Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity

Journal of Cell Science

Volumn 119, Issue 10, 2006, Pages 2107-2118

  Yamanaka, Tomoyuki ^a,b,c   Horikoshi, Yosuke ^a   Izumi, Natsuko ^a,b   Suzuki, Atsushi ^a   Mizuno, Keiko ^a   Ohno, Shigeo ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b Kihara Memorial Yokohama Foundation for the Advancement of Life Sciences   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Apical membrane domain; Epithelial cell polarity; Lgl; PAR

Indexed keywords

CALCIUM ION; COLLAGEN; PROTEIN KINASE C; PROTEIN LGL; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 6; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL CULTURE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CELL POLARITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOG; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; WESTERN BLOTTING;

ANIMALS; CELL LINE; CELL POLARITY; COLLAGEN; DOGS; EPITHELIAL CELLS; HOMEODOMAIN PROTEINS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; PROTEIN KINASE C; PROTEINS; RECEPTORS, THROMBIN; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS;

EID: 33745217610     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02938     Document Type: Article

References (48)

1. Akimoto, K., Mizuno, K., Osada, S., Hirai, S., Tanuma, S., Suzuki, K. and Ohno, S. (1994). A new member of the third class in the protein kinase C family, PKC lambda, expressed dominantly in an undifferentiated mouse embryonal carcinoma cell line and also in many tissues and cells. J. Biol. Chem, 269, 12677-12683.
2. 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.
3. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
4. Bilder, D., Li, M. and Perrimon, N. (2000). Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289, 113-116.
5. Brummelkamp, T. R., Bernards, R. and Agami, R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553.
6. Cao, X., Ding, X., Guo, Z., Zhou, R., Wang, F., Fog, V., Long, F., Bi, F., Fan, D., Forte, J. G. et al. (2005). PALS1 specifies the localization of ezrin to the apical membrane of gastric parietal cells. J. Biol. Chem. 280, 13584-13592.
7. Chalmers, A. D., Pambos, M., Mason, J., Lang, S., Wylie, C. and Papalopulu, N. (2005). aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development 132, 977-986.
8. Chen, X. and Macara, I. G. (2005). Par-3 controls fight junction assembly through the Rac exchange factor Tiam1. Nat. Cell Biol. 7, 262-269.
9. Gao, L., Joberty, G. and Macara, I. G. (2002). Assembly of epithelial fight junctions is negatively regulated by Par6. Curr. Biol. 12, 221-225.
10. Gateff, E. (1978). Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200, 1448-1459.
11. Gilbert, T. and Rodriguez-Boulan, E. (1991). Induction of vacuolar apical compartments in the Caco-2 intestinal epithelial cell line. J. Cell Sci. 100, 451-458.
12. 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.
13. Hurd, T. W., Fan, S., Liu, C. J., Kweon, H. K., Hakansson, K. and Margolis, B. (2003). Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par-3 regulates cell polarity in mammalian epithelia. Curr. Biol. 13, 2092-2090.
14. 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.
15. 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 fight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143, 95-106.
16. 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.
17. Klezovitch, O., Fernandez, T. E., Tapscott, S. J. and Vasioukhin, V. (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev. 18, 559-571.
18. Knust, E. and Bossinger, O. (2002). Composition and formation of intercellular junctions in epithelial cells. Science 298, 1955-1959.
19. Lemmers, C., Michel, D., Lane-Guermonprez, L., Delgrossi, M. H., Medina, E., Arsanto, J. P. and Le Bivic, A. (2004). CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol. Biol. Cell 15, 1324-1333.
20. 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.
21. Macara, I. G. (2004). Par proteins: partners in polarization. Curr. Biol. 14, R160-R162.
