Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, aubergine, in nuage

Development

Volumn 130, Issue 5, 2003, Pages 859-871

  Findley, Seth D ^a   Tamanaha, Mio ^a   Clegg, Nigel J ^a   Ruohola Baker, Hannele ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Germ plasm; Nuage; Oogenesis

Indexed keywords

DROSOPHILA PROTEIN; GENE PRODUCT; PROTEIN AUBERGINE; PROTEIN MAELSTORM; RNA; RNA HELICASE; UNCLASSIFIED DRUG;

ALLELE; CELL GRANULE; CELL NUCLEUS; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; GENE MUTATION; GERM LINE; INTRACELLULAR TRANSPORT; MOLECULAR EVOLUTION; MORPHOLOGY; NONHUMAN; NUAGE; OVARY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; REVIEW;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE TRIPHOSPHATASES; ALLELES; ANIMALS; CYTOPLASMIC GRANULES; DEAD-BOX RNA HELICASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FATTY ACIDS, UNSATURATED; FEMALE; GERM CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INSECT PROTEINS; OOGENESIS; OVARY; PEPTIDE INITIATION FACTORS; RNA HELICASES; RNA INTERFERENCE;

ANIMALIA; HEXAPODA; SOLANUM MELONGENA;

EID: 0037352528     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00310     Document Type: Review

References (80)

