Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling

Development

Volumn 132, Issue 7, 2005, Pages 1675-1686

  von Stein, Walter ^a,b   Ramrath, Andreas ^b   Grimm, Alexandra ^b,c   Müller Borg, Marion ^b   Wodarz, Andreas ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Actin cytoskeleton; Cell polarity; Drosophila; PAR proteins; PTEN

Indexed keywords

ACTIN; CELL PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE C; PROTEIN OSKAR; PROTEINASE ACTIVATED RECEPTOR 3; UNCLASSIFIED DRUG; VASA PROTEIN;

ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BLASTODERM; CELL DIVISION; CELL MUTANT; CELL NUCLEUS; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOSKELETON; DEVELOPMENTAL STAGE; EGG LAYING; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENZYME ACTIVITY; EPITHELIUM; GERM CELL; GERMPLASM; IN VITRO STUDY; IN VIVO STUDY; MUTANT; NEUROBLAST; NONHUMAN; OOCYTE CLEAVAGE; OVARY; PHENOTYPE; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYNCYTIUM;

ACTINS; ANIMALS; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIUM; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; OOCYTES; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN KINASE C; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 17744386543     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01720     Document Type: Article

References (81)

1. Bilder, D., Schober, M. and Perrimon, N. (2003). Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5, 53-58.
2. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
3. Broadus, J. and Doe, C. Q. (1997). Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr. Biol. 7, 827-835.
4. Cai, Y., Yu, F., Lin, S., Chia, W. and Yang, X. (2003). Apical complex genes control mitotic spindle geometry and relative size of daughter cells in drosophila neuroblast and pI asymmetric divisions. Cell 112, 51-62.
5. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development of Drosophila melanogaster. Berlin, Heidelberg: Springer-Verlag.
6. Caroni, P. (2001). New EMBO members' review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts. EMBO J. 20, 4332-4336.
7. Chou, M. M., Hou, W., Johnson, J., Graham, L. K., Lee, M. H., Chen, C. S., Newton, A. C., Schaffhausen, B. S. and Toker, A. (1998). Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr. Biol. 8, 1069-1077.
8. 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.
9. Czech, M. P. (2000). PIP2 and PIP3: complex roles at the cell surface. Cell 100, 603-606.
10. Doe, C. Q. and Bowerman, B. (2001). Asymmetric cell division: fly neuroblast meets worm zygote. Curr. Opin. Cell Biol. 13, 68-75.
11. Erdelyi, 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.
12. Foe, V. E. and Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61, 31-70.
13. Funamoto, S., Meili, R., Lee, S., Parry, L. and Firtel, R. A. (2002). Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109, 611-623.
14. Gao, X., Neufeld, T. P. and Pan, D. (2000). Drosophila PTEN regulates cell growth and proliferation through PI3K- dependent and -independent pathways. Dev. Biol. 221, 404-418.
15. Goberdhan, D. C., Paricio, N., Goodman, E. C., Mlodzik, M. and Wilson, C. (1999). Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. Genes Dev. 13, 3244-3258.
16. Gray, A., van Der Kaay, J. and Downes, C. P. (1999). The pleckstrin homology domains of protein kinase B and GRP1 (general receptor for phosphoinositides-1) are sensitive and selective probes for the cellular detection of phosphatidylinositol 3,4-bisphosphate and/or phosphatidylinositol 3,4,5-trisphosphate in vivo. Biochem. J. 344, 929-936.
17. Hatanaka, K. and Okada, M. (1991). Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment. Development 111, 909-920.
18. Hay, B., Ackerman, L., Barbel, S., Jan, L. Y. and Jan, Y. N. (1988). Identification of a component of Drosophila polar granules. Development 103, 625-640.
19. Hirose, T., Izumi, Y., Nagashima, Y., Tamai-Nagai, Y., Kurihara, H., Sakai, T., Suzuki, Y., Yamanaka, T., Suzuki, A., Mizuno, K. et al. (2002). Involvement of ASIP/PAR-3 in the promotion of epithelial tight junction formation. J. Cell Sci. 115, 2485-2495.
20. Huang, H., Potter, C. J., Tao, W., Li, D. M., Brogiolo, W., Hafen, E., Sun, H. and Xu, T. (1999). PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126, 5365-5372.
21. Hutterer, A., Betschinger, J., Petronczki, M. and Knoblich, J. A. (2004). Sequential roles of Cdc42, Par-6, aPKC, and Lg1 in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 6, 845-854.
22. Huynh, J. R., Petronczki, M., Knoblich, J. A. and St Johnston, D. (2001). Bazooka and PAR-6 are required with PAR-1 for the maintenance of oocyte fate in Drosophila. Curr. Biol. 11, 901-906.
