Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila

Current Biology

Volumn 13, Issue 14, 2003, Pages 1159-1168

  Forrest, Kevin M ^a   Gavis, Elizabeth R ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; DROSOPHILA; HEXAPODA;

EID: 0038376482     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-9822(03)00451-2     Document Type: Article

References (58)

1. Gavis, E.R., and Lehmann, R. (1992). Localization of nanos RNA controls embryonic polarity. Cell 71, 301-313.
2. Wang, C., Dickinson, L.K., and Lehmann, R. (1994). Genetics of nanos localization in Drosophila. Dev. Dyn. 199, 103-115.
3. Gavis, E.R., and Lehmann, R. (1994). Translational regulation of nanos by RNA localization. Nature 369, 315-318.
4. Wang, C., and Lehmann, R. (1991). Nanos is the localized posterior determinant in Drosophila. Cell 66, 637-647.
5. Gavis, E.R., Curtis, D., and Lehmann, R. (1996). Identification of cis-acting sequences that control nanos RNA localization. Dev. Biol. 176, 36-50.
6. Kobayashi, S., Yamada, M., Asaoka, M., and Kitamura, T. (1996). Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380, 708-711.
7. Forbes, A., and Lehmann, R. (1998). Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679-690.
8. Bashirullah, A., Cooperstock, R.L., and Lipshitz, H.D. (1998). RNA localization in development. Annu. Rev. Biochem. 67, 335-394.
9. Dalby, B., and Glover, D.M. (1992). 3′ non-translated sequences in Drosophila cyclin B transcripts direct posterior pole accumulation late in oogenesis and peri-nuclear association in syncytial embryos. Development 115, 989-997.
10. Jongens, T.A., Hay, B., Jan, L.Y., and Jan, Y.N. (1992). The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. Cell 70, 569-584.
11. Nakamura, A., Amikura, R., Mukai, M., Kobayashi, S., and Lasko, P. (1996). Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science 274, 2075-2079.
12. Raff, J.W., Whitfield, W.G.F., and Glover, D.M. (1990). Two distinct mechanisms localise cyclin B transcripts in syncytial Drosophila embryos. Development 110, 1249-1261.
13. Brendza, R.P., Serbus, L.R., Duffy, J.B., and Saxton, W.M. (2000). A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289, 2120-2122.
14. Cha, B.-J., Serbus, L.R., Koppetsch, B.S., and Theurkauf, W.E. (2002). Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat. Cell Biol. 4, 592-598.
15. Palacios, I.M., and St Johnston, D. (2002). Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129, 5473-5485.
16. Januschke, J., Gervais, L., Dass, S., Kaltschmidt, J.A., Lopez-Schier, H., St Johnston, D., Brand, A.H., Roth, S., and Guichet, A. (2002). Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr. Biol. 12, 1971-1981.
17. Duncan, J.E., and Warrior, R. (2002). The cytoplasmic Dynein and Kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr. Biol. 12, 1982-1991.
18. MacDougall, N., Clark, A., MacDougall, E., and Davis, I. (2003). Drosophila gurken (TG Falpha) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps. Dev. Cell 4, 307-319.
19. Theurkauf, W.E., Smiley, S., Wong, M.L., and Alberts, B.M. (1992). Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923-936.
20. Cha, B.J., Koppetsch, B.S., and Theurkauf, W.E. (2001). In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106, 35-46.
21. Pokrywka, N.J., and Stephenson, E.C. (1991). Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 113, 55-66.
22. Pokrywka, N.J., and Stephenson, E.C. (1995). Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167, 363-370.
23. Clark, I., Giniger, E., Ruohola-Baker, H., Jan, L.Y., and Jan, Y.N. (1994). Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4, 289-300.
24. Gutzeit, H.O. (1986). The role of microtubules in the differentiation of ovarian follicles during vitellogenesis in Drosophila. W. Roux's Arch. Dev. Biol. 195, 173-181.
25. Glotzer, J.B., Saffrich, R., Glotzer, M., and Ephrussi, A. (1997). Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Curr. Biol. 7, 326-337.
26. Erdélyi, M., Michon, A.-M., Guichet, A., Glotzer, J.B., and Ephrussi, A. (1995). Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature 377, 524-527.
27. Polesello, C., Delon, I., Valenti, P., Ferrer, P., and Payre, F. (2002). Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4, 782-789.
28. Jankovics, F., Sinka, R., Lukacsovich, T., and Erdelyi, M. (2002). MOESIN crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr. Biol. 12, 2060-2065.
29. Bertrand, E., Chartrand, P., Schaefer, M., Shenoy, S.M., Singer, R.H., and Long, R.M. (1998). Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2, 437-445.
