Organizing the cell cortex: The role of ERM proteins

Nature Reviews Molecular Cell Biology

Volumn 11, Issue 4, 2010, Pages 276-287

  Fehon, Richard G ^a   McClatchey, Andrea I ^b   Bretscher, Anthony ^c  

^a UNIVERSITY OF CHICAGO   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; EPIDERMAL GROWTH FACTOR RECEPTOR; EZRIN; HERMES ANTIGEN; INSULIN RECEPTOR SUBSTRATE 1; INTERCELLULAR ADHESION MOLECULE 2; LEUKOSIALIN; MOESIN; P SELECTIN GLYCOPROTEIN LIGAND 1; RADIXIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 3; SONIC HEDGEHOG PROTEIN;

ANTIGEN PRESENTING CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL MEMBRANE; CELL STRUCTURE; CYTOSKELETON; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; HUMAN; IMMUNE RESPONSE; METASTASIS; MITOSIS; NONHUMAN; OOCYTE; OSTEOSARCOMA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MICROVILLI; SIGNAL TRANSDUCTION;

EID: 77949826033     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2866     Document Type: Review

References (114)

1. Lajoie, P., Goetz, J. G., Dennis, J. W. & Nabi, I. R. Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. J. Cell Biol. 185, 381-385 (2009).
2. Saotome, I., Curto, M. & McClatchey, A. I. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6, 855-864 (2004).
3. Chorna-Ornan, I. et al. Light-regulated interaction of Dmoesin with TRP and TRPL channels is required for maintenance of photoreceptors. J. Cell Biol. 171, 143-152 (2005).
4. Kunda, P., Pelling, A. E., Liu, T. & Baum, B. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91-101 (2008).
5. Carreno, S. et al. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J. Cell Biol. 180, 739-746 (2008).
6. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M. & Fehon, R. G. Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87 (2003).
7. Ivetic, A. & Ridley, A. J. Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes. Immunology 11 2, 165-176 (2004).
8. Bretscher, A., Edwards, K. & Fehon, R. G. ERM proteins and merlin: integrators at the cell cortex. Nature Rev. Mol. Cell Biol. 3, 586-599 (2002).
9. Gautreau, A., Louvard, D. & Arpin, M. ERM proteins and NF2 tumor suppressor: the Yin and Yang of cortical actin organization and cell growth signaling. Curr. Opin. Cell Biol. 14, 104-109 (2002).
10. Tsukita, S. & Yonemura, S. Cortical actin organization: lessons from ERM (Ezrin/Radixin/Moesin) proteins. J. Biol. Chem. 274, 34507-34510 (1999).
11. Turunen, O., Wahlstrom, T. & Vaheri, A. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126, 1445-1453 (1994).
12. Gary, R. & Bretscher