23. Iijima, M. and Devreotes, P. (2002). Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109, 599-610.
24. Jiang, H., Guo, W., Liang, X. and Rao, Y. (2005). Both the establishment and the maintenance of neuronal polarity require active mechanisms; critical roles of GSK-3β and its upstream regulators. Cell 120, 123-135.
25. Joberty, G., Petersen, C., Gao, L. and Macara, I. G. (2000). The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2, 531-539.
26. Johansson, A., Driessens, M. and Aspenstrom, P. (2000). The mammalian homologue of the caenorhabditis elegans polarity protein PAR-6 is a binding partner for the Rho GTPases Cdc42 and Rac1. J. Cell Sci. 113, 3267-3275.
27. Kemphues, K. (2000). PARsing embryonic polarity. Cell 101, 345-348.
28. Kemphues, K. J., Priess, J. R., Morton, D. G. and Cheng, N. S. (1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311-320.
29. Knoblich, J. A., Jan, L. Y. and Jan, Y. N. (1997). The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc. Natl. Acad. Sci. USA 94, 13005-13010.
30. Kotelevets, L., van Hengel, J., Bruyneel, E., Mareel, M., van Roy, F. and Chastre, E. (2005). Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J. 19, 115-117.
31. Lantz, V. A., Clemens, S. E. and Miller, K. G. (1999). The actin cytoskeleton is required for maintenance of posterior pole plasm components in the Drosophila embryo. Mech. Dev. 85, 111-122.
32. 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.
33. Le Good, J. A., Ziegler, W. H., Parekh, D. B., Alessi, D. R., Cohen, P. and Parker, P. J. (1998). Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281, 2042-2045.
34. Leslie, N. R. and Downes, C. P. (2002). PTEN: The down side of PI 3-kinase signalling. Cell Signal 14, 285-295.
35. Leslie, N. R., Gray, A., Pass, I., Orchiston, E. A. and Downes, C. P. (2000). Analysis of the cellular functions of PTEN using catalytic domain and C-terminal mutations: differential effects of C-terminal deletion on signalling pathways downstream of phosphoinositide 3-kinase. Biochem. J. 346, 827-833.
36. Leslie, N. R., Bennett, D., Gray, A., Pass, I., Hoang-Xuan, K. and Downes, C. P. (2001). Targeting mutants of PTEN reveal distinct subsets of tumour suppressor functions. Biochem. J. 357, 427-435.
37. Liliental, J., Moon, S. Y., Lesche, R., Mamillapalli, R., Li, D., Zheng, Y., Sun, H. and Wu, H. (2000). Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr. Biol. 10, 401-404.
38. 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.
39. Millard, T. H., Sharp, S. J. and Machesky, L. M. (2004). Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem. J. 380, 1-17.
40. Müller, 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.
41. Ohno, S. (2001). Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 13 641-348.
42. Oldham, S., Stocker, H., Laffargue, M., Wittwer, F., Wymann, M. and Hafen, E. (2002). The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP(3) levels. Development 129, 4103-4109.
43. Pellettieri, J. and Seydoux, G. (2002). Anterior-posterior polarity in C. elegans and Drosophila-PARallels and differences. Science 298, 1946-1950.
44. Petronczki, M. and Knoblich, J. A. (2001). DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat. Cell Biol. 3, 43-49.
45. Pollard, T. D., Blanchoin, L. and Mullins, R. D. (2000). Molecular mechanisms controlling actin filament dynamics in nonmusele cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545-576.
46. Qiu, R. G., Abo, A. and Martin, G. S. (2000). A human homolog of the C. elegans polarity determinant par-6 links rac and cdc42 to PKCzeta signaling and cell transformation. Curr. Biol. 10, 697-707.
47. Radimerski, T., Montague, J., Rintelen, F., Stocker, H., van Der Kaay, J., Downes, C. P., Hafen, E. and Thomas, G. (2002). dS6K-regulated cell growth is dPKB/dPI(3)K-independent, but requires dPDK1. Nat. Cell Biol. 4, 251-255.
48. Robinson, D. N. and Cooley, L. (1997). Genetic analysis of the actin cytoskeleton in the Drosophila ovary. Annu. Rev. Cell Dev. Biol. 13, 147-170.
49. Rolls, M. M., Albertson, R., Shih, H. P., Lee, C. Y. and Doe, C. Q. (2003). Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J. Cell Biol. 163 1089-1098.
50. Rongo, C. and Lehmann, R. (1996). Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet. 12, 102-109.
51. Scanga, S. E., Ruel, L., Binari, R. C., Snow, B., Stambolic, V., Bouchard, D., Peters, M., Calvieri, B., Mak, T. W., Woodgett, J. R. et al. (2000). The conserved PI3′K/PTEN/Akt signaling pathway regulates both cell size and survival in Drosophila. Oncogene 19, 3971-3977.
52. Schober, M., Schaefer, M. and Knoblich, J. A. (1999). Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402, 548-551.
53. Servant, G., Weiner, O. D., Herzmark, P., Balla, T., Sedat, J. W. and Bourne, H. R. (2000). Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287, 1037-1040.
