• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Jul 2001; 158(3): 1177–1188.
PMCID: PMC1461719

An interaction type of genetic screen reveals a role of the Rab11 gene in oskar mRNA localization in the developing Drosophila melanogaster oocyte.


Abdomen and germ cell development of Drosophila melanogaster embryo requires proper localization of oskar mRNA to the posterior pole of the developing oocyte. oskar mRNA localization depends on complex cell biological events like cell-cell communication, dynamic rearrangement of the microtubule network, and function of the actin cytoskeleton of the oocyte. To investigate the cellular mechanisms involved, we developed a novel interaction type of genetic screen by which we isolated 14 dominant enhancers of a sensitized genetic background composed of mutations in oskar and in TropomyosinII, an actin binding protein. Here we describe the detailed analysis of two allelic modifiers that identify Drosophila Rab11, a gene encoding small monomeric GTPase. We demonstrate that mutation of the Rab11 gene, involved in various vesicle transport processes, results in ectopic localization of oskar mRNA, whereas localization of gurken and bicoid mRNAs and signaling between the oocyte and the somatic follicle cells are unaffected. We show that the ectopic oskar mRNA localization in the Rab11 mutants is a consequence of an abnormally polarized oocyte microtubule cytoskeleton. Our results indicate that the internal membranous structures play an important role in the microtubule organization in the Drosophila oocyte and, thus, in oskar RNA localization.

