Drosophila aPKC is required for mitotic spindle orientation during symmetric division of epithelial cells

Development

Volumn 139, Issue 3, 2012, Pages 503-513

  Guilgur, Leonardo G ^a   Prudêncio, Pedro ^a   Ferreira, Tânia ^a   Pimenta Marques, Ana Rita ^a   Martinho, Rui Gonçalo ^a,b  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

aPKC; Drosophila; Epithelial cells; Mitosis; Spindle orientation

Indexed keywords

PROTEIN KINASE C;

ALLELE; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL INTERACTION; CELL POLARITY; CHICKEN; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME LOCALIZATION; EPITHELIUM CELL; FEMALE; IN VIVO STUDY; MAMMAL CELL; MICROTUBULE; MITOSIS SPINDLE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; TISSUE CULTURE;

ANIMALS; CELL DIVISION; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; FEMALE; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; MALE; MITOTIC SPINDLE APPARATUS; MUTATION; PROTEIN KINASE C;

MAMMALIA;

EID: 84855420819     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.071027     Document Type: Article

References (42)

1. Baena-Lopez, L. A., Baonza, A. and Garcia-Bellido, A. (2005). The orientation of cell divisions determines the shape of Drosophila organs. Curr. Biol. 15, 1640-1644.
2. Betschinger, J. and Knoblich, J. A. (2004). Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol. 14, R674-R685.
3. Betschinger, J., Mechtler, K. and Knoblich, J. A. (2003). The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422, 326-330.
4. Bilder, D., Schober, M. and Perrimon, N. (2003). Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5, 53-58.
5. Durgan, J., Kaji, N., Jin, D. and Hall, A. (2011). Par6B and Atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J. Biol. Chem. 286, 12461-12474.
6. Fernandez-Minan, A., Martin-Bermudo, M. D. and Gonzalez-Reyes, A. (2007). Integrin signaling regulates spindle orientation in Drosophila to preserve the follicular-epithelium monolayer. Curr. Biol. 17, 683-688.
7. Georgiou, M., Marinari, E., Burden, J. and Baum, B. (2008). Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr. Biol. 18, 1631-1638.
8. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
9. Hao, Y., Du, Q., Chen, X., Zheng, Z., Balsbaugh, J. L., Maitra, S., Shabanowitz, J., Hunt, D. F. and Macara, I. G. (2010). Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical pins. Curr. Biol. 20, 1809-1818.
10. Harris, T. J. and Peifer, M. (2005). The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J. Cell Biol. 170, 813-823.
11. Harris, T. J. and Peifer, M. (2007). aPKC controls microtubule organization to balance adherens junction symmetry and planar polarity during development. Dev. Cell 12, 727-738.
12. Hutterer, A., Betschinger, J., Petronczki, M. and Knoblich, J. A. (2004). Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 6, 845-854.
13. Izumi, Y., Hirose, T., Tamai, Y., Hirai, S., Nagashima, Y., Fujimoto, T., Tabuse, Y., Kemphues, K. J. and Ohno, S. (1998). An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143, 95-106.
14. Jaffe, A. B., Kaji, N., Durgan, J. and Hall, A. (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183, 625-633.
15. 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.
16. 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.
17. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
18. Knust, E. and Bossinger, O. (2002). Composition and formation of intercellular junctions in epithelial cells. Science 298, 1955-1959.
19. Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T. and Matsuzaki, F. (2008). Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101.
20. Krahn, M. P., Buckers, J., Kastrup, L. and Wodarz, A. (2010). Formation of a Bazooka-Stardust complex is essential for plasma membrane polarity in epithelia. J. Cell Biol. 190, 751-760.
21. Lee, J. D. and Treisman, J. E. (2001). Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr. Biol. 11, 1147-1152.
22. Li, K. and Kaufman, T. C. (1996). The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85, 585-596.
23. Messerschmidt, A., Macieira, S., Velarde, M., Badeker, M., Benda, C., Jestel, A., Brandstetter, H., Neuefeind, T. and Blaesse, M. (2005). Crystal structure of the catalytic domain of human atypical protein kinase C-iota reveals interaction mode of phosphorylation site in turn motif. J. Mol. Biol. 352, 918-931.
24. 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 141, 509-523.
25. Ninov, N., Chiarelli, D. A. and Martin-Blanco, E. (2007). Extrinsic and intrinsic mechanisms directing epithelial cell sheet replacement during Drosophila metamorphosis. Development 134, 367-379.
26. Parmentier, M. L., Woods, D., Greig, S., Phan, P. G., Radovic, A., Bryant, P. and O'Kane, C. J. (2000). Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. 20, RC84.
27. 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.
28. Peyre, E., Jaouen, F., Saadaoui, M., Haren, L., Merdes, A., Durbec, P. and Morin, X. (2011). A lateral belt of cortical LGN and NuMA guides mitotic spindle movements and planar division in neuroepithelial cells. J. Cell Biol. 193, 141-154.
29. Pimenta-Marques, A., Tostoes, R., Marty, T., Barbosa, V., Lehmann, R. and Martinho, R. G. (2008). Differential requirements of a mitotic acetyltransferase in somatic and germ line cells. Dev. Biol. 323, 197-206.
30. Qin, Y., Meisen, W. H., Hao, Y. and Macara, I. G. (2010). Tuba, a Cdc42 GEF, is required for polarized spindle orientation during epithelial cyst formation. J. Cell Biol. 189, 661-669.
31. 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.
32. Schaefer, M., Shevchenko, A. and Knoblich, J. A. (2000). A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10, 353-362.
33. Schaefer, M., Petronczki, M., Dorner, D., Forte, M. and Knoblich, J. A. (2001). Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107, 183-194.
34. Schober, M., Schaefer, M. and Knoblich, J. A. (1999). Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402, 548-551.
35. Segalen, M. and Bellaiche, Y. (2009). Cell division orientation and planar cell polarity pathways. Semin. Cell Dev. Biol. 20, 972-977.
36. Siller, K. H. and Doe, C. Q. (2009). Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11, 365-374.
37. Suzuki, A. and Ohno, S. (2006). The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119, 979-987.
38. 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.
39. Yamashita, Y. M. and Fuller, M. T. (2008). Asymmetric centrosome behavior and the mechanisms of stem cell division. J. Cell Biol. 180, 261-266.
40. Yu, F., Morin, X., Cai, Y., Yang, X. and Chia, W. (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.
41. Yu, F., Cai, Y., Kaushik, R., Yang, X. and Chia, W. (2003). Distinct roles of Galphai and Gbeta13F subunits of the heterotrimeric G protein complex in the mediation of Drosophila neuroblast asymmetric divisions. J. Cell Biol. 162, 623-633.
42. Zheng, Z., Zhu, H., Wan, Q., Liu, J., Xiao, Z., Siderovski, D. P. and Du, Q. (2010). LGN regulates mitotic spindle orientation during epithelial morphogenesis. J. Cell Biol. 189, 275-288.