Differential roles of PtdIns(4,5)P2and phosphorylation in moesin activation during Drosophila development

Journal of Cell Science

Volumn 123, Issue 12, 2010, Pages 2058-2067

  Roch, Fernando ^a,b   Polesello, Cédric ^a,b   Roubinet, Chantal ^a,b,c   Martin, Marianne ^d   Roy, Christian ^d   Valenti, Philippe ^a,b   Carreno, Sébastien ^c   Mangeat, Paul ^d,e   Payre, François ^a,b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b CNRS   (France)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d UNIV MONTPELLIER   (France)

^e Centre National de la Recherche Scientifique   (France)

Author keywords

Actin cytoskeleton; Drosophila morphogenesis; ERM proteins; Moesin; PtdIns(4,5)P2

Indexed keywords

ACTIN; EZRIN; MOESIN; PHOSPHATIDYLINOSITOL; RADIXIN; THREONINE;

ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DROSOPHILA; INSECT DEVELOPMENT; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CYTOSKELETAL PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; WING;

EID: 77953556360     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.064550     Document Type: Article

References (36)

1. Barret, C., Roy, C., Montcourrier, P., Mangeat, P. and Niggli, V. (2000). Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2)) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067-1080.
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. Bretscher, A., Edwards, K. and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599.
4. Calleja, M., Moreno, E., Pelaz, S. and Morata, G. (1996). Visualization of gene expression in living adult Drosophila. Science 274, 252-255. (Pubitemid 26353203)
5. Carreno, S., Kouranti, I., Glusman, E. S., Fuller, M. T., Echard, A. and Payre, F. (2008). Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J. Cell Biol. 180, 739-746. (Pubitemid 351397773)
6. Chorna-Ornan, I., Tzarfaty, V., Ankri-Eliahoo, G., Joel-Almagor, T., Meyer, N. E., Huber, A., Payre, F. and Minke, B. (2005). Light-regulated interaction of Dmoesin with TRP and TRPL channels is required for maintenance of photoreceptors. J. Cell Biol. 171, 143-152. (Pubitemid 41434609)
7. Coscoy, S., Waharte, F., Gautreau, A., Martin, M., Louvard, D., Mangeat, P., Arpin, M. and Amblard, F. (2002). Molecular analysis of microscopic ezrin dynamics by two-photon FRAP. Proc. Natl. Acad. Sci. USA 99, 12813-12818.
8. Fievet, B. T., Gautreau, A., Roy, C., Del Maestro, L., Mangeat, P., Louvard, D. and Arpin, M. (2004). Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659. (Pubitemid 38282949)
9. Gary, R. and Bretscher, A. (1995). Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 6, 1061-1075.
10. Gervais, L., Claret, S., Januschke, J., Roth, S. and Guichet, A. (2008). PIP5K-dependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development 135, 3829-3838.
11. Hamada, K., Shimizu, T., Matsui, T., Tsukita, S. and Hakoshima, T. (2000). Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J. 19, 4449-4462.
12. Hao, J. J., Liu, Y., Kruhlak, M., Debell, K. E., Rellahan, B. L. and Shaw, S. (2009). Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J. Cell Biol. 184, 451-462.
13. Hassan, B. A., Prokopenko, S. N., Breuer, S., Zhang, B., Paululat, A. and Bellen, H. J. (1998). skittles, a Drosophila phosphatidylinositol 4-phosphate 5-kinase, is required for cell viability, germline development and bristle morphology, but not for neurotransmitter release. Genetics 150, 1527-1537. (Pubitemid 28555555)
14. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129. (Pubitemid 24232280)
15. Hayashi, K., Yonemura, S., Matsui, T. and Tsukita, S. (1999). Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues. J. Cell Sci. 112, 1149-1158.
16. Hipfner, D. R., Keller, N. and Cohen, S. M. (2004). Slik Sterile-20 kinase regulates Moesin activity to promote epithelial integrity during tissue growth. Genes Dev. 18, 2243-2248. (Pubitemid 39209572)
17. Karagiosis, S. A. and Ready, D. F. (2004). Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131, 725-732.
18. Khanna, C., Wan, X., Bose, S., Cassaday, R., Olomu, O., Mendoza, A., Yeung, C., Gorlick, R., Hewitt, S. M. and Helman, L. J. (2004). The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat. Med. 10, 182-186.
19. Kunda, P., Pelling, A. E., Liu, T. and Baum, B. (2008). Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91-101.
20. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461. (Pubitemid 29159845)
21. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K. and Tsukita, S. (1998). Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657. (Pubitemid 28134067)
22. McCartney, B. M. and Fehon, R. G. (1996). Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol. 133, 843-852.
23. Nakamura, F., Huang, L., Pestonjamasp, K., Luna, E. J. and Furthmayr, H. (1999). Regulation of F-actin binding to platelet moesin in vitro by both phosphorylation of threonine 558 and polyphosphatidylinositides. Mol. Biol. Cell 10, 2669-2685.
24. Niggli, V., Andreoli, C., Roy, C. and Mangeat, P. (1995). Identification of a phosphatidylinositol-4,5-bisphosphate-binding domain in the N-terminal region of ezrin. FEBS Lett. 376, 172-176.
25. Pearson, M. A., Reczek, D., Bretscher, A. and Karplus, P. A. (2000). Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101, 259-270.
26. Polesello, C. and Payre, F. (2004). Small is beautiful: what flies tell us about ERM protein function in development. Trends Cell. Biol. 14, 294-302.
27. Polesello, C., Delon, I., Valenti, P., Ferrer, P. and Payre, F. (2002). Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4, 782-789.
28. Rasmussen, M., Alexander, R. T., Darborg, B. V., Mobjerg, N., Hoffmann, E. K., Kapus, A. and Pedersen, S. F. (2008). Osmotic cell shrinkage activates ezrin/radixin/moesin (ERM) proteins: activation mechanisms and physiological implications. Am. J. Physiol. Cell Physiol. 294, C197-C212.
29. Rogers S. L, Rogers G. C, Sharp D. J, Vale R. D. (2002). Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol.158, 873-884.
30. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M. and Fehon, R. G. (2003). Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87. (Pubitemid 36077089)
31. Stauffer, T. P., Ahn, S. and Meyer, T. (1998). Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr. Biol. 8, 343-346.
32. Turunen, O., Wahlstrom, T. and Vaheri, A. (1994). Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126, 1445-1453. (Pubitemid 24284609)
33. Yin, H. L. and Janmey, P. A. (2003). Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789.
34. Yonemura, S., Matsui, T. and Tsukita, S. (2002). Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580. (Pubitemid 34778074)
35. Yu, Y., Khan, J., Khanna, C., Helman, L., Meltzer, P. S. and Merlino, G. (2004). Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat. Med. 10, 175-181.
36. Zelhof, A. C. and Hardy, R. W. (2004). WASp is required for the correct temporal morphogenesis of rhabdomere microvilli. J. Cell Biol. 164, 417-426.