Full Text

The Full Text of this article is available as a PDF (181K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • González-Reyes A, St Johnston D. Role of oocyte position in establishment of anterior-posterior polarity in Drosophila. Science. 1994 Oct 28;266(5185):639–642. [PubMed]
  • González-Reyes A, Elliott H, St Johnston D. Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature. 1995 Jun 22;375(6533):654–658. [PubMed]
  • Hay B, Ackerman L, Barbel S, Jan LY, Jan YN. Identification of a component of Drosophila polar granules. Development. 1988 Aug;103(4):625–640. [PubMed]
  • Hay B, Jan LY, Jan YN. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell. 1988 Nov 18;55(4):577–587. [PubMed]
  • Horowitz H, Berg CA. The Drosophila pipsqueak gene encodes a nuclear BTB-domain-containing protein required early in oogenesis. Development. 1996 Jun;122(6):1859–1871. [PubMed]
  • Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 1992 Dec;6(12A):2312–2326. [PubMed]
  • Jongens TA, Hay B, Jan LY, Jan YN. The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. Cell. 1992 Aug 21;70(4):569–584. [PubMed]
  • Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nüsslein-Volhard C. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 1988 Jun;7(6):1749–1756. [PMC free article] [PubMed]
  • Kobayashi S, Yamada M, Asaoka M, Kitamura T. Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature. 1996 Apr 25;380(6576):708–711. [PubMed]
  • Boswell RE, Prout ME, Steichen JC. Mutations in a newly identified Drosophila melanogaster gene, mago nashi, disrupt germ cell formation and result in the formation of mirror-image symmetrical double abdomen embryos. Development. 1991 Sep;113(1):373–384. [PubMed]
  • Lane ME, Kalderon D. RNA localization along the anteroposterior axis of the Drosophila oocyte requires PKA-mediated signal transduction to direct normal microtubule organization. Genes Dev. 1994 Dec 15;8(24):2986–2995. [PubMed]
  • Breitwieser W, Markussen FH, Horstmann H, Ephrussi A. Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev. 1996 Sep 1;10(17):2179–2188. [PubMed]
  • Lasko P. Cell-cell signalling, microtubule organization and RNA localization: is PKA a link? Bioessays. 1995 Feb;17(2):105–107. [PubMed]
  • Brendza RP, Serbus LR, Duffy JB, Saxton WM. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science. 2000 Sep 22;289(5487):2120–2122. [PMC free article] [PubMed]
  • Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler Y, Ray GS, Goldenring JR. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 1999 Jan;10(1):47–61. [PMC free article] [PubMed]
  • Micklem DR, Dasgupta R, Elliott H, Gergely F, Davidson C, Brand A, González-Reyes A, St Johnston D. The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr Biol. 1997 Jul 1;7(7):468–478. [PubMed]
  • Chen W, Feng Y, Chen D, Wandinger-Ness A. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell. 1998 Nov;9(11):3241–3257. [PMC free article] [PubMed]
  • Montell DJ, Rorth P, Spradling AC. slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell. 1992 Oct 2;71(1):51–62. [PubMed]
  • Chou TB, Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics. 1996 Dec;144(4):1673–1679. [PMC free article] [PubMed]
  • Nakamura A, Amikura R, Mukai M, Kobayashi S, Lasko PF. Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science. 1996 Dec 20;274(5295):2075–2079. [PubMed]
  • Clark I, Giniger E, Ruohola-Baker H, Jan LY, Jan YN. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr Biol. 1994 Apr 1;4(4):289–300. [PubMed]
  • Neuman-Silberberg FS, Schüpbach T. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell. 1993 Oct 8;75(1):165–174. [PubMed]
  • Clark IE, Jan LY, Jan YN. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development. 1997 Jan;124(2):461–470. [PubMed]
  • Nuoffer C, Balch WE. GTPases: multifunctional molecular switches regulating vesicular traffic. Annu Rev Biochem. 1994;63:949–990. [PubMed]
  • Cox D, Lee DJ, Dale BM, Calafat J, Greenberg S. A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):680–685. [PMC free article] [PubMed]
  • Perrimon N, Lanjuin A, Arnold C, Noll E. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics. 1996 Dec;144(4):1681–1692. [PMC free article] [PubMed]
  • Deng WM, Ruohola-Baker H. Laminin A is required for follicle cell-oocyte signaling that leads to establishment of the anterior-posterior axis in Drosophila. Curr Biol. 2000 Jun 1;10(11):683–686. [PubMed]
  • Deshpande G, Calhoun G, Yanowitz JL, Schedl PD. Novel functions of nanos in downregulating mitosis and transcription during the development of the Drosophila germline. Cell. 1999 Oct 29;99(3):271–281. [PubMed]
  • Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6187–6192. [PMC free article] [PubMed]
  • Ephrussi A, Dickinson LK, Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 1991 Jul 12;66(1):37–50. [PubMed]
  • Roth S, Neuman-Silberberg FS, Barcelo G, Schüpbach T. cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell. 1995 Jun 16;81(6):967–978. [PubMed]
  • Erdélyi M, Michon AM, Guichet A, Glotzer JB, Ephrussi A. Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature. 1995 Oct 12;377(6549):524–527. [PubMed]
  • Ruden DM, Sollars V, Wang X, Mori D, Alterman M, Lu X. Membrane fusion proteins are required for oskar mRNA localization in the Drosophila egg chamber. Dev Biol. 2000 Feb 15;218(2):314–325. [PubMed]
  • Theurkauf WE, Smiley S, Wong ML, Alberts BM. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development. 1992 Aug;115(4):923–936. [PubMed]
  • Ruohola H, Bremer KA, Baker D, Swedlow JR, Jan LY, Jan YN. Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell. 1991 Aug 9;66(3):433–449. [PubMed]
  • Tomancak P, Piano F, Riechmann V, Gunsalus KC, Kemphues KJ, Ephrussi A. A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat Cell Biol. 2000 Jul;2(7):458–460. [PubMed]
  • Schüpbach T, Roth S. Dorsoventral patterning in Drosophila oogenesis. Curr Opin Genet Dev. 1994 Aug;4(4):502–507. [PubMed]
  • Ullrich O, Reinsch S, Urbé S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol. 1996 Nov;135(4):913–924. [PMC free article] [PubMed]
  • Urbé S, Huber LA, Zerial M, Tooze SA, Parton RG. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 1993 Nov 15;334(2):175–182. [PubMed]
  • Sipos L, Mihály J, Karch F, Schedl P, Gausz J, Gyurkovics H. Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. Genetics. 1998 Jun;149(2):1031–1050. [PMC free article] [PubMed]
  • Volknandt W, Pevsner J, Elferink LA, Scheller RH. Association of three small GTP-binding proteins with cholinergic synaptic vesicles. FEBS Lett. 1993 Feb 8;317(1-2):53–56. [PubMed]
  • Smith JL, Wilson JE, Macdonald PM. Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos. Cell. 1992 Sep 4;70(5):849–859. [PubMed]
  • Wang C, Lehmann R. Nanos is the localized posterior determinant in Drosophila. Cell. 1991 Aug 23;66(4):637–647. [PubMed]
  • Sonoda J, Wharton RP. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 1999 Oct 15;13(20):2704–2712. [PMC free article] [PubMed]
  • Wang X, Kumar R, Navarre J, Casanova JE, Goldenring JR. Regulation of vesicle trafficking in madin-darby canine kidney cells by Rab11a and Rab25. J Biol Chem. 2000 Sep 15;275(37):29138–29146. [PubMed]
  • St Johnston D, Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. [PubMed]
  • Tetzlaff MT, Jäckle H, Pankratz MJ. Lack of Drosophila cytoskeletal tropomyosin affects head morphogenesis and the accumulation of oskar mRNA required for germ cell formation. EMBO J. 1996 Mar 15;15(6):1247–1254. [PMC free article] [PubMed]
  • Wilson JE, Connell JE, Schlenker JD, Macdonald PM. Novel genetic screen for genes involved in posterior body patterning in Drosophila. Dev Genet. 1996;19(3):199–209. [PubMed]
  • Theurkauf WE, Hazelrigg TI. In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development. 1998 Sep;125(18):3655–3666. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...