Anterior-posterior axis specification in drosophila oocytes: Identification of novel bicoid and oskar mRNA localization factors

Genetics

Volumn 188, Issue 4, 2011, Pages 883-896

  Chang, Chin Wen ^a,b   Nashchekin, Dmitry ^a   Wheatley, Lucy ^a   Irion, Uwe ^c   Dahlgaard, Katja ^d   Montague, Tessa G ^a   Hall, Jacqueline ^a   St Johnston, Daniel ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Taipei Zoo   (Taiwan)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PROTEIN BICOID; PROTEIN OSKAR; UNCLASSIFIED DRUG;

ABDOMEN; ACTIN FILAMENT; ALLELE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTERIOR POSTERIOR AXIS; ARTICLE; CELLULAR DISTRIBUTION; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENETIC COMPLEMENTATION; HEAD; INSECT CELL; MALE; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSGENE;

DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 80051498479     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.129312     Document Type: Article

References (88)

1. Albertson, R., and C. Q. Doe, 2003 Dlg, Scrib and Lgl regulate neuroblast cell size and mitotic spindle asymmetry. Nat. Cell Biol. 5: 166-170.
2. Babu, K., Y. Cai, S. Bahri, X. Yang, and W. Chia, 2004 Roles of Bifocal, Homer, and F-actin in anchoring Oskar to the posterior cortex of Drosophila oocytes. Genes Dev. 18: 138-143.
3. Basto, R., J. Lau, T. Vinogradova, A. Gardiol, C. G. Woods et al., 2006 Flies without centrioles. Cell 125: 1375-1386.
4. Bastock, R., and D. St. Johnston, 2008 Drosophila oogenesis. Curr. Biol. 18: R1082-R1087.
5. Becalska, A. N., and E. R. Gavis, 2009 Lighting up mRNA localization in Drosophila oogenesis. Development 136: 2493-2503.
6. Bellen, H. J., R. W. Levis, G. Liao, Y. He, J. W. Carlson et al., 2004 The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167: 761-781.
7. Berleth, T., M. Burri, G. Thoma, D. Bopp, S. Richstein et al., 1988 The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 7: 1749-1756.
8. Brendza, R., L. Serbus, J. Duffy, and W. Saxton, 2000 A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289: 2120-2122.
9. Broadus, J., S. Fuerstenberg, and C. Q. Doe, 1998 Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391: 792-795.
10. Cha, B., B. Koppetsch, and W. Theurkauf, 2001 In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106: 35-46.
11. Chou, T., and N. Perrimon, 1996 The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144: 1673-1679.
12. Clark, A., C. Meignin, and I. Davis, 2007 A Dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte. Development 134: 1955-1965.
13. Dahlgaard, K., A. A. Raposo, T. Niccoli, and D. St. Johnston, 2007 Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev. Cell 13: 539-553.
14. Emmons, S., H. Phan, J. Calley, W. Chen, B. James et al., 1995 Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus. Genes Dev. 9: 2482-2494.
15. Ephrussi, A., and D. Johnston, 2004 Seeing is believing the bicoid morphogen gradient matures. Cell. 116: 143-152.
16. Ephrussi, A., and R. Lehmann, 1992 Induction of germ cell formation by oskar. Nature 358: 387-392.
17. Ephrussi, A., L. K. Dickinson, and R. Lehmann, 1991 Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66: 37-50.
18. Erben, V., M. Waldhuber, D. Langer, I. Fetka, R. P. Jansen et al., 2008 Asymmetric localization of the adaptor protein Miranda in neuroblasts is achieved by diffusion and sequential interaction of Myosin II and VI. J. Cell Sci. 121: 1403-1414.
19. Ferrandon, D., L. Elphick, C. Nusslein-Volhard, and D. St. Johnston, 1994 Staufen protein associates with the 39UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79: 1221-1232.
20. Fuerstenberg, S., C. Y. Peng, P. Alvarez-Ortiz, T. Hor, and C. Q. Doe, 1998 Identification of Miranda protein domains regulating asymmetric cortical localization, cargo binding, and cortical release. Mol. Cell. Neurosci. 12: 325-339.
21. Gervais, L., C. Sandra, J. Januschke, S. Roth and A. Guichet, 2008 PIP5K-dependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development. 135: 3829-3838.
22. Giansanti, M. G., M. Gatti, and S. Bonaccorsi, 2001 The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 128: 1137-1145.
23. Giansanti, M. G., E. Bucciarelli, S. Bonaccorsi, and M. Gatti, 2008 Drosophila SPD-2 is an essential centriole component required for PCM recruitment and astral-microtubule nucleation. Curr. Biol. 18: 303-309.
24. Gregory, S. L., and N. H. Brown, 1998 Kakapo, a gene required for adhesion between and within cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J. Cell Biol. 143: 1271-1282.
25. Groen, A. C., L. A. Cameron, M. Coughlin, D. T. Miyamoto, T. J. Mitchison et al., 2004 XRHAMM functions in ran-dependent microtubule nucleation and pole formation during anastral spindle assembly. Curr. Biol. 14: 1801-1811.
