Role for mRNA localization in translational activation but not spatial restriction of nanos RNA

Development

Volumn 126, Issue 4, 1999, Pages 659-669

  Bergsten, Sherri Evans ^a   Gavis, Elizabeth R ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

3' Untranslated region; Drosophila melanogaster; Nanos; RNA localization; Translational regulation

Indexed keywords

MESSENGER RNA; NUCLEOTIDE; SIGNAL PEPTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE LOCATION; GERM CELL; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; REPRESSOR GENE; RESTRICTION MAPPING; TRANSGENE; TRANSLATION REGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; INSECT PROTEINS; OOGENESIS; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSGENES;

ANIMALIA; DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER;

EID: 0033046510     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Berleth, T., Burri, M., Thoma, G., Bopp, D., Richstein, S., Frigerio, G., Noll, M. and Nüsslein-Volhard, C. (1988). The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 7, 1749-1756.
2. Cheung, H.-K., Serano, T. L. and Cohen, R. S. (1992). Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg. Development 114, 653-661.
3. 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.
4. Clark, I. E., Jan, L. Y. and Jan, Y. N. (1997). Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron, and muscle. Development 124, 461-470.
5. Curtis, D., Apfeld, J. and Lehmann, R. (1995). nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development 121, 1899-1910.
6. Dahanukar, A. and Wharton, R. P. (1996). The Nanos gradient in Drosophila embryos is generated by transiational regulation. Genes Dev. 10, 2610-2620.
7. Deshler, J. O., Highett, M. I. and Schnapp, B. J. (1997). Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276, 1128-1131.
8. Ding, D. and Lipshitz, H. D. (1993). A molecular screen for polar-localized maternal RNAs in the early embryo of Drosophila. Zygote 1, 257-271.
9. Driever, W. and Nüsslein-Volhard, C. (1988). A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93.
10. Driever, W., Thoma, G. and Nüsslein-Volhard, C. (1989). Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340, 363-367.
11. Dubnau, J. and Struhl, G. (1996). RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694-699.
12. Ephrussi, A., Dickinson, L. K. and Lehmann, R. (1991). oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37-50.
13. Ephrussi, A. and Lehmann, R. (1992). Induction of germ cell formation by oskar. Nature 358, 387-392.
14. 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.
15. 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.
16. Gautreau, D., Cote, C. A. and Mowry, K. L. (1997). Two copies of a subelement from the Vg1 RNA localization sequence are sufficient to direct vegetal localization in Xenopus oocytes. Development 124, 5013-5020.
17. Gavis, E. R., Curtis, D. and Lehmann, R. (1996a). Identification of cis-acting sequences that control nanos RNA localization. Dev. Biol. 176, 36-50.
18. Gavis, E. R. and Lehmann, R. (1992). Localization of nanos RNA controls embryonic polarity. Cell 71, 301-313.
19. Gavis, E. R. and Lehmann, R. (1994). Translational regulation of nanos by RNA localization. Nature 369, 315-318.
20. Gavis, E. R., Lunsford, L., Bergsten, S. E. and Lehmann, R. (1996b). A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122, 2791-2800.
21. Glotzer, J. B. and Ephrussi, A. (1996). mRNA localization and the cytoskeleton. Sem. Cell. Dev. Biol. 7, 357-365.
22. 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.
23. Gutzeit, H. O. and Koppa, R. (1982). Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila. J. Embryol. Exp. Morph. 67, 101-111.
24. Hülskamp, M. and Tautz, D. (1991). Gap genes and gradients - the logic behind the gaps. BioEssays 13, 261-268.
25. Kim-Ha, J., Kerr, K. and Macdonald, P. M. (1995). Translational regulation of oskar mRNA by Bruno, an ovarian RNA-hinding protein, is essential. Cell 81, 403-412.
26. Kim-Ha, J., Smith, J. L. and Macdonald, P. M. (1991). oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23-35.
27. Kim-Ha, J., Webster, P. J., Smith, J. L. and Macdonald, P. M. (1993). Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. Development 119, 169-178.
28. 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.
29. Lantz, V., Ambrosio, L. and Schedl, P. (1992). The Drosophila orb gene is predicted to encode sex-specific germline RNA-hinding proteins and has localized transcripts in ovaries and early embryos. Development 115, 75-88.
