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Squid is required for efficient posterior localization of oskar mRNA during Drosophila oogenesis

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Abstract

The nuclear–cytoplasmic shuttling heterogeneous nuclear RNA-binding protein (hnRNP) Squid (Sqd) is required during Drosophila melanogaster oogenesis, where it plays a critical role in the regulation of the TGFα-like molecule Gurken (Grk). Three Sqd isoforms have been described, SqdA, S and B, and two of these, SqdA and SqdS, differentially function in grk mRNA nuclear export, cytoplasmic transport and translational control during oogenesis. Here, we report that Sqd is also required for the regulation of oskar (osk) mRNA, functioning in the cytoplasmic localization of the osk transcript. In oocytes from sqd females, osk mRNA is not efficiently localized to the posterior pole, but rather accumulates at the anterior cortex. Furthermore, anterior patterning defects observed in embryos from sqd females expressing only the SqdS protein isoform suggest that Sqd may also play a role in the translational regulation of the mislocalized osk mRNA. These findings provide additional support for models of mRNA regulation in which cytoplasmic events, such as localization and translational regulation, are coupled. These results also place Sqd among an emerging class of proteins, including such other members as Bruno (Bru) and Hrb27C/Hrp48, which function in multiple aspects of both grk and osk mRNA regulation during Drosophila oogenesis.

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References

  • Braat AK, Yan N, Arn E, Harrison D, Macdonald PM (2004) Localization-dependent oskar protein accumulation; control after the initiation of translation. Dev Cell 7:125–131

    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

    Google Scholar 

  • Castagnetti S, Ephrussi A (2003) Orb and a long poly(A) tail are required for efficient oskar translation at the posterior pole of the Drosophila oocyte. Development 130:835–843

    Google Scholar 

  • Chang JS, Tan L, Schedl P (1999) The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev Biol 215:91–106

    Google Scholar 

  • Clark IE, Giniger H, Ruohola-Baker H, Jan L, Jan Y (1994) Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr Biol 4:289–300

    Google Scholar 

  • Clark I, Jan LY, Jan YN (1997) Reciprocal localization of nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124:461–470

    Google Scholar 

  • Davis I (2004) A helicase that gets Oskar’s message across. Nat Cell Biol 6:285–287

    Google Scholar 

  • Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93

    Google Scholar 

  • Duncan JE, Warrior R (2002) The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr Biol 12:1982–1991

    Google Scholar 

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

    CAS  PubMed  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

    Google Scholar 

  • Ghabriel A, Ray RP, Schüpbach T (1998) okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev 12:2711–2723

    Google Scholar 

  • Gonzalez-Reyes A, St. Johnston D (1994) Role of oocyte position in the establishment of anterior–posterior polarity in Drosophila. Science 266:639–642

    Google Scholar 

  • Gonzalez-Reyes A, Elliott H, St. Johnston D (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signaling. Nature 375:654–658

    Google Scholar 

  • Goodrich JS, Clouse KN, Schüpbach T (2004) Hrb27C, Sqd and Otu cooperatively regulate gurken mRNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development 131:1949–1958

    Google Scholar 

  • Gunkel N, Yano T, Markussen F-H, Olsen LC, Ephrussi A (1998) Localization-dependent translation requires a function interaction between the 5′ and 3′ ends of oskar mRNA. Genes Dev 12:41652–41664

    Google Scholar 

  • Hachet O, Ephrussi A (2001) Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr Biol 11:1666–1674

    Google Scholar 

  • Hachet O, Ephrussi A (2004) Splicing of osk mRNA in the nucleus is coupled to its cytoplasmic localization. Nature 428:959–963

    Google Scholar 

  • Huynh J-R, Munro TP, Smith-Litiere K, Lepesant J-A, St. Johnston D (2004) The Drosophila hnRNPA/B homolog, Hrp48, is specifically required for a distinct step in osk mRNA localization. Dev Cell 6:625–635

    Google Scholar 

  • Januschke J, Gervais L, Dass S, Kaltschmidt JA, Lopez-Schier H, St. Johnston S, Brand AH, Roth S, Guichet A (2002) Polar transport in the Drosophila oocyte requires dynein and kinesin I cooperation. Curr Biol 12:1971–1981

    Google Scholar 

  • Johnstone O, Lasko P (2001) Translational regulation and RNA localization Drosophila oocytes and embryos. Annu Rev Genet 35:365–406

    Google Scholar 

  • Kelley RL (1993) Initial organization of the Drosophila dorso-ventral axis depends on an RNA-binding protein encoded by the squid gene. Genes Dev 7:948–960

    Google Scholar 

  • Kim-Ha J, Smith JL, Macdonald PM (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35

    Google Scholar 

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

    Google Scholar 

  • Lehmann R, Nusslein-Volhard C (1986) Abdominal segmentation, pole cell formation, embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47:141–152