26. Guichet, A., F. Peri, and S. Roth, 2001 Stable anterior anchoring of the oocyte nucleus is required to establish dorsoventral polarity of the Drosophila egg. Dev. Biol. 237: 93-106.
27. Hachet, O., and A. Ephrussi, 2001 Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr. Biol. 11: 1666-1674.
28. Hachet, O., and A. Ephrussi, 2004 Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428: 959-963.
29. Hofmann, M., C. Fieber, V. Assmann, M. Gottlicher, J. Sleeman et al., 1998 Identification of IHABP, a 95 kDa intracellular hyaluronate binding protein. J. Cell Sci. 111(12): 1673-1684.
30. Ikeshima-Kataoka, H., J. B. Skeath, Y. Nabeshima, C. Q. Doe, and F. Matsuzaki, 1997 Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 390: 625-629.
31. Irion, U., and D. St. Johnston, 2007 Bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445: 554-558.
32. Irion, U., J. Adams, C. Chang, and D. St. Johnston, 2006 Miranda couples oskar mRNA/Staufen complexes to the bicoid mRNA localization pathway. Dev. Biol. 297: 522-533.
33. Jankovics, F., R. Sinka, T. Lukacsovich, and M. Erdelyi, 2002 MOESIN crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr. Biol. 12: 2060-2065.
34. Jenny, A., O. Hachet, P. Závorszky, A. Cyrklaff, M. D. J. Weston et al., 2006 A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 133: 2827-2833.
35. Kim-Ha, J., J. L. Smith, and P. M. Macdonald, 1991 Oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66: 23-35.
36. Kolodziej, P. A., L. Y. Jan, and Y. N. Jan, 1995 Mutations that affect the length, fasciculation, or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron 15: 273-286.
37. Lécuyer, E., H. Yoshida, N. Parthasarathy, C. Alm, T. Babak et al., 2007 Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
38. Luschnig, S., B. Moussian, J. Krauss, I. Desjeux, J. Perkovic et al., 2004 An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics 167: 325-342.
39. Manseau, L. J., and T. Schupbach, 1989 Cappuccino and spire: two unique maternal-effect loci required for both the anteroposterior and dorsoventral patterns of the Drosophila embryo. Genes Dev. 3: 1437-1452.
40. Manseau, L., J. Calley, and H. Phan, 1996 Profilin is required for posterior patterning of the Drosophila oocyte. Development 122: 2109-2116.
41. Marchler-Bauer, A., J. B. Anderson, F. Chitsaz, M. K. Derbyshire, C. DeWeese-Scott et al., 2009 CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37: D205-D210.
42. Martin, S., V. Leclerc, K. Smith-Litiere, and D. St. Johnston, 2003 The identification of novel genes required for Drosophila anteroposterior axis formation in a germline clone screen using GFP-Staufen. Development 130: 4201-4215.
43. Matsuzaki, F., T. Ohshiro, H. Ikeshima-Kataoka, and H. Izumi, 1998 Miranda localizes staufen and prospero asymmetrically in mitotic neuroblasts and epithelial cells in early Drosophila embryogenesis. Development 125: 4089-4098.
44. Maxwell, C. A., J. J. Keats, M. Crainie, X. Sun, T. Yen et al., 2003 RHAMM is a centrosomal protein that interacts with dynein and maintains spindle pole stability. Mol. Biol. Cell 14:2262-2276.
45. Mische, S., M. Li, M. Serr, and T. S. Hays, 2007 Direct observation of regulated ribonucleoprotein transport across the nurse cell/ oocyte boundary. Mol Biol Cell. 18: 2254-2263.
46. Mohr, S., S. Dillon, and R. Boswell, 2001 The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes Dev. 15: 2886-2899.
47. Newmark, P., and R. Boswell, 1994 The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila. Development 120: 1303-1313.
48. Nusslein-Volhard, C., H. G. Frohnhofer, and R. Lehmann, 1987 Determination of anteroposterior polarity in Drosophila. Science 238: 1675-1681.
49. Ohshiro, T., T. Yagami, C. Zhang, and F. Matsuzaki, 2000 Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature 408: 593-596.
50. Palacios, I., D. Gatfield, D. St. Johnston, and E. Izaurralde, 2004 An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427: 753-757.
51. Parks, A. L., K. R. Cook, M. Belvin, N. A. Dompe, R. Fawcett et al., 2004 Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36: 288-292.
52. Peng, C. Y., L. Manning, R. Albertson, and C. Q. Doe, 2000 The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408: 596-600.
53. Polesello, C., I. Delon, P. Valenti, P. Ferrer, and F. Payre, 2002 Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4: 782-789.
54. Presgraves, D. C., 2003 A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955-972.
55. Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond et al., 2002 Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615.
56. Quinlan, M. E., J. E. Heuser, E. Kerkhoff, and R. D. Mullins, 2005 Drosophila Spire is an actin nucleation factor. Nature 433: 382-388.
