Bazooka is required for polarisation of the Drosophila anterior-posterior axis

Development

Volumn 137, Issue 10, 2010, Pages 1765-1773

  Doerflinger, Hélène ^a   Vogt, Nina ^b,c   Torres, Isabel L ^a,d   Mirouse, Vincent ^a,e   Koch, Iris ^b   Nüsslein Volhard, Christiane ^b   St Johnston, Daniel ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c NEW YORK UNIVERSITY   (United States)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Axis formation; Drosophila; Lgl; Oogenesis; Par 1; Par 6; Polarity

Indexed keywords

PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3;

ANIMAL TISSUE; ARTICLE; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO POLARITY; ENZYME PHOSPHORYLATION; GENE IDENTIFICATION; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CELL NUCLEUS; CELL POLARITY; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROTUBULES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; TISSUE DISTRIBUTION; TUMOR SUPPRESSOR PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 77952215397     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.045807     Document Type: Article

References (68)

1. Bastock, R. and St Johnston, D. (2008). Drosophila oogenesis. Curr. Biol. 18, R1082-R1087.
2. Benton, R. and St Johnston, D. (2003a). A conserved oligomerization domain in drosophila Bazooka/PAR-3 is important for apical localization and epithelial polarity. Curr. Biol. 13, 1330-1334.
3. Benton, R. and St Johnston, D. (2003b). Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115, 691-704.
4. Benton, R., Palacios, I. M. and St Johnston, D. (2002). Drosophila 14-3-3/PAR-5 is an essential mediator of PAR-1 function in axis formation. Dev. Cell 3, 659-671.
5. 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. 22, 22.
6. Cheeks, R. J., Canman, J. C., Gabriel, W. N., Meyer, N., Strome, S. and Goldstein, B. (2004). C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Curr. Biol. 14, 851-862.
7. Chou, T. B. and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643-653.
8. 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.
9. Clark, I., 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.
10. Cowan, C. R. and Hyman, A. A. (2007). Acto-myosin reorganization and PAR polarity in C. elegans. Development 134, 1035-1043.
11. Cox, D. N., Lu, B., Sun, T., Williams, L. T. and Jan, Y. N. (2001a). Drosophila par-1 is required for oocyte differentiation and microtubule organization. Curr. Biol. 11, 75-87.
12. Cox, D. N., Seyfried, S. A., Jan, L. Y. and Jan, Y. N. (2001b). Bazooka and atypical protein kinase C are required to regulate oocyte differentiation in the Drosophila ovary. Proc. Natl. Acad. Sci. USA 98, 14475-14480.
13. Cuenca, A. A., Schetter, A., Aceto, D., Kemphues, K. and Seydoux, G. (2003). Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130, 1255-1265.
14. Djiane, A., Yogev, S. and Mlodzik, M. (2005). The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell 121, 621-631.
15. Doerflinger, H., Benton, R., Shulman, J. M. and St Johnston, D. (2003). The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium. Development 130, 3965-3975.
16. Doerflinger, H., Benton, R., Torres, I. L., Zwart, M. F. and St Johnston, D. (2006). Drosophila anterior-posterior polarity requires actin-dependent PAR-1 recruitment to the oocyte posterior. Curr. Biol. 16, 1090-1095.
17. Eberl, D. F. and Hilliker, A. J. (1988). Characterization of X-linked recessive lethal mutations affecting embryonic morphogenesis in Drosophila melanogaster. Genetics 118, 109-120.
18. 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.
19. Goldstein, B. and Hird, S. N. (1996). Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467-1474.
20. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
21. Gonczy, P. and Rose, L. S. (2005). Asymmetric cell division and axis formation in the embryo. WormBook 1-20. http://www.wormbook.org.
22. González-Reyes, A. and St Johnston, D. (1998). Patterning of the follicle cell layer along the anterior-posterior axis during Drosophila oogenesis. Development 125, 2837-2846.
23. Gonzalez-Reyes, A., Elliott, H. and St Johnston, D. (1995). Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654-658.
24. Hao, Y., Boyd, L. and Seydoux, G. (2006). Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell 10, 199-208.
25. Hurov, J. B., Watkins, J. L. and Piwnica-Worms, H. (2004). Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14, 736-741.
26. Huynh, J. 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.
27. Huynh, J., Petronczki, M., Knoblich, J. A. and Johnston, D. S. (2001a). Bazooka and PAR-6 are required with PAR-1 for the maintenance of oocyte fate in Drosophila. Curr. Biol. 11, 901-906.
28. Huynh, J. R., Shulman, J. M., Benton, R. and St Johnston, D. (2001b). PAR-1 is required for the maintenance of oocyte fate in Drosophila. Development 128, 1201-1209.
29. Januschke, J., Gervais, L., Gillet, L., Keryer, G., Bornens, M. and Guichet, A. (2006). The centrosome-nucleus complex and microtubule organization in the Drosophila oocyte. Development 133, 129-139.
30. Kim, S., Gailite, I., Moussian, B., Luschnig, S., Goette, M., Fricke, K., Honemann-Capito, M., Grubmuller, H. and Wodarz, A. (2009). Kinaseactivity- independent functions of atypical protein kinase C in Drosophila. J. Cell Sci. 122, 3759-3771.
31. 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.
