Moesin orchestrates cortical polarity of melanoma tumour cells to initiate 3D invasion

Journal of Cell Science

Volumn 122, Issue 19, 2009, Pages 3492-3501

  Estecha, Ana ^a   Sánchez Martín, Lorena ^a   Puig Kröger, Amaya ^a   Bartolomé, Rubén A ^b   Teixidó, Joaquín ^b   Samaniego, Rafael ^a   Sánchez Mateos, Paloma ^a  

^a HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Invasion; Metastasis; Moesin; Polarity

Indexed keywords

ACTIN; EZRIN; F ACTIN; MOESIN; MYOSIN II; RHO FACTOR; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CELL ADHESION; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM; EXTRACELLULAR MATRIX; MELANOMA CELL; METASTASIS; MOUSE; NONHUMAN; PATHOGENESIS; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; THREE DIMENSIONAL IMAGING;

ACTINS; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL POLARITY; CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; LUNG; MELANOMA; MICE; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS;

EID: 70350774025     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.053157     Document Type: Article

References (55)

1. Amieva, M. R., Litman, P., Huang, L., Ichimaru, E. and Furthmayr, H. (1999). Disruption of dynamic cell surface architecture of NIH3T3 fibroblasts by the N-terminal domains of moesin and ezrin: in vivo imaging with GFP fusion proteins. J. Cell Sci. 112, 111-125.
2. Barrero-Villar, M., Cabrero, J. R., Gordon-Alonso, M., Barroso-Gonzalez, J., Alvarez- Losada, S., Munoz-Fernandez, M. A., Sanchez-Madrid, F. and Valenzuela-Fernandez, A. (2009). Moesin is required for HIV-1-induced CD4-CXCR4 interaction, F-actin redistribution, membrane fusion and viral infection in lymphocytes. J. Cell Sci. 122, 103-113.
3. Bartolome, R. A., Galvez, B. G., Longo, N., Baleux, F., Van Muijen, G. N., Sanchez- Mateos, P., Arroyo, A. G. and Teixido, J. (2004). Stromal cell-derived factor-1alpha promotes melanoma cell invasion across basement membranes involving stimulation of membrane-type 1 matrix metalloproteinase and Rho GTPase activities. Cancer Res. 64, 2534-2543.
4. Bornens, M., Paintrand, M. and Celati, C. (1989). The cortical microfilament system of lymphoblasts displays a periodic oscillatory activity in the absence of microtubules: implications for cell polarity. J. Cell Biol. 109, 1071-1083.
5. 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.
6. Brown, M. J., Nijhara, R., Hallam, J. A., Gignac, M., Yamada, K. M., Erlandsen, S. L., Delon, J., Kruhlak, M. and Shaw, S. (2003). Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 102, 3890-3899.
7. Burridge, K. and Doughman, R. (2006). Front and back by Rho and Rac. Nat. Cell Biol. 8, 781-782.
8. 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.
9. Chambers, A. F., Groom, A. C. and MacDonald, I. C. (2002). Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572.
10. Charafe-Jauffret, E., Monville, F., Bertucci, F., Esterni, B., Ginestier, C., Finetti, P., Cervera, N., Geneix, J., Hassanein, M., Rabayrol, L. et al. (2007). Moesin expression is a marker of basal breast carcinomas. Int. J. Cancer 121, 1779-1785.
11. Charras, G. T., Coughlin, M., Mitchison, T. J. and Mahadevan, L. (2008). Life and times of a cellular bleb. Biophys. J. 94, 1836-1853.
12. Clark, E. A. and Brugge, J. S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-239.
13. Condeelis, J., Singer, R. H. and Segall, J. E. (2005). The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21, 695-718.
14. Cowan, C. R. and Hyman, A. A. (2007). Acto-myosin reorganization and PAR polarity in C. elegans. Development 134, 1035-1043.
15. Doyle, A. D., Wang, F. W., Matsumoto, K. and Yamada, K. M. (2009). One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 184, 481-490.
16. Edwards, K. A., Demsky, M., Montague, R. A., Weymouth, N. and Kiehart, D. P. (1997). GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 191, 103-117.
17. Even-Ram, S. and Yamada, K. M. (2005). Cell migration in 3D matrix. Curr. Opin. Cell Biol. 17, 524-532.
18. Faure, S., Salazar-Fontana, L. I., Semichon, M., Tybulewicz, V. L., Bismuth, G., Trautmann, A., Germain, R. N. and Delon, J. (2004). ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nat. Immunol. 5, 272-279.
19. 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.
20. Giannone, G., Dubin-Thaler, B. J., Dobereiner, H. G., Kieffer, N., Bresnick, A. R. and Sheetz, M. P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
21. 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.
22. Hiscox, S. and Jiang, W. G. (1999). Ezrin regulates cell-cell and cell-matrix adhesion, a possible role with E-cadherin/beta-catenin. J. Cell Sci. 112, 3081-3090.
23. Huang, L., Wong, T. Y., Lin, R. C. and Furthmayr, H. (1999). Replacement of threonine 558, a critical site of phosphorylation of moesin in vivo, with aspartate activates F-actin binding of moesin. Regulation by conformational change. J. Biol. Chem. 274, 12803-12810.