22. Mizuno, K., Suzuki, A., Hirose, T., Kitamura, K., Kutsuzawa, K., Futaki, M., Amano, Y. and Ohno, S. (2003). Self-association of PAR-3-mediated by the conserved N-terminal domain contributes to the development of epithelial tight junctions. J. Biol. Chem. 278, 31240-31250.
23. 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.
24. Musch, A., Cohen, D., Yeaman, C., Nelson, W. J., Rodriguez-Boulan, E. and Brennwald, P. J. (2002). Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol. Biol. Cell 13, 158-168.
25. O'Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P. and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838.
26. O'Brien, L. E., Zegers, M. M. and Mostov, K. E. (2002). Opinion: building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3, 531-537.
27. 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, 641-648.
28. Ohshiro, T., Yagami, T., Zhang, C. and Matsuzaki, F. (2000). Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature 408, 593-596.
29. Ojakian, G. K., Nelson, W. J. and Beck, K. A. (1997). Mechanisms for de novo biogenesis of an apical membrane compartment in groups of simple epithelial cells surrounded by extracellular matrix. J. Cell Sci. 110, 2781-2794.
30. Ojakian, G. K., Ratcliffe, D. R. and Schwimmer, R. (2001). Integrin regulation of cell-cell adhesion during epithelial tubule formation. J. Cell Sci. 114, 941-952.
31. Peng, C. Y., Manning, L., Albertson, R. and Doe, C. Q. (2000). The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408, 596-600.
32. 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.
33. Rogers, K. K., Jou, T. S., Guo, W. and Lipschutz, J. H. (2003). The Rho family of small GTPases is involved in epithelial cystogenesis and tubulogenesis. Kidney Int. 63, 1632-1644.
34. Roh, M. H., Fan, S., Liu, C. J. and Margolis, B. (2003). The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J. Cell Sci. 116, 2895-2906.
35. 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.
36. Schwimmer, R. and Ojakian, G. K. (1995). The alpha 2 beta 1 integrin regulates collagen-mediated MDCK epithelial membrane remodeling and tubule formation. J. Cell Sci. 108, 2487-2498.
37. 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.
38. Suzuki, A., Ishiyama, C., Hashiba, K., Shimizu, M., Ebnet, K. and Ohno, S. (2002). aPKC kinase activity is required for the asymmetric differentiation of the premature junctional complex during epithelial cell polarization. J. Cell Sci. 115, 3565-3573.
39. 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.
40. Tanaka, J., Miwa, Y., Miyoshi, K., Ueno, A. and Inoue, H. (1999). Construction of Epstein-Barr virus-based expression vector containing mini-oriP. Biochem. Biophys Res. Commun. 264, 938-943.
41. Vega-Salas, D. E., Salas, P. J. and Rodriguez-Boulan, E. (1987). Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney epithelial cells: cell-cell interactions control the appearance of a novel intracellular storage compartment. J. Cell Biol. 104, 1249-1259.
42. Vega-Salas, D. E., Salas, P. J. and Rodriguez-Boulan, E. (1988). Exocytosis of vacuolar apical compartment (VAC): a cell-cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial cells. J. Cell Biol. 107, 1717-1728.
43. Wang, A. Z., Ojakian, G. K. and Nelson, W. J. (1990). Steps in the morphogenesis of a polarized epithelium. I. Uncoupling the roles of cell-cell and cell-substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci. 95, 137-151.
44. Wang, Q., Hurd, T. W. and Margolis, B. (2004). Tight junction protein Par6 interacts with an evolutionarily conserved region in the amino terminus of PALS1/stardust. J. Biol. Chem. 279, 30715-30721.
45. 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.
46. 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.
47. Yamanaka, T., Horikoshi, Y., Sugiyama, Y., Ishiyama, C., Suzuki, A., Hirose, T., Iwamatsu, A., Shinohara, A. and Ohno, S. (2003). Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr. Biol. 13, 734-743.
48. Yu, W., Datta, A., Leroy, P., O'Brien, L. E., Mak, G., Jou, T. S., Matlin, K. S., Mostov, K. E. and Zegers, M. M. (2005). Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell 16, 433-445.