57. Quinlan, M. E., S. Hilgert, A. Bedrossian, R. D. Mullins, and E. Kerkhoff, 2007 Regulatory interactions between two actin nucleators, Spire and Cappuccino. J. Cell Biol. 179: 117-128.
58. Roper, K., and N. H. Brown, 2004 A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr. Biol. 14: 99-110.
59. Roper, K., S. L. Gregory, and N. H. Brown, 2002 The 'spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci. 115: 4215-4225.
60. Rosales-Nieves, A. E., J. E. Johndrow, L. C. Keller, C. R. Magie, D. M. Pinto-Santini et al., 2006 Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat. Cell Biol. 8: 367-376.
61. Schaefer, M., A. Shevchenko, A. Shevchenko, and J. A. Knoblich, 2000 A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10: 353-362.
62. Schnorrer, F., S. Luschnig, I. Koch, and C. Nusslein-Volhard, 2002 G-Tubulin 37C and g-tubulin ring complex protein 75 are essential for bicoid RNA localization during Drosophila oogenesis. Dev. Cell 3: 685-696.
63. Schuldt, A., J. Adams, C. Davidson, D. Micklem, J. Haseloff et al., 1998 Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12: 1847-1857.
64. Schupbach, T., and E. Wieschaus, 1989 Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121: 101-117.
65. Serbus, L., B. Cha, W. Theurkauf, and W. Saxton, 2005 Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132: 3743-3752.
66. Shen, C. P., L. Y. Jan, and Y. N. Jan, 1997 Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90: 449-458.
67. Shen, C. P., J. A. Knoblich, Y. M. Chan, M. M. Jiang, L. Y. Jan et al., 1998 Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes Dev. 12: 1837-1846.
68. Shiga, Y., and M. Tanaka-Matakatsu, and S. Hayashi, 1996 A nuclear GFP/ beta- galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38: 99-106.
69. Siegrist, S. E., and C. Q. Doe, 2005 Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell 123: 1323-1335.
70. Simon, M. A., 1994 Signal transduction during the development of the Drosophila R7 photoreceptor. Dev. Biol. 166: 431-442.
71. St. Johnston, D., 2002 The art and design of genetic screens: Drosophila melanogaster. Nat. Rev. Genet. 3: 176-188.
72. St. Johnston, D., 2005 Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6: 363-375.
73. St. Johnston, D., W. Driever, T. Berleth, S. Richstein, and C. Nusslein-Volhard, 1989 Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development 107: 13-19.
74. Tanaka, T., and A. Nakamura, 2008 The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development 135: 1107-1117.
75. Van Doren, M., A. L. Williamson, and R. Lehmann, 1998 Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol. 8: 243-246.
76. Vanzo, N., and A. Ephrussi, 2002 Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte. Development 129: 3705-3714.
77. Vanzo, N., A. Oprins, D. Xanthakis, A. Ephrussi, and C. Rabouille, 2007 Stimulation of endocytosis and actin dynamics by Oskar polarizes the Drosophila oocyte. Dev. Cell 12: 543-555.
78. Vogt, N., I. Koch, H. Schwarz, F. Schnorrer, and C. Nusslein-Volhard, 2006 The gammaTuRC components Grip75 and Grip128 have an essential microtubule-anchoring function in the Drosophila germline. Development 133: 3963-3972.
79. Weil, T. T., K. M. Forrest, and E. R. Gavis, 2006 Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev. Cell 11: 251-262.
80. Weil, T. T., R. Parton, I. Davis, and E. R. Gavis, 2008 Changes in bicoid mRNA anchoring highlight conserved mechanisms during the oocyte-to-embryo transition. Curr. Biol. 18: 1055-1061.
81. Weil, T. T., D. Xanthakis, R. Parton, I. Dobbie, C. Rabouille et al., 2010 Distinguishing direct from indirect roles for bicoid mRNA localization factors. Development 137: 169-176.
82. Wellington, A., S. Emmons, B. James, J. Calley, M. Grover et al., 1999 Spire contains actin binding domains and is related to ascidian posterior end mark-5. Development 126: 5267-5274.
83. Wharton, R. P., and G. Struhl, 1991 RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67: 955-967.
84. Yousef, M. S., H. Kamikubo, M. Kataoka, R. Kato, and S. Wakatsuki, 2008 Miranda cargo-binding domain forms an elongated coiledcoil homodimer in solution: implications for asymmetric cell division in Drosophila. Protein Sci. 17: 908-917.
85. Yu, F., X. Morin, Y. Cai, X. Yang, and W. Chia, 2000 Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100: 399-409.
86. Zhang, Y., 2008 I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
87. Zhang, Y., 2009 I-TASSER: fully automated protein structure prediction in CASP8. Proteins 77: 100-113.
88. Zimyanin, V. L., K. Belaya, J. Pecreaux, M. J. Gilchrist, A. Clark et al., 2008 In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134: 843-853.