24. Hughes, S. C. and Fehon, R. G. (2007). Understanding ERM proteins-the awesome power of genetics finally brought to bear. Curr. Opin. Cell Biol. 19, 51-56.
25. Ilani, T., Khanna, C., Zhou, M., Veenstra, T. D. and Bretscher, A. (2007). Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin. J. Cell Biol. 179, 733-746.
26. Ivetic, A. and Ridley, A. J. (2004). Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes. Immunology 112, 165-176.
27. Jankovics, F., Sinka, R., Lukacsovich, T. and Erdelyi, M. (2002). MOESIN crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr. Biol. 12, 2060-2065.
28. 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.
29. Kobayashi, H., Sagara, J., Kurita, H., Morifuji, M., Ohishi, M., Kurashina, K. and Taniguchi, S. (2004). Clinical significance of cellular distribution of moesin in patients with oral squamous cell carcinoma. Clin. Cancer Res. 10, 572-580.
30. 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.
31. Lamb, R. F., Roy, C., Diefenbach, T. J., Vinters, H. V., Johnson, M. W., Jay, D. G. and Hall, A. (2000). The TSC1 tumour suppressor hamartin regulates cell adhesion through ERM proteins and the GTPase Rho. Nat. Cell Biol. 2, 281-287.
32. Longo, N., Yanez-Mo, M., Mittelbrunn, M., de la Rosa, G., Munoz, M. L., Sanchez-Madrid, F. and Sanchez-Mateos, P. (2001). Regulatory role of tetraspanin CD9 in tumor-endothelial cell interaction during transendothelial invasion of melanoma cells. Blood 98, 3717-3726.
33. 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.
34. Matsui, T., Yonemura, S. and Tsukita, S. (1999). Activation of ERM proteins in vivo by Rho involves phosphatidyl-inositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9, 1259-1262.
35. Niggli, V. and Rossy, J. (2008). Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton. Int. J. Biochem. Cell Biol. 40, 344-349.
36. 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.
37. Paluch, E., van der Gucht, J. and Sykes, C. (2006). Cracking up: symmetry breaking in cellular systems. J. Cell Biol. 175, 687-692.
38. Pankov, R., Endo, Y., Even-Ram, S., Araki, M., Clark, K., Cukierman, E., Matsumoto, K. and Yamada, K. M. (2005). A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793-802.
39. Partridge, M. A. and Marcantonio, E. E. (2006). Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol. Biol. Cell 17, 4237-4248.
40. Pinner, S. and Sahai, E. (2008). PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat. Cell Biol. 10, 127-137.
41. 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.
42. Prag, S., Parsons, M., Keppler, M. D., Ameer-Beg, S. M., Barber, P., Hunt, J., Beavil, A. J., Calvert, R., Arpin, M., Vojnovic, B. et al. (2007). Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42. Mol. Biol. Cell 18, 2935-2948.
43. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z. et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
44. Rodriguez, O. C., Schaefer, A. W., Mandato, C. A., Forscher, P., Bement, W. M. and Waterman-Storer, C. M. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599-609.
45. Sahai, E. (2007). Illuminating the metastatic process. Nat. Rev. Cancer 7, 737-749.
46. Serrador, J. M., Alonso-Lebrero, J. L., del Pozo, M. A., Furthmayr, H., Schwartz-Albiez, R., Calvo, J., Lozano, F. and Sanchez-Madrid, F. (1997). Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization. J. Cell Biol. 138, 1409-1423.
47. Shaw, R. J., Henry, M., Solomon, F. and Jacks, T. (1998). RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol. Biol. Cell 9, 403-419.
48. 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.
49. Takahashi, K., Sasaki, T., Mammoto, A., Takaishi, K., Kameyama, T., Tsukita, S. and Takai, Y. (1997). Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272, 23371-23375.
50. Tsuji, K., Yamauchi, K., Yang, M., Jiang, P., Bouvet, M., Endo, H., Kanai, Y., Yamashita, K., Moossa, A. R. and Hoffman, R. M. (2006). Dual-color imaging of nuclear-cytoplasmic dynamics, viability, and proliferation of cancer cells in the portal vein area. Cancer Res. 66, 303-306.
51. Van Muijen, G. N., Cornelissen, L. M., Jansen, C. F., Figdor, C. G., Johnson, J. P., Brocker, E. B. and Ruiter, D. J. (1991). Antigen expression of metastasizing and non-metastasizing human melanoma cells xenografted into nude mice. Clin. Exp. Metastasis 9, 259-272.
52. van Rheenen, J., Song, X., van Roosmalen, W., Cammer, M., Chen, X., Desmarais, V., Yip, S. C., Backer, J. M., Eddy, R. J. and Condeelis, J. S. (2007). EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J. Cell Biol. 179, 1247-1259.
53. Wyckoff, J. B., Pinner, S. E., Gschmeissner, S., Condeelis, J. S. and Sahai, E. (2006). ROCK- and myosin-dependent matrix deformation enables protease-independent tumorcell invasion in vivo. Curr. Biol. 16, 1515-1523.
54. 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.
55. 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.