30. Wilkie, G.S., and Davis, I. (2001). Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105, 209-219.
31. Bullock, S.L., and Ish-Horowicz, D. (2001). Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature 414, 611-616.
32. Bergsten, S.E., and Gavis, E.R. (1999). Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development 126, 659-669.
33. Spradling, A.C. (1993). Developmental genetics of oogenesis. In The Development of Drosophila melanogaster, Volume I, M. Bate and A. Martinez Arias, eds. (Cold Spring Harbor: Cold Spring Harbor Press), pp. 1-70.
34. Gutzeit, H.O., and Koppa, R. (1982). Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila. J. Embryol. Exp. Morphol. 67, 101-111.
35. Gutzeit, H.O. (1986). The role of microfilaments in cytoplasmic streaming in Drosophila follicles. J. Cell Sci. 80, 159-169.
36. Theurkauf, W.E. (1994). Premature microtubule-dependent cytoplasmic streaming in cappuccino and spire mutant oocytes. Science 265, 2093-2096.
37. Langford, G. (1995). Actin- and microtubule-dependent organelle motors: interrelationships between the two motility systems. Curr. Opin. Cell Biol. 7, 82-88.
38. Lantz, V.A., Clemens, S.E., and Miller, K.G. (1999). The actin cytoskeleton is required for maintenance of posterior pole plasm components in the Drosophila embryo. Mech. Dev. 85, 111-122.
39. Dahanukar, A., and Wharton, R.P. (1996). The Nanos gradient in Drosophila embryos is generated by translational regulation. Genes Dev. 10, 2610-2620.
40. Kloc, M., Larabell, C., Chan, A.P., and Etkin, L.D. (1998). Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech. Dev. 75, 81-93.
41. MacArthur, H., Bubunenko, M., Houston, D.W., and King, M.L. (1999). Xcat2 RNA is a translationally sequestered germ plasm component in Xenopus. Mech. Dev. 84, 75-88.
42. Kloc, M., Larabell, C., and Etkin, L.D. (1996). Elaboration of the messenger transport organizer pathway for localization of RNA to the vegetal cortex of Xenopus oocytes. Dev. Biol. 180, 119-130.
43. Bally-Cuif, L., Schatz, W.J., and Ho, R.K. (1998). Characterization of the zebrafish Orb/CPEB-ralated RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech. Dev. 77, 31-47.
44. Maegawa, S., Yasuda, K., and Inoue, K. (1999). Maternal mRNA localization of zebrafish DAZ-like gene. Mech. Dev. 81, 223-226.
45. Gavis, E.R., Lunsford, L., Bergsten, S.E., and Lehmann, R. (1996). A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122, 2791-2800.
46. Dalby, B., and Glover, D.M. (1993). Discrete sequence elements control posterior pole accumulation and translational repression of maternal cyclin B RNA in Drosophila. EMBO J. 12, 1219-1227.
47. Bergsten, S.E., Huang, T., Chatterjee, S., and Gavis, E.R. (2001). Recognition and long-range interactions of a minimal nanos RNA localization signal element. Development 128, 427-435.
48. Vanzo, N.F., and Ephrussi, A. (2002). Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte. Development 129, 3705-3714.
49. Warn, R.M., Smith, L., and Warn, A. (1985). Three distinct distributions of F-actin occur during the divisions of polar surface caps to produce pole cells in Drosophila embryos. J. Cell Biol. 100, 1010-1015.
50. Lindsley, D.L., and Zimm, G.G. (1992). The genome of Drosophila melanogaster (San Diego: Academic Press, Inc.).
51. Lehmann, R., and Nüsslein-Volhard, C. (1991). The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112, 679-691.
52. Schüpbach, T., and Wieschaus, E. (1986). Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. W. Roux's Arch. Dev. Biol. 195, 302-317.
53. Schüpbach, T., and Wieschaus, E. (1989). Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121, 101-117.
54. Kelso, R.J., Hudson, A.M., and Cooley, L. (2002). Drosophila Kelch regulates actin organization via Src64-dependent tyrosine phosphorylation. J. Cell Biol. 156, 703-713.
55. Hunter, C., and Wieschaus, E. (2000). Regulated expression of nullo is required for the formation of distinct apical and basal adherens junctions in the Drosophila blastoderm. J. Cell Biol. 150, 391-401.
56. Govind, S., Brennan, L., and Steward, R. (1993). Homeostatic balance between dorsal and cactus proteins in the Drosophila embryos. Development 117, 135-148.
57. Theurkauf, W.E., Baum, H., Bo, J., and Wensink, P.C. (1986). Tissue-specific and constitutive alpha-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl. Acad. Sci. USA 83, 8477-8481.
58. Hay, B., Jan, L.H., and Jan, Y.N. (1990). Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development 109, 425-433.