The origin of dorsoventral polarity in Drosophila

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 358, Issue 1436, 2003, Pages 1317-1329

  Roth, Siegfried ^a   Edwards, R G ^b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Reproductive BioMedicine Online   (United Kingdom)

Author keywords

Axis formation; Germline soma signalling; mRNA localization; Nuclear movement; Transforming growth factor

Indexed keywords

FLY;

ANIMALIA; DROSOPHILA; HEXAPODA; INSECTA;

EID: 0041353563     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2003.1325     Document Type: Review

References (94)

1. Brendza, R. P., Serbus, L. R., Saxton, W. M. & Duffy, J. B. 2002 Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes. Curr. Biol. 12, 1541-1545.
2. Büning, J. 1994 The insect ovary. London: Chapman & Hall.
3. Casci, T., Vinos, J. & Freeman, M. 1999 Sprouty, an intracellular inhibitor of Ras signaling. Cell 96, 655-665.
4. Cha, B. J., Koppetsch, B. S. & Theurkauf, W. E. 2001 In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106, 35-46.
5. Cha, B. J., Serbus, L. R., Koppetsch, B. S. & Theurkauf, W. E. 2002 Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat. Cell. Biol. 4, 592-598.
6. Chen, G., Handel, K. & Roth, S. 2000 The maternal NF-kappaB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development 127, 5145-5156.
7. Cohen, R. S. 2002 Oocyte patterning: dynein and kinesin, inc. Curr. Biol. 12, R797-R799.
8. DeLotto, Y. & DeLotto, R. 1998 Proteolytic processing of the Drosophila Spatzle protein by easter generates a dimeric NGF-like molecule with ventralising activity. Mech. Dev. 72, 141-148.
9. Dissing, M., Giordano, H. & DeLotto, R. 2001 Autoproteolysis and feedback in a protease cascade directing Drosophila dorsal-ventral cell fate. EMBO J. 20, 2387-2393.
10. Duncan, J. E. & Warrior, R. 2002 The cytoplasmic Dynein and Kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr. Biol. 12, 1982-1991.
11. Ferguson, E. L. 1996 Conservation of dorsal-ventral patterning in arthropods and chordates. Curr. Opin. Genet. Dev. 6, 424-431.
12. Ghiglione, C., Carraway III, K. L., Amundadottir, L. T., Boswell, R. E., Perrimon, N. & Duffy, J. B. 1999 The transmembrane molecule kekkon 1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis. Cell 96, 847-856.
13. Ghiglione, C., Bach, E. A., Paraiso, Y., Carraway III, K. L., Noselli, S. & Perrimon, N. 2002 Mechanism of activation of the Drosophila EGF receptor by the TGFalpha ligand Gurken during oogenesis. Development 129, 175-186.
14. Godt, D. & Tepass, U. 1998 Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387-391.
15. Golembo, M., Schweitzer, R., Freeman, M. & Shilo, B. Z. 1996 Argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122, 223-230.
16. Gonzalez-Reyes, A. & St Johnston, D. 1994 Role of oocyte position in establishment of anterior-posterior polarity in Drosophila. Science 266, 639-642.
17. Gonzalez-Reyes, A. & St Johnston, D. 1998 The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125, 3635-3644.
18. Gonzalez-Reyes, A., Elliott, H. & St Johnston, D. 1995 Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654-658.
19. Gross, S. P., Welte, M. A., Block, S. M. & Wieschaus, E. F. 2002 Coordination of opposite-polarity microtubule motors. J. Cell. Biol. 156, 715-724.
20. Guichard, A., Roark, M., Ronshaugen, M. & Bier, E. 2000 Brother of rhomboid, a rhomboid-related gene expressed during early Drosophila oogenesis, promotes EGF-R/MAPK signaling. Devl Biol. 226, 255-266.
21. Guichet, A., Peri, F. & Roth, S. 2001 Stable anterior anchoring of the oocyte nucleus is required to establish dorsoventral polarity of the Drosophila egg. Devl Biol. 237, 93-106.
22. Gutzeit, H. O. & Sander, K. 1985 Establishment of polarity in the insect egg. San Diego, CA: Academic.
