The tumor suppressor Lgl1 forms discrete complexes with NMII-A and Par6α-aPKCζ that are affected by Lgl1 phosphorylation

Journal of Cell Science

Volumn 127, Issue 2, 2014, Pages 295-304

  Dahan, Inbal ^a   Petrov, Daria ^a   Cohen Kfir, Einav ^a   Ravid, Shoshana ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

Cell motility; Lethal giant larvae (Lgl); Non muscle myosin

Indexed keywords

MYOSIN; NON MUSCLE MYOSIN IIA; PROTEIN KINASE C LAMBDA; PROTEIN LGL1; PROTEIN PAR6ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; FOCAL ADHESION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

CELL MOTILITY; LETHAL GIANT LARVAE (LGL); NON-MUSCLE MYOSIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; CYTOSKELETON; GLYCOPROTEINS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NIH 3T3 CELLS; NONMUSCLE MYOSIN TYPE IIA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PSEUDOPODIA; TUMOR SUPPRESSOR PROTEINS;

EID: 84892518329     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.127357     Document Type: Article

References (48)

1. 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.
2. Betschinger, J., Eisenhaber, F. and Knoblich, J. A. (2005). Phosphorylationinduced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae. Curr. Biol. 15, 276-282.
3. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
4. Bilder, D. and Perrimon, N. (2000). Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403, 676-680.
5. Bilder, D., Li, M. and Perrimon, N. (2000). Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289, 113-116.
6. Cai, Y., Biais, N., Giannone, G., Tanase, M., Jiang, G., Hofman, J. M., Wiggins, C. H., Silberzan, P., Buguin, A., Ladoux, B. et al. (2006). Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91, 3907-3920.
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. Conti, M. A. and Adelstein, R. S. (2008). Nonmuscle myosin II moves in new directions. J. Cell Sci. 121, 11-18.
9. Dahan, I., Yearim, A., Touboul, Y. and Ravid, S. (2012). The tumor suppressor Lgl1 regulates NMII-A cellular distribution and focal adhesion morphology to optimize cell migration. Mol. Biol. Cell 23, 591-601.
10. Dulyaninova, N. G., Malashkevich, V. N., Almo, S. C. and Bresnick, A. R. (2005). Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation. Biochemistry 44, 6867-6876.
11. Etienne-Manneville, S. (2008). Polarity proteins in glial cell functions. Curr. Opin. Neurobiol. 18, 488-494.
12. Even-Faitelson, L. and Ravid, S. (2006). PAK1 and aPKCzeta regulate myosin II-B phosphorylation: a novel signaling pathway regulating filament assembly. Mol. Biol. Cell 17, 2869-2881.
13. Gao, L. and Macara, I. G. (2004). Isoforms of the polarity protein par6 have distinct functions. J. Biol. Chem. 279, 41557-41562.
14. Golomb, E., Ma, X., Jana, S. S., Preston, Y. A., Kawamoto, S., Shoham, N. G., Goldin, E., Conti, M. A., Sellers, J. R. and Adelstein, R. S. (2004). Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J. Biol. Chem. 279, 2800-2808.
15. Gupton, S. L. and Waterman-Storer, C. M. (2006). Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361-1374.
16. 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.
17. Jay, P. Y., Pham, P. A., Wong, S. A. and Elson, E. L. (1995). A mechanical function of myosin II in cell motility. J. Cell Sci. 108, 387-393.
18. Kalmes, A., Merdes, G., Neumann, B., Strand, D. and Mechler, B. M. (1996). A serine-kinase associated with the p127-l(2)gl tumour suppressor of Drosophila may regulate the binding of p127 to nonmuscle myosin II heavy chain and the attachment of p127 to the plasma membrane. J. Cell Sci. 109, 1359-1368.
19. Katsuragawa, Y., Yanagisawa, M., Inoue, A. and Masaki, T. (1989). Two distinct nonmuscle myosin-heavy-chain mRNAs are differentially expressed in various chicken tissues. Eur. J. Biochem. 184, 611-616.
20. 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.