1. Ambros, V. (2001). microRNAs: tiny regulators with great potential. Cell 107, 823-826.
2. Amikura, R., Hanyu, K., Kashikawa, M. and Kobayashi, S. (2001). Tudor protein is essential for the localization of mitochondrial RNAs in polar granules of Drosophila embryos. Mech. Dev. 107, 97-104.
3. Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M. and Gvozdev, V. A. (2001). Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11, 1017-1027.
4. Bardsley, A., McDonald, K. and Boswell, R. E. (1993). Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization. Development 119, 207-219.
5. Bernstein, E., Caudy, A. A., Hammond, S. M. and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366.
6. Billy, E., Brondani, V., Zhang, H., Muller, U. and Filipowicz, W. (2001). Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc. Natl. Acad. Sci. USA 98, 14428-14433.
7. Byers, T. J., Dubreuil, R., Branton, D., Kiehart, D. P. and Goldstein, L. S. (1987). Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J. Cell Biol. 105, 2103-2110.
8. Callebaut, I. and Mornon, J. P. (1997). The human EBNA-2 coactivator p100: multidomain organization and relationship to the staphylococcal nuclease fold and to the tudor protein involved in Drosophila melanogaster development. Biochem. J. 321, 125-132.
9. Carmell, M. A., Xuan, Z., Zhang, M. Q. and Hannon, G. J. (2002). The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733-2742.
10. Carrera, P., Johnstone, O., Nakamura, A., Casanova, J., Jackle, H. and Lasko, P. (2000). VASA mediates translation through interaction with a Drosophila yIF2 homolog. Mol. Cell 5, 181-187.
11. 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.
12. Clegg, N. J., Frost, D. M., Larkin, M. K., Subrahmanyan, L., Bryant, Z. and Ruohola-Baker, H. (1997). maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA. Development 124, 4661-4671.
13. Clegg, N. J., Findley, S. D., Mahowald, A. P. and Ruohola-Baker, H. (2001). Maelstrom is required to position the MTOC in stage 2-6 Drosophila oocytes. Dev. Genes Evol. 211, 44-48.
14. Crittenden, S. L., Bernstein, D. S., Bachorik, J. L., Thompson, B. E., Gallegos, M., Petcherski, A. G., Moulder, G., Barstead, R., Wickens, M. and Kimble, J. (2002). A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417, 660-663.
15. Dreyfuss, G., Kim, V. N. and Kataoka, N. (2002). Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3, 195-205.
16. Eddy, E. M. (1975). Germ plasm and the differentiation of the germ line. Int. Rev. Cytol. 43, 229-281.
17. Fagard, M., Boutet, S., Morel, J. B., Bellini, C. and Vaucheret, H. (2000). AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. USA 97, 11650-11654.
18. Fasken, M., Saunders, R., Rosenberg, M. and Brighty, D. W. (2000). A leptomycin B-sensitive homologue of human CRM1 promotes nuclear export of nuclear export sequence-containing protiens in Drosophila cell. J. Biol. Chem. 275, 1878-1886.
19. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997). CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.
20. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. and Nishida, E. (1997). CRM1 is reponsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311.
21. Ghabrial, A., Ray, R. P. and Schupbach, T. (1998). okra and spindle-B encode components of the RAD52 DNA repair pathway and effect meiosis and patterning in Drosophila oogenesis. Genes Dev 12, 2711-2723.
22. Ghabrial, A. and Schupbach, T. (1999). Activation of a meiotic checkpoint regulate translation of Gurken during Drosophila oogenesis. Nat. Cell Biol. 1, 354-357.
23. Gillespie, D. E. and Berg, C. A. (1995). Homelss is required for RNA localization in Drosophila oogenesis and encodes a new member of the DEH family of RNA-dependent ATPases. Genes Dev 9, 2495-2508.
24. Golumbeki, G.S., Bardsley, A., Tax, F. and Boswell, R.E. (1991). tudor, a posterior-group gene of Drosophila melanogater, encodes a novel protein and an mRNA localized during mid-oogenesis. Genes Dev. 5, 2060-2070.
25. Gonzalez-Reyes, A. (1999). DNA repair and pattern formation come together. Nat. Cell Biol. 1, E150-E-152.
26. Gonzales-Reyes, A., Elliott, H. and St Johnston, D. (1997). Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. Development 124, 4927-4937.
27. Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D. L., Fire, A., Ruvkun, G. and Mello, C. C. (2001). Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans development timing. Cell 106, 23-34.
28. Grosshans, H. and Slack, F.J. (2002). Micro-RNAs: small is plentiful. J. Cell Biol., 156, 17-21.
29. Hamamoto, T., Gunji, S., Tsuji, H. and Beppu, T. (1983). Leptomycins A and B, new antifungal antibiotics. I. Taxonomy of the producing strain and their fermentation, purification and characterization. J. Antibiot. 36, 639-645.
30. Hammond, S. M., Boettchener, S., Caudy, A. A., Kobayashi, R. and Hannon, G. J. (2001). Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293, 1146-1150.
31. Harris, A. N. and Macdonald, P.M. (2001). Aubergine encodes a Drosophila polar granule component requires for pole cell formation and related to eIF2C. Development 128, 2823-2832.
32. Hay, B., Ackeman, L., Barbel, S., Jan, L.Y. and Jan, Y.N. (1988). Idenfitican of a component of Drosophila polar granulkes. Development 103. 625-640.
33. Hay, B., Jan, L. Y. and Jan, Y. N. (1988b). A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55, 577-587.
34. Hutvagner, G., McLachlan, J., Pasquinelli, A. E., Balint, E., Tuschl, T. and Zamore, P. D. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838.
35. Huynh, J. R. and St Johnston, D. (2000). The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 127, 2785-2794.
36. Illmensee, K. and Mahowald, A. P. (1974). Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA 71, 1016-1020.
37. Illmensee, K. and Mahowald, A. P. (1976). The autonomous function of germ plasm in a somatic region of the Drosophila egg. Exp. Cell Res. 97, 127-140.
