  CAS  PubMed  Google Scholar 

  • Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, Matsumoto N, Nishizawa T, Nakanaga K, Aoki J et al (2012) Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491:284–287

    Article  CAS  PubMed  Google Scholar 

  • Okada M, Kleinman IA, Schneide HA (1974) Restoration of fertility in sterilized Drosophila eggs by transplantation of polar cytoplasm. Dev Biol 37:43–54

    Article  CAS  PubMed  Google Scholar 

  • Page SL, McKim KS, Deneen B, Van Hook TL, Hawley RS (2000) Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics 155:1757–1772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parton RM, Hamilton RS, Ball G, Yang L, Cullen CF, Lu W, Ohkura H, Davis I (2011) A PAR-1-dependent orientation gradient of dynamic microtubules directs posterior cargo transport in the Drosophila oocyte. J Cell Biol 194:121–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patil VS, Kai T (2010) Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas. Curr Biol 20:724–730

    Article  CAS  PubMed  Google Scholar 

  • Pek JW, Kai T (2011a) A Role for Vasa in regulating mitotic chromosome condensation in Drosophila. Curr Biol 21:39–44

    Article  CAS  PubMed  Google Scholar 

  • Pek JW, Kai T (2011b) DEAD-box RNA helicase Belle/DDX3 and the RNA interference pathway promote mitotic chromosome segregation. Proc Natl Acad Sci USA 108:12007–12012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelisson A, Song SU, Prudhomme N, Smith PA, Bucheton A, Corces VG (1994) Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J 13:4401–4411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pestova TV, Lomakin IB, Lee JH, Choi SK, Dever TE, Hellen CU (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403:332–335

    Article  CAS  PubMed  Google Scholar 

  • Pray LA (2008) Transposons: the jumping genes. Nat Educ 1:204

    Google Scholar 

  • Roth S, Lynch JA (2009) Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol 1:a001891

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth S, Neuman-Silberberg FS, Barcelo G, Schüpbach T (1995) cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81:967–978

    Article  CAS  PubMed  Google Scholar 

  • Rudolph MG, Klostermeier D (2015) When core competence is not enough: functional interplay of the DEAD-box helicase core with ancillary domains and auxiliary factors in RNA binding and unwinding. Biol Chem 396:849–865

    Article  CAS  PubMed  Google Scholar 

  • Saito K (2013) The epigenetic regulation of transposable elements by Piwi-interacting RNAs in Drosophila. Genes Genet Syst 88:9–17

    Article  CAS  PubMed  Google Scholar 

  • Schupbach T, Wieschaus E (1986a) Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113:443–448

    Article  CAS  PubMed  Google Scholar 

  • Schupbach T, Wieschaus E (1986b) Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux Arch Dev Biol 195:302–317

    Article  PubMed  Google Scholar 

  • Schwer B, Meszaros T (2000) RNA helicase dynamics in pre-mRNA splicing. EMBO J 19:6582–6591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seleme MD, Busseau I, Malinsky S, Bucheton A, Teninges D (1999) High-frequency retrotransposition of a marked I factor in Drosophila melanogaster correlates with a dynamic expression pattern of the ORF1 protein in the cytoplasm of oocytes. Genetics 151:761–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sengoku T, Nureki O, Nakamura A, Satoru KI, Yokoyama S (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125:287–300

    Article  CAS  PubMed  Google Scholar 

  • Sinsimer KS, Lee JJ, Thiberge SY, Gavis ER (2013) Germ plasm anchoring is a dynamic state that requires persistent trafficking. Cell Rep 5:1169–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snee MJ, Macdonald PM (2004) Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J Cell Sci 117:2109–2120

    Article  CAS  PubMed  Google Scholar 

  • Somma MP, Fasulo B, Siriaco G, Cenci G (2003) Chromosome condensation defects in barren RNA-interfered Drosophila cells. Genetics 165:1607–1611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steinhauer J, Kalderon D (2006) Microtubule polarity and axis formation in the Drosophila oocyte. Dev Dyn 235:1455–1468