30. Lantz, V. and Schedl, P. (1994). Multiple cis-acting target sequences are required for orb mRNA localization during Drosophila oogenesis. Mol. Cell. Biol. 14, 2235-2242.
31. 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.
32. Lehmann, R. and Rongo, C. (1993). Germ plasm formation and germ cell determination. Sem. Dev. Biol. 4, 149-159.
33. Lindsley, D. L. and Zimm, G. G. (1992). The genome of Drosophila melanogaster. San Diego: Academic Press.
34. Macdonald, P. M. and Kerr, K. (1997). Redundant RNA recognition events in bicoid mRNA localization. RNA 3, 1413-1420.
35. Macdonald, P. M., Kerr, K., Smith, J. L. and Leask, A. (1993). RNA regulatory element BLE1 directs the early steps of bicoid mRNA localization. Development 118, 1233-1243.
36. Mach, J. M. and Lehmann, R. (1997). An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev. 11, 423-435.
37. Markussen, F.-H., Michon, A.-M., Breitwieser, W. and Ephrussi, A. (1995). Translational control of oskar generates Short OSK. the isoform that induces pole plasm assembly. Development 121, 3723-3732.
38. Micklem, D. R., Dasgupta, R., Elliot, H., Gergely, F., Davidson, C., Brand, A., González-Reyes, A. and St Johnston, D. (1997). The mago nashi gene is required for the polarization of the oocyte and the formation of perpendicular axes in Drosophila. Curr. Biol. 7, 468-478.
39. Mismer, D. and Rubin, G. M. (1987). Analysis of the promoter of the nina E opsin gene in Drosophila melanogaster. Genetics 116, 565-578.
40. Neuman-Silberberg, F. S. and Schüpbach, T. (1993). The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFα-like protein. Cell 75, 165-174.
41. O'Connell, P. and Roshbash, M. (1984). Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 12, 5495-5513.
42. 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.
43. Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W. J. and Jäckle, H. (1996). RNA binding and translational suppression by bicoid. Nature 379, 746-749.
44. Rongo, C., Gavis, E. R. and Lehmann, R. (1995). Localization of oskar RNA regulates oskar translation and requires Oskar protein. Development 121, 2737-2746.
45. Sambrook, J., Fritsch, K. F. and Maniatis, T. (1999). Molecular cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
46. Schüpbach, T. and Wieschaus, E. (1986). Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Wilhelm Roux's Archiv. Dev. Biol. 195, 302-317.
47. Serano, T. L. and Cohen, R. S. (1995). Gratuitous mRNA localization in the Drosophila oocyte. Development 121, 3013-3021.
48. Smibert, C. A., Wilson, J. E., Kerr, K. and Macdonald, P. M. (1996). smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev. 1996, 2600-2609.
49. Spradling, A. C. (1986). P element-mediated transformation. In Drosophila: A Practical Approach. (ed. D. B. Roberts), pp. 175-197. Oxford: IRL Press.
50. Spradling, A. C. (1993). Developmental genetics of oogenesis. In The Development of Drosophila melanogasler vol. I. (ed. M. Bate and A. Martinez Arias), pp. 1-70. Cold Spring Harbor, NY: Cold Spring Harbor Press.
51. St Johnston, D., Driever, W., Berleth, T., Richstein, S. and Nüsslein-Volhard, C. (1989). Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development Suppl. 107, 13-19.
52. Struhl, G., Struhl, K. and Macdonald, P. M. (1989). The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259-1273.
53. Suter, B., Romberg, L. M. and Steward, R. (1989). Bicandal-D, a Drosophila gene involved in developmental asymmetry: Localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains. Genes Dev. 3, 1957-1968.
54. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals a translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
55. Theurkauf, W. E., Alberts, B. M., Jan, Y. N. and Jongens, T. A. (1993). A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169-1180.
56. Theurkauf, W. E., Smiley, S., Wang, 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.
57. Wang, C., Dickinson, L. K. and Lehmann, R. (1994). Genetics of nanos localization in Drosophila. Dev. Dynam. 199, 103-115.
58. Wang, C. and Lehmann, R. (1991). Nanos is the localized posterior determinant in Drosophila. Cell 66, 637-647.
59. Webster, P. J., Liang, L., Berg, C. A., Lasko, P. and Macdonald, P. M. (1997). Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev. 11, 2510-2521.
60. Wharton, R. P. and Struhl, G. (1991). RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67, 955-967.
61. Wieschaus, E. F. and Nüsslein-Volhard, C. (1986). Looking at embryos. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 199-227. Oxford: IRL Press.
62. Zhou, Y. and King, M. L. (1996). RNA transport to the vegetal cortex of Xenopus oocytes. Dev. Biol. 179, 173-183.