23. Hashimoto, C., Hudson, K. L. & Anderson, K. V. 1988 The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52, 269-279.
24. Hashimoto, C., Gerttula, S. & Anderson, K. V. 1991 Plasma membrane localization of the Toll protein in the syncytial Drosophila embryo: importance of transmembrane signaling for dorsal-ventral pattern formation. Development 111, 1021-1028.
25. Hinton, H. E. 1981 Biology of insect eggs. Oxford: Pergamon.
26. Hoffmann, J. A., Kafatos, F. C., Janeway, C. A. & Ezekowitz, R. A. 1999 Phylogenetic perspective in innate immunity. Science 284, 1313-1318.
27. Holt, R. A. (and 120 others) 2002 The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129-149.
28. James, K. E., Dorman, J. B. & Berg, C. A. 2002 Mosaic analyses reveal the function of Drosophila Ras in embryonic dorsoventral patterning and dorsal follicle cell morphogenesis. Development 129, 2209-2222.
29. Januschke, J., Gervais, L., Dass, S., Kaltschmidt, J. A., Lopez-Schier, H., Johnston, D. S., Brand, A. H., Roth, S. & Guichet, A. 2002 Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr. Biol. 12, 1971-1981.
30. Johnstone, O. & Lasko, P. 2001 Translational regulation and RNA localization in Drosophila oocytes and embryos. A. Rev. Genet. 35, 365-406.
31. Kleine-Schonnefeld, H. & Engels, W. 1981 Symmetrical pattern of follicle arrangement in the ovary of Musca domestica. Zoomorphology 98, 185-190.
32. Koch, E. A. & Spitzer, R. H. 1983 Multiple effects of colchicine on oogenesis in Drosophila: induced sterility and switch of potential oocyte to nurse-cell developmental pathway. Cell Tissue Res. 228, 21-32.
33. Kramer, S., Okabe, M., Hacohen, N., Krasnow, M. A. & Hiromi, Y. 1999 Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126, 2515-2525.
34. Lall, S. & Patel, N. H. 2001 Conservation and divergence in molecular mechanisms of axis formation. A. Rev. Genet. 35, 407-437.
35. Lee, J. R., Urban, S., Garvey, C. F. & Freeman, M. 2001 Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161-171.
36. LeMosy, E. K., Tan, Y. Q. & Hashimoto, C. 2001 Activation of a protease cascade involved in patterning the Drosophila embryo. Proc. Natl Acad. Sci. USA 98, 5055-5060.
37. Li, M.-G., McGrail, M., Serr, M. & Hays, T. S. 1994 Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol. 126, 1475-1494.
38. MacDougall, N., Clark, A., MacDougall, E. & Davis, I. 2003 Drosophila gurken (TGFalpha) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps. Devl Cell 4, 307-319.
39. Maxton-Küchenmeister, J., Handel, K., Schmidt-Ott, U., Roth, S. & Jäckle, H. 1999 Toll homolog expression in the beetle Tribolium suggests a different mode of dorsoventral patterning than in Drosophila embryos. Mech. Dev. 83, 107-114.
40. Meinhardt, H. 1982 Models of biological pattern formation. London: Academic.
41. Micklem, D. R., Dasgupta, R., Elliott, H., Gergely, F., Davidson, C., Brand, A., Gonzalez Reyes, A. & St Johnston, D. 1997 The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr. Biol. 7, 468-478.
42. Mizuguchi, K., Parker, J. S., Blundell, T. L. & Gay, N. J. 1998 Getting knotted: a model for the structure and activation of Spatzle. Trends Biochem. Sci. 23, 239-242.
43. Montell, D. J., Keshishian, H. & Spradling, A. C. 1991 Laser ablation studies of the role of the Drosophila oocyte nucleus in pattern formation. Science 254, 290-293.
44. Morisato, D. 2001 Spatzle regulates the shape of the Dorsal gradient in the Drosophila embryo. Development 128, 2309-2319.
45. Morisato, D. & Anderson, K. V. 1994 The spatzle gene encodes a component of the extracellular signaling pathway establishing the dorsal-ventral pattern of the Drosophila embryo. Cell 76, 677-688.
46. Morisato, D. & Anderson, K. V. 1995 Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. A. Rev. Genet. 29, 371-399.
