Development Genes and Evolution

, Volume 215, Issue 7, pp 340–349

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

  • Amanda Norvell
  • Alain Debec
  • Daniel Finch
  • Lisa Gibson
  • Brandi Thoma
Original Article

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.

Keywords

Drosophila oogenesis Squid Gurken Oskar RNA localization 

References

  1. Braat AK, Yan N, Arn E, Harrison D, Macdonald PM (2004) Localization-dependent oskar protein accumulation; control after the initiation of translation. Dev Cell 7:125–131Google Scholar
  2. 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 289:2120–2122Google Scholar
  3. 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 130:835–843Google Scholar
  4. Chang JS, Tan L, Schedl P (1999) The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev Biol 215:91–106Google Scholar
  5. 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 4:289–300Google Scholar
  6. 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 124:461–470Google Scholar
  7. Davis I (2004) A helicase that gets Oskar’s message across. Nat Cell Biol 6:285–287Google Scholar
  8. Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93Google Scholar
  9. Duncan JE, Warrior R (2002) The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr Biol 12:1982–1991Google Scholar
  10. Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387–392PubMedGoogle Scholar
  11. Ephrussi A, Dickinson LK, Lehmann R (1991) oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50Google Scholar
  12. 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 12:2711–2723Google Scholar
  13. Gonzalez-Reyes A, St. Johnston D (1994) Role of oocyte position in the establishment of anterior–posterior polarity in Drosophila. Science 266:639–642Google Scholar
  14. Gonzalez-Reyes A, Elliott H, St. Johnston D (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signaling. Nature 375:654–658Google Scholar
  15. 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 131:1949–1958Google Scholar
  16. 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 12:41652–41664Google Scholar
  17. Hachet O, Ephrussi A (2001) Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr Biol 11:1666–1674Google Scholar
  18. Hachet O, Ephrussi A (2004) Splicing of osk mRNA in the nucleus is coupled to its cytoplasmic localization. Nature 428:959–963Google Scholar
  19. 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 6:625–635Google Scholar
  20. 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 12:1971–1981Google Scholar
  21. Johnstone O, Lasko P (2001) Translational regulation and RNA localization Drosophila oocytes and embryos. Annu Rev Genet 35:365–406Google Scholar
  22. Kelley RL (1993) Initial organization of the Drosophila dorso-ventral axis depends on an RNA-binding protein encoded by the squid gene. Genes Dev 7:948–960Google Scholar
  23. Kim-Ha J, Smith JL, Macdonald PM (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35Google Scholar
  24. Kim-Ha J, Kerr K, Macdonald PM (1995) Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential. Cell 81:403–412Google Scholar
  25. 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 47:141–152Google Scholar
  26. 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 4:307–319Google Scholar
  27. 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 121:3723–3732Google Scholar
  28. Matunis EL, Matunis MJ, Dreyfuss G (1992) Characterization of the major hnRNP proteins from Drosophila melanogaster. J Cell Biol 116:257–269Google Scholar
  29. 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 91:2781–2784Google Scholar
  30. 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 7:468–478Google Scholar
  31. 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 15:2886–2899Google Scholar
  32. 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 98:15050–15055Google Scholar
  33. 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 6:69–78Google Scholar
  34. 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 6:427–435Google Scholar
  35. Neuman-Silberberg S, Schüpbach T (1993) The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFα-like protein. Cell 75:165–174Google Scholar
  36. 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 124:3197–3207Google Scholar
  37. 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 13:864–876Google Scholar
  38. 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 oocyteGoogle Scholar
  39. Palacios IM, Gatfield D, St. Johnston D, Izaurralde E (2004) An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427:753–757Google Scholar
  40. Ray RP, Schüpbach TS (1996) Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev 10:1711–1723Google Scholar
  41. Riechmann V, Ephrussi A (2001) Axis formation during Drosophila oogenesis. Curr Opin Genet Dev 11:374–383Google Scholar
  42. 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 81:967–978Google Scholar
  43. Schüpbach T (1987) Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of eggshell and embryo in Drosophila melanogaster. Cell 49:699–707Google Scholar
  44. Smith JL, Wilson JE, Macdonald PM (1992) Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos. Cell 70:849–859Google Scholar
  45. St. Johnston D, Beuchle D, Nüsslein-Volhard C (1991) Staufen, a gene required to localize maternal RNAs in Drosophila eggs. Cell 66:651–663Google Scholar
  46. 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 1:444–449Google Scholar
  47. Theurkauf WE, Smiley S, Wong ML, Alberts BM (1992) Reorganization of the cytoskeleton during Drosophila oogenesis—implications for axis specification and intercellular transport. Development 115:923–936Google Scholar
  48. 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 154:511–523Google Scholar
  49. 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 163:1197–1204Google Scholar
  50. 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 6:637–648Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Amanda Norvell
    • 1
  • Alain Debec
    • 2
  • Daniel Finch
    • 1
  • Lisa Gibson
    • 1
  • Brandi Thoma
    • 1
  1. 1.Department of BiologyThe College of New JerseyEwingUSA
  2. 2.Biologie du Développement, Observatoire OcéanologiqueUniversité Pierre et Marie CurieVillefranche-sur-Mer CedexFrance

Personalised recommendations