54. Shi, S. H., Jan, L. Y. and Jan, Y. N. (2003). Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112, 63-75.
55. Smith, A., Smith, A., Alrubaie, S., Coehlo, C., Leevers, S. J. and Ashworth, A. (1999). Alternative splicing of the Drosophila PTEN gene. Biochim. Biophys. Acta 1447, 313-317.
56. Songyang, Z., Fanning, A. S., Fu, C., Xu, J., Marfatia, S. M., Chishti, A. H., Crompton, A., Chan, A. C., Anderson, J. M. and Cantley, L. C. (1997). Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77.
57. Spradling, A. C. (1993). Developmental generics of oogenesis. In The Development of Drosophila melanogaster, Vol. 1 (ed. M. Bate and A. Martinez-Arias), pp. 1-70. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
58. St Johnston, D., Beuchle, D. and Nusslein-Volhard, C. (1991). Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63.
59. Stambolic, V., Suzuki, A., de la Pompa, J. L., Brothers, G. M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J. M., Siderovski, D. P. and Mak, T. W. (1998). Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95, 29-39.
60. Standaert, M. L., Bandyopadhyay, G., Kanoh, Y., Sajan, M. P. and Farese, R. V. (2001). Insulin and PIP3 activate PKC-zeta by mechanisms that are both dependent and independent of phosphorylation of activation loop (T410) and autophosphorylation (T560) sites. Biochemistry 40, 249-255.
61. Stocker, H. and Hafen, E. (2000). Genetic control of cell size. Curr. Opin. Genet. Dev. 10, 529-535.
62. Stocker, H., Andjelkovic, M., Oldham, S., Laffargue, M., Wymann, M. P., Hemmings, B. A. and Hafen, E. (2002). Living with lethal PIP3 levels: viability of flies lacking PTEN restored by a PH domain mutation in Akt/PKB. Science 295, 2088-2091.
63. Suzuki, A., Yamanaka, T., Hirose, T., Manabe, N., Mizuno, K., Shimizu, M., Akimoto, K., Izumi, Y., Ohnishi, T. and Ohno, S. (2001). Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J. Cell Biol. 152, 1183-1196.
64. Tanentzapf, G. and Tepass, U. (2003). Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5, 46-52.
65. Tetzlaff, M. T., Jackle, H. and Pankratz, M. J. (1996). Lack of Drosophila cytoskeletal tropomyosin affects head morphogenesis and the accumulation of oskar mRNA required for germ cell formation. EMBO J. 15, 1247-1254.
66. Tomancak, P., Guichet, A., Zavorszky, P. and Ephrussi, A. (1998). Oocyte polarity depends on regulation of gurken by Vasa. Development 125, 1723-1732.
67. Varnai, P. and Balla, T. (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510.
68. von Dassow, G. and Schubiger, G. (1994). How an actin network might cause fountain streaming and nuclear migration in the syncytial Drosophila embryo. J. Cell Biol. 127, 1637-1653.
69. Wallenfang, M. R. and Seydoux, G. (2000). Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408, 89-92.
70. Wang, F., Herzmark, P., Weiner, O. D., Srinivasan, S., Servant, G. and Bourne, H. R. (2002). Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat. Cell Biol. 4, 513-518.
71. Wheatley, S., Kulkarni, S. and Karess, R. (1995). Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937-1946.
72. Wodarz, A. (2002). Establishing cell polarity in development. Nat. Cell Biol. 4, E39-E44.
73. Wodarz, A. and Huttner, W. B. (2003). Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech. Dev. 120, 1297-1309.
74. 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.
75. Wodarz, A., Ramrath, A., Grimm, A. and Knust, E. (2000). Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150, 1361-1374.
76. Wu, X., Hepner, K., Castelino-Prabhu, S., Do, D., Kaye, M. B., Yuan, X. J., Wood, J., Ross, C., Sawyers, C. L. and Whang, Y. E. (2000a). Evidence for regulation of the PTEN tumor suppressor by a membrane-localized multi-PDZ domain containing scaffold protein MAGI-2. Proc. Natl. Acad. Sci. USA 97, 4233-4238.
77. Wu, Y., Dowbenko, D., Spencer, S., Laura, R., Lee, J., Go, Q. and Lasky, L. A. (2000b). Interaction of the tumor suppressor PTEN/MMAC with a PDZ domain of MAGI3, a novel membrane-associated guanylate kinase. J. Biol. Chem. 275, 21477-21485.
78. Yamanaka, T., Horikoshi, Y., Suzuki, A., Sugiyama, Y., Kitamura, K., Maniwa, R., Nagai, Y., Yamashita, A., Hirose, T., Ishikawa, H. et al. (2001). PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 6, 721-731.
79. Yin, H. L. and Janmey, P. A. (2003). Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789.
80. Yohn, C. B., Pusateri, L., Barbosa, V. and Lehmann, R. (2003). I(3)malignant brain tumor and three novel genes are required for Drosophila germ-cell formation. Genetics 165, 1889-1900.
81. Zheng, Y. (2001). Db1 family guanine nucleotide exchange factors. Trends Biochem. Sci. 26, 724-732.