47. Muresan, V., Stankewich, M. C., Steffen, W., Morrow, J. S., Holzbaur, E. L. & Schnapp, B. J. 2001 Dynactin-dependent, dynein-driven vesicle transport in the absence of membrane proteins: a role for spectrin and acidic phospholipids. Mol. Cell 7, 173-183.
48. Netzel, H. 1965 Über die Übereinstimmung von Polarität und Bilateralsymmetrie in Embryo, Ei, Oocyte und Oocytenkern bei Gryllus domesticus L. Roux' Arch. Entwicklungsmech. 156, 88-95.
49. Netzel, H. 1968 Die Ausprägung von Polarität und Bilateralsymmetrie in den Oocyten von Gryllus domesticus L. Roux' Arch. Entwicklungsmech. 160, 119-166.
50. Neuman-Silberberg, F. S. & Schupbach, T. 1993 The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF-alpha-like protein. Cell 75, 165-174.
51. Neuman-Silberberg, F. S. & Schupbach, T. 1994 Dorsoventral axis formation of Drosophila depends on the correct dosage of the gene gurken. Development 120, 2457-2463.
52. Nilson, L. A. & Schupbach, T. 1998 Localized requirements for windbeutel and pipe reveal a dorsoventral prepattern within the follicular epithelium of the Drosophila ovary. Cell 93, 253-262.
53. Norvell, A., Kelley, R. L., Wehr, K. & Schupbach, T. 1999 Specific isoforms of squid, a Drosophila hnRNP, perform distinct roles in Gurken localization during oogenesis. Genes Dev. 13, 864-876.
54. Pai, L. M., Barcelo, G. & Schüpbach, T. 2000 D-cbl, a negative regulator of the Egfr pathway, is required for dorsoventral patterning in Drosophila oogenesis. Cell 103, 51-61.
55. Palacios, I. M. & Johnston, D. S. 2001 Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. A. Rev. Cell Dev. Biol. 17, 569-614.
56. Patel, N. H., Hayward, D. C., Lall, S., Pirkl, N. R., DiPietro, D. & Ball, E. E. 2001 Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128, 3459-3472.
57. Peri, F., Bökel, C. & Roth, S. 1999 Local Gurken signaling and dynamic MAPK activation during Drosophila oognesis. Mech. Dev. 81, 75-88.
58. Peri, F. & Roth, S. 2000 Combined activities of Gurken and Decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development 127, 841-850.
59. Peri, F., Technau, M. & Roth, S. 2002 Mechanisms of Gurken-dependent pipe regulation and the robustness of dorsoventral patterning in Drosophila. Development 129, 2965-2975.
60. Powers, J. & Barlowe, C. 1998 Transport of axl2p depends on erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product. J. Cell Biol. 142, 1209-1222.
61. Powers, J. & Barlowe, C. 2002 Erv14p directs a transmembrane secretory protein into COPII-coated transport vesicles. Mol. Biol. Cell 13, 880-891.
62. Queenan, A. M., Ghabrial, A. & Schupbach, T. 1997 Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124, 3871-3880.
63. Queenan, A. M., Barcelo, G., Van Buskirk, C. & 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.
64. Reich, A. & Shilo, B. Z. 2002 Keren, a new ligand of the Drosophila epidermal growth factor receptor, undergoes two modes of cleavage. EMBO J. 21, 4287-4296.
65. Reich, A., Sapir, A. & Shilo, B. 1999 Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126, 4139-4147.
66. Riechmann, V. & Ephrussi, A. 2001 Axis formation during Drosophila oogenesis. Curr. Opin. Genet. Dev. 11, 374-383.
67. Roth, S. & Schüpbach, T. 1994 The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120, 2245-2257.
68. Roth, S., Jordan, P. & Karess, R. 1999 Binulcear Drosophila oocytes: consequences and implications for dorsoventral patterning in oogenesis and embryogenesis. Development 126, 927-934.
69. Roth, S., Neuman-Silberberg, F. S., Barcelo, G. & Schupbach, T. 1995 Cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967-978.
70. Sander, K. 1971 Pattern formation in longitudinal halves of leaf hopper eggs (Homoptera) and some remarks on the definition of embryonic regulation. Wilhelm Roux Arch. Entw. Mech. Org. 167, 336-352.