32. Kuchinke, U., Grawe, F. and Knust, E. (1998). Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 8, 1357-1365.
33. Lane, M. E. and Kalderon, D. (1994). RNA localization along the anteroposterior axis of the Drosophila oocyte requires PKA-mediated signal transduction to direct normal microtubule organization. Genes Dev. 8, 2986-2995.
34. Li, Q., Xin, T., Chen, W., Zhu, M. and Li, M. (2008). Lethal(2)giant larvae is required in the follicle cells for formation of the initial AP asymmetry and the oocyte polarity during Drosophila oogenesis. Cell Res. 18, 372-384.
35. Lighthouse, D. V., Buszczak, M. and Spradling, A. C. (2008). New components of the Drosophila fusome suggest it plays novel roles in signaling and transport. Dev. Biol. 317, 59-71.
36. Lin, D., Edwards, A. S., Fawcett, J. P., Mbamalu, G., Scott, J. D. and Pawson, T. (2000). A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2, 540-547.
37. Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G. et al. (2004). LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843.
38. Luschnig, S., Moussian, B., Krauss, J., Desjeux, I., Perkovic, J. and Nüsslein-Volhard, C. (2004). An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics 167, 325-342.
39. Martin, S. G. and St Johnston, D. (2003). A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421, 379-384.
40. Morais de Sa, E., Mirouse, V. and St Johnston, D. (2010). aPKC phosphorylation of Bazooka defines the apical/lateral border in Drosophila epithelial cells. Cell (in press).
41. Muller, H. A. and Wieschaus, E. (1996). armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149-163.
42. Munro, E., Nance, J. and Priess, J. R. (2004). Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 7, 413-424. (Pubitemid 39232976)
43. Nagai-Tamai, Y., Mizuno, K., Hirose, T., Suzuki, A. and Ohno, S. (2002). Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7, 1161-1171. (Pubitemid 35256337)
44. Neuman-Silberberg, F. and Schüpbach, T. (1993). The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFalike protein. Cell 75, 165-174. (Pubitemid 23306030)
45. 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.
46. Pinheiro, E. M. and Montell, D. J. (2004). Requirement for Par-6 and Bazooka in Drosophila border cell migration. Development 131, 5243-5251.
47. Riechmann, V. and Ephrussi, A. (2004). Par-1 regulates bicoid mRNA localisation by phosphorylating Exuperantia. Development 131, 5897-5907.
48. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
49. Roth, S., Neuman-Silberberg, F. S., Barcelo, G. and 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.
50. Ruohola, H., Bremer, K. A., Baker, D., Swedlow, J. R., Jan, L. Y. and Jan, Y. N. (1991). Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66, 433-449.
51. Schnorrer, F., Luschnig, S., Koch, I. and Nüsslein-Volhard, C. (2002). gamma-Tubulin37C and gamma-tubulin ring complex protein 75 are essential for bicoid RNA localization during Drosophila oogenesis. Dev. Cell 3, 685-696.
52. Shulman, J. M., Benton, R. and St Johnston, D. (2000). The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localisation to the posterior pole. Cell 101, 377-388.
53. Spradling, A. (1993). Developmental genetics of oogenesis. In The Development of Drosophila melanogaster, vol.1 (ed. M. Bate and A. Martinez-Arias), pp. 1-70. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory press.
54. St Johnston, D. (2005). Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6, 363-375.
55. St Johnston, D., Beuchle, D. and Nüsslein-Volhard, C. (1991). Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63.
56. Sung, H., Telley, I., Papadaki, P., Ephrussi, A., Surrey, T. and Rorth, P. (2008). Drosophila Ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev. Cell 15, 866-876.
57. Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N. et al. (2004). aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435.
58. 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.
59. 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.
60. Tian, A. G. and Deng, W. M. (2008). Lgl and its phosphorylation by aPKC regulate oocyte polarity formation in Drosophila. Development 135, 463-471.
61. Tian, A. G. and Deng, W. M. (2009). Par-1 and Tau regulate the anterior-posterior gradient of microtubules in Drosophila oocytes. Dev. Biol. 327, 458-464.
62. Tomancak, P., Piano, F., Riechmann, V., Gunsalus, K. C., Kemphues, K. J. and Ephrussi, A. (2000). A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat. Cell Biol. 2, 458-460.
63. von Stein, W., Ramrath, A., Grimm, A., Müller-Borg, M. and Wodarz, A. (2005). Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132, 1675-1686.
64. Wei, S. Y., Escudero, L. M., Yu, F., Chang, L. H., Chen, L. Y., Ho, Y. H., Lin, C. M., Chou, C. S., Chia, W., Modolell, J. et al. (2005). Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev. Cell 8, 493-504.
65. Wirtz-Peitz, F., Nishimura, T. and Knoblich, J. A. (2008). Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135, 161-173.
66. Wodarz, A. (2002). Establishing cell polarity in development. Nat. Cell Biol. 4, E39-E44.
67. Wodarz, A., Ramrath, A., Kuchinke, U. and Knust, E. (1999). Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402, 544-547.
68. Zimyanin, V. L., Belaya, K., Pecreaux, J., Gilchrist, M. J., Clark, A., Davis, I. and St Johnston, D. (2008). In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134, 843-853.