21. Knust, E. and Bossinger, O. (2002). Composition and formation of intercellular junctions in epithelial cells. Science 298, 1955-1959.
22. Kolega, J. (1998). Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells. J. Cell Sci. 111, 2085-2095.
23. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
24. Leitges, M., Sanz, L., Martin, P., Duran, A., Braun, U., García, J. F., Camacho, F., Diaz-Meco, M. T., Rennert, P. D. and Moscat, J. (2001). Targeted disruption of the zetaPKC gene results in the impairment of the NF-kappaB pathway. Mol. Cell 8, 771-780.
25. Mitchison, T. J. and Cramer, L. P. (1996). Actin-based cell motility and cell locomotion. Cell 84, 371-379.
26. Murakami, N., Kotula, L. and Hwang, Y.-W. (2000). Two distinct mechanisms for regulation of nonmuscle myosin assembly via the heavy chain: phosphorylation for MIIB and mts 1 binding for MIIA. Biochemistry 39, 11441-11451.
27. Müsch, 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.
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. Peng, C. Y., Manning, L., Albertson, R. and Doe, C. Q. (2000). The tumoursuppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408, 596-600.
30. Phillips, C. L., Yamakawa, K. and Adelstein, R. S. (1995). Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J. Muscle Res. Cell Motil. 16, 379-389.
31. Plant, P. J., Fawcett, J. P., Lin, D. C., Holdorf, A. D., Binns, K., Kulkarni, S. and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301-308.
32. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
33. 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.
34. Ronen, D. and Ravid, S. (2009). Myosin II tailpiece determines its paracrystal structure, filament assembly properties, and cellular localization. J. Biol. Chem. 284, 24948-24957.
35. Rosenberg, M. and Ravid, S. (2006). Protein kinase Cgamma regulates myosin IIB phosphorylation, cellular localization, and filament assembly. Mol. Biol. Cell 17, 1364-1374.
36. Rosse, C., Linch, M., Kermorgant, S., Cameron, A. J., Boeckeler, K. and Parker, P. J. (2010). PKC and the control of localized signal dynamics. Nat. Rev. Mol. Cell Biol. 11, 103-112.
37. Sheffield, P., Garrard, S. and Derewenda, Z. (1999). Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr. Purif. 15, 34-39.
38. Shohet, R. V., Conti, M. A., Kawamoto, S., Preston, Y. A., Brill, D. A. and Adelstein, R. S. (1989). Cloning of the cDNA encoding the myosin heavy chain of a vertebrate cellular myosin. Proc. Natl. Acad. Sci. USA 86, 7726-7730.
39. Simons, M., Wang, M., McBride, O. W., Kawamoto, S., Yamakawa, K., Gdula, D., Adelstein, R. S. and Weir, L. (1991). Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ. Res. 69, 530-539.
40. Sripathy, S., Lee, M. and Vasioukhin, V. (2011). Mammalian Llgl2 is necessary for proper branching morphogenesis during placental development. Mol. Cell. Biol. 31, 2920-2933.
41. Strand, D., Jakobs, R., Merdes, G., Neumann, B., Kalmes, A., Heid, H. W., Husmann, I. and Mechler, B. M. (1994). The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol. 127, 1361-1373.
42. Straussman, R., Ben-Ya'acov, A., Woolfson, D. N. and Ravid, S. (2007). Kinking the coiled coil-negatively charged residues at the coiled-coil interface. J. Mol. Biol. 366, 1232-1242.
43. Vasioukhin, V. (2006). Lethal giant puzzle of Lgl. Dev. Neurosci. 28, 13-24.
44. Verkhovsky, A. B., Svitkina, T. M. and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
45. Vicente-Manzanares, M., Zareno, J., Whitmore, L., Choi, C. K. and Horwitz, A. F. (2007). Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176, 573-580.
46. Vicente-Manzanares, M., Koach, M. A., Whitmore, L., Lamers, M. L. and Horwitz, A. F. (2008). Segregation and activation of myosin IIB creates a rear in migrating cells. J. Cell Biol. 183, 543-554.
47. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. and Horwitz, A. R. (2009). Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790.
48. 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.