    Google Scholar 

  • MacDougall N, Clark A, MacDougall E, Davis I (2003) Drosophila gurken (TGFα) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps. Dev Cell 4:307–319

    Google Scholar 

  • Markussen F-H, Michon A-M, Breitwieser W, Ephrussi A (1995) Translational control of oskar generates Short Osk, the isoform that induces pole plasm assembly. Development 121:3723–3732

    Google Scholar 

  • Matunis EL, Matunis MJ, Dreyfuss G (1992) Characterization of the major hnRNP proteins from Drosophila melanogaster. J Cell Biol 116:257–269

    Google Scholar 

  • Matunis EL, Kelley RL, Dreyfuss G (1994) Essential role for a heterogeneous nuclear ribonucleoprotein (hnRNP) in oogenesis: hrp40 is absent from the germline in the dorso-ventral mutant squid. Proc Natl Acad Sci U S A 91:2781–2784

    Google Scholar 

  • Micklem DR, Dasgupta R, Ellioitt H, Gergely F, Davidson C, Brand A, Gonzalez-Reyes A, St. Johnston D (1997) The mago nashi gene is required for the polarisation of the oocyte and formation of perpendicular axes in Drosophila. Curr Biol 7:468–478

    Google Scholar 

  • Mohr SE, Dillon ST, Boswell RE (2001) The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes Dev 15:2886–2899

    Google Scholar 

  • Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A 98:15050–15055

    Google Scholar 

  • Nakamura A, Sato K, Hanyu-Nakamura K (2004) Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates osk mRNA translation in oogenesis. Dev Cell 6:69–78

    Google Scholar 

  • Navarro C, Puthalakath H, Adams JM, Strasser A, Lehmann R (2004) Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate. Nat Cell Biol 6:427–435

    Google Scholar 

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

    Google Scholar 

  • Newmark PA, Mohr SE, Gong L, Boswell RE (1997) Mago nashi mediates the posterior follicle cell-to-oocyte signal to organize axis formation in Drosophila. Development 124:3197–3207

    Google Scholar 

  • Norvell A, Kelley RL, Wehr K, Schüpbach T (1999) Specific isoforms of Squid, a Drosophila hnRNP, perform distinct roles in Gurken localization during oogenesis. Genes Dev 13:864–876

    Google Scholar 

  • Palacios I, St. Johnston D (2002) Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte

  • Palacios IM, Gatfield D, St. Johnston D, Izaurralde E (2004) An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427:753–757

    Google Scholar 

  • Ray RP, Schüpbach TS (1996) Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev 10:1711–1723

    Google Scholar 

  • Riechmann V, Ephrussi A (2001) Axis formation during Drosophila oogenesis. Curr Opin Genet Dev 11:374–383

    Google Scholar 

  • Roth S, Neuman-Silberberg S, 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

    Google Scholar 

  • Schüpbach T (1987) Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of eggshell and embryo in Drosophila melanogaster. Cell 49:699–707

    Google Scholar 

  • Smith JL, Wilson JE, Macdonald PM (1992) Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos. Cell 70:849–859

    Google Scholar 

  • St. Johnston D, Beuchle D, Nüsslein-Volhard C (1991) Staufen, a gene required to localize maternal RNAs in Drosophila eggs. Cell 66:651–663

    Google Scholar 

  • Swan A, Nguyen T, Suter B (1999) Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat Cell Biol 1:444–449

    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

    Google Scholar 

  • van Eeden FJM, Palacios IM, Petronczki M, Weston MJD, St. Johnston D (2001) Barentz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J Cell Biol 154:511–523

    Google Scholar 

  • Wilhelm JE, Hilton M, Amos Q, Henzel WJ (2004) Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentz. J Cell Biol 163:1197–1204

    Google Scholar 

  • Yano T, deQuinto SL, Matsui Y, Shevchenko A, Shevchenko A, Ephrussi A (2004) Hrp 48, a Drosophila hnRNPa/B homolog, binds and regulates translation of osk mRNA. Dev Cell 6:637–648

    Google Scholar 

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Acknowledgements

We are grateful to Anne Ephrussi, Nicole Clouse, Jennifer Goodrich and Trudi Schüpbach for providing fly stocks, reagents and antibodies. We would also like to thank a number of individuals, including Marcia O’Connell, Trudi Schüpbach and Jennifer Goodrich for their many helpful discussions and for their thoughtful suggestions on the manuscript. AD was supported by the Ligue Nationale Contre le Cancer, (comité des Alpes Maritimes).

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Correspondence to Amanda Norvell.

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Communicated by S. Roth

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Norvell, A., Debec, A., Finch, D. et al. Squid is required for efficient posterior localization of oskar mRNA during Drosophila oogenesis. Dev Genes Evol 215, 340–349 (2005). https://doi.org/10.1007/s00427-005-0480-2

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