    Article  CAS  PubMed  Google Scholar 

  • Styhler S, Nakamura A, Swan A, Suter B, Lasko P (1998) Vasa is required for Gurken accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125:1569–1578

    CAS  PubMed  Google Scholar 

  • Styhler S, Nakamura A, Lasko P (2002) Vasa localization requires the SPRY-domain and SOCS-box containing protein, Gustavus. Dev Cell 3:865–876

    Article  CAS  PubMed  Google Scholar 

  • Su TT, Campbell SD, O’Farrell PH (1998) The cell cycle program in germ cells of the Drosophila embryo. Dev Biol 196:160–170

    Article  CAS  PubMed  Google Scholar 

  • Tautz D (1988) Regulation of the Drosophila segmentation gene hunchback by 2 maternal morphogenetic centers. Nature 332:281–284

    Article  CAS  PubMed  Google Scholar 

  • Theurkauf WE, Smiley S, Wong ML, Alberts BM (1992) Reorganization of the cytoskeleton during Drosophila oogenesis – implications for axis specification and intercellular transport. Development 115:923–936

    CAS  PubMed  Google Scholar 

  • Thio GL, Ray RP, Barcelo G, Schupbach T (2000) Localization of gurken RNA in Drosophila oogenesis requires elements in the 5′ and 3′ regions of the transcript. Dev Biol 221:435–446

    Article  CAS  PubMed  Google Scholar 

  • Tomancak P, Guichet A, Zavorszky P, Ephrussi A (1998) Oocyte polarity depends on regulation of gurken by Vasa. Development 125:1723–1732

    CAS  PubMed  Google Scholar 

  • Torres IL, Lopez-Schier H, St Johnston D (2003) A notch/delta-dependent relay mechanism establishes anterior-posterior polarity in Drosophila. Dev Cell 5:547–558

    Article  CAS  PubMed  Google Scholar 

  • Ulvila J, Parikka M, Kleino A, Sormunen R, Ezekowitz RA, Kocks C, Ramet M (2006) Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 281:14370–14375

    Article  CAS  PubMed  Google Scholar 

  • Webster PJ, Liang L, Berg CA, Lasko P, Macdonald PM (1997) Translational repressor Bruno plays multiple roles in development and is widely conserved. Genes Dev 11:2510–2521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster A, Li S, Hur JK, Wachsmuth M, Bois JS, Perkins EM, Patel DJ, Aravin AA (2015) Aub and Ago3 are recruited to nuage through two mechanisms to form a ping-pong complex assembled by Krimper. Mol Cell 59:564–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weil TT (2014) mRNA localization in the Drosophila germline. RNA Biol 11:1010–1018

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiol J, Spinelli P, Laussmann MA, Homolka D, Yang Z, Cora E, Couté Y, Conn S, Kadlec J, Sachidanandam R, Kaksonen M, Cusack S, Ephrussi A, Pillai RS (2014) RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 157:1698–1711

    Article  CAS  PubMed  Google Scholar 

  • Zaessinger S, Busseau I, Simonelig M (2006) Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 133:4573–4583

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, Schultz N, Vreven T, Meignin C, Davis I, Zamore PD, et al. (2012). UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151: 871-884

    Google Scholar 

  • Zhao T, Graham OS, Raposo A, St Johnston D (2012) Growing microtubules push the oocyte nucleus to polarize the Drosophila dorsal-ventral axis. Science 336:999–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou R, Hotta I, Denli AM, Hong P, Perrimon N, Hannon GJ (2008) Comparative analysis of argonaute-dependent small RNA pathways in Drosophila. Mol Cell 32:592–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimyanin VL, Belaya K, Pecreaux J, Gilchrist MJ, Clark A, Davis I, St Johnston D (2008) In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134:843–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul Lasko .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Dehghani, M., Lasko, P. (2017). Multiple Functions of the DEAD-Box Helicase Vasa in Drosophila Oogenesis. In: Kloc, M. (eds) Oocytes. Results and Problems in Cell Differentiation, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-319-60855-6_6

Download citation

Publish with us

Policies and ethics