38. Kataoka, Y., Takeichi, M. and Uemura, T. (2001). Developmental roles and molecular characterization of a Drosophila homologue of Arabidopsis Argonaute1, the founder of a novel gene superfamily. Genes Cells 6, 313-325.
39. Kennerdell, J. R., Yamaguchi, S. and Carthew, R. W. (2002). RNAi is activated during Drosophila oocyte maturation in a manner dependent on aubergine and spindle-E. Genes Dev. 16, 1884-1889.
40. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W. and Tuschl, T. (2002). Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739.
42. Lasko, P. F. and Ashburner, M. (1988). The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611-617.
43. Lasko, P. F. and Ashburner, M. (1990). Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 4, 905-921.
44. Li, M., McGrail, M., Serr, M. and Hays, T. S. (1994). Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol. 126, 1475-1494.
45. Liang, L., Diehl-Jones, W. and Lasko, P. (1994). Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120, 1201-1211.
46. Mahowald, A. P. (1968). Polar granules of Drosophila. II. Ultrastructural changes during early embryogenesis. J. Exp. Zool. 167, 237-261.
47. Mahowald, A. P. (1971a). Polar granules of Drosophila. III. The continuity of polar granules during the life cycle of Drosophila. J. Exp. Zool. 176, 329-343.
48. Mahowald, A. P. (1971b). Origin and continuity of polar granules. In Origin and Continuity of Cell Organelles (ed. J. Reinert and H. Ursprung), pp. 159-169. New York: Springer-Verlag.
49. Mahowald, A. P. (2001). Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 203, 187-213.
50. Mahowald, A. P. and Strasshein, J. M. (1970). Intercellular migration of centrioles in the germarium of Drosophila melanogaster. An electron microscopic study. J. Cell Biol. 45, 306-320.
51. McKim, K. S. and Hayashi-Hagihara, A. (1998). mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 12, 2932-2942.
52. Nakamura, A., Amikura, R., Hanyu, K. and Kobayashi, S. (2001). Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128, 3233-3242.
53. Page, S. L. and Hawley, R. S. (2001). c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 15, 3130-3143.
54. Pare, C. and Suter, B. (2000). Subcellular localization of Bic-D::GFP is linked to an asymmetric oocyte nucleus. J. Cell Sci. 113, 2119-2127.
55. Ponting, C. P. (1997). Tudor domains in proteins that interact with RNA. Trends Biochem. Sci. 22, 51-52.
56. Queenan, A. M., Barcelo, G., van Buskirk, C. and Schupbach, T. (1999). The transmembrane region of Gurken is not required for biological activity, but is necessary for transport to the oocyte membrane in Drosophila. Mech. Dev. 89, 35-42.
57. Ray, R. P. and Schupbach, T. (1996). Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev. 10, 1711-1723.
58. Raz, E. (2000). The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, 1017.1-1017.6.
59. Riechmann, V. and Ephrussi, A. (2001). Axis formation during Drosophila oogenesis. Curr. Opin. Genet. Dev. 11, 374-383.
60. Rongo, C. and Lehmann, R. (1996). Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet. 12, 102-109.
61. Saffman, E. E. and Lasko, P. (1999). Germline development in vertebrates and invertebrates. Cell Mol. Life Sci. 55, 1141-1163.
62. Schupbach, T. and Wieschaus, E. (1991). Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119-1136.
63. Selenko, P., Sprangers, R., Stier, G., Buhler, D., Fischer, U. and Sattler, M. (2001). SMN tudor domain structure and its interaction with the Sm proteins. Nat. Struct. Biol. 8, 27-31.
64. Shatkin, A. J. and Manley, J. L. (2000). The ends of the affair: capping and polyadenylation. Nat. Struct. Biol. 7, 838-842.
65. Smith, P. A. and King, R. C. (1968). Genetic control of synaptonemal complexes in Drosophila melanogaster. Genetics 60, 335-351.
66. Stade, K., Ford, C. S., Guthrie, C. and Weis, K. (1997). Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90, 1041-1050.
67. Stapleton, W., Das, S. and McKee, B. D. (2001). A role of the Drosophila homeless gene in repression of Stellate in male meiosis. Chromosoma 110, 228-240.
68. Stuurman, N., Maus, N. and Fisher, P. A. (1995). Interphase phosphorylation of the Drosophila nuclear lamin: site- mapping using a monoclonal antibody. J. Cell Sci. 108, 3137-3144.
69. Styhler, S., Nakamura, A., Swan, A., Suter, B. and Lasko, P. (1998). vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125, 1569-1578.
70. Suter, B. and Steward, R. (1991). Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation. Cell 67, 917-926.
71. Tanner, N. K. and Linder, P. (2001). DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell 8, 251-262.
72. Tearle, R. and Nüsslein-Volhard, C. (1987). Tübingen mutants stocklist. Drosophila Inf. Serv. 66, 209-226.
73. Theurkauf, W. E. and Hazelrigg, T. I. (1998). In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development 125, 3655-3666.
74. Tomancak, P., Guichet, A., Zavorszky, P. and Ephrussi, A. (1998). Oocyte polarity depends on regulation of gurken by Vasa. Development 125, 1723-1732.
75. Wharton, R. P., Sonoda, J., Lee, T., Patterson, M. and Murata, Y. (1998). The Pumilio RNA-binding domain is also a translational regulator. Mol. Cell 1, 863-872.
76. Wilhelm, J. E., Mansfield, J., Hom-Booher, N., Wang, S., Turck, C. W., Hazelrigg, T. and Vale, R. D. (2000). Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes. J. Cell Biol. 148, 427-440.
77. Williams, R. W. and Rubin, G. M. (2002). ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos. Proc. Natl. Acad. Sci. USA 99, 6889-6894.
78. Wilsch-Brauninger, M., Schwarz, H. and Nusslein-Volhard, C. (1997). A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J. Cell Biol. 139, 817-829.
79. Wilson, J. E., Connell, J. E. and Macdonald, P. M. (1996). aubergine enhances oskar translation in the Drosophila ovary. Development 122, 1631-1639.
80. Zaccai, M. and Lipshitz, H. D. (1996). Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4, 159-166.