71. Sander, K. 1976 Specification of the basic body pattern in insect embryogenesis. Adv. Insect Physiol. 12, 125-238.
72. Saunders, C. & Cohen, R. 1999 The role of oocyte transcription, the 5′UTR, and translation repression and derepression in Drosophila gurken mRNA and protein localization. Mol. Cell 3, 43-54.
73. Schwalm, F. E. 1988 Insect morphogenesis. Basel: Karger.
74. Schweitzer, R. & Shilo, B. Z. 1997 A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13, 191-196.
75. Schweitzer, R., Howes, R., Smith, R., Shilo, B. Z. & Freeman, M. 1995 Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376, 699-702.
76. Sen, J., Goltz, J. S., Stevens, L. & Stein, D. 1998 Spatially restricted expression of pipe in the Drosophila egg chamber defines embryonic dorsal-ventral polarity. Cell 95, 471-481.
77. Sen, J., Goltz, J. S., Konsolaki, M., Schupbach, T. & Stein, D. 2000 Windbeutel is required for function and correct subcellular localization of the Drosophila patterning protein Pipe. Development 127, 5541-5550.
78. Shmueli, A., Cohen-Gazala, O. & Neuman-Silberberg, F. S. 2002 Gurken, a TGF-alpha-like protein involved in axis determination in Drosophila, directly binds to the EGF-receptor homolog Egfr. Biochem. Biophys. Res. Commun. 291, 732-737.
79. Shvartsman, S. Y., Muratov, C. B. & Lauffenburger, D. A. 2002 Modeling and computational analysis of EGF receptor-mediated cell communication in Drosophila oogenesis. Development 129, 2577-2589.
80. Spradling, A. C. 1993 Developmental genetics of oogenesis. In The development of Drosophila melanogaster, vol. 1 (ed. M. Bate & A. Martinez-Arias), pp. 1-70. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
81. St Johnston, D. & Nusslein-Volhard, C. 1992 The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219.
82. Stathopoulos, A. & Levine, M. 2002 Dorsal gradient networks in the Drosophila embryo. Devl Biol. 246, 57-67.
83. Stauber, M., Prell, A. & Schmidt-Ott, U. 2002 A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc. Natl Acad. Sci. USA 99, 274-279.
84. Steven Wiley, H., Shvartsman, S. Y. & Lauffenburger, D. A. 2003 Computational modeling of the EGF-receptor system: a paradigm for systems biology. Trends Cell Biol. 13, 43-50.
85. Swan, A., Nguyen, T. & Suter, B. 1999 Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat. Cell Biol. 1, 444-449.
86. Theurkauf, W., Smiley, S., Wong, M. & Alberts, B. 1992 Reorganisation of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923-936.
87. Thio, G. L., Ray, R. P., Barcelo, G. & Schupbach, T. 2000 Localization of gurken RNA in Drosophila oogenesis requires elements in the 5′ and 3′ regions of the transcript. Devl Biol. 221, 435-446.
88. Tsruya, R., Schlesinger, A., Reich, A., Gabay, L., Sapir, A. & Shilo, B. Z. 2002 Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev. 16, 222-234.
89. Twombly, V., Blackman, R. K., Jin, H., Graff, J. M., Padgett, R. W. & Gelbart, W. M. 1996 The TGF-beta signaling pathway is essential for Drosophila oogenesis. Development 122, 1555-1565.
90. Urban, S., Lee, J. R. & Freeman, M. 2001 Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173-182.
91. Urban, S., Lee, J. R. & Freeman, M. 2002 A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J. 21, 4277-4286.
92. Van Eeden, F. & St Johnston, D. 1999 The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 9, 396-404.
93. Wasserman, J. & Freeman, M. 1998 An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355-364.
94. Webster, P. J., Suen, J. & Macdonald, P. M. 1994 Drosophila virilis oskar transgenes direct body patterning but not pole cell formation or maintenance of mRNA localization in D. melanogaster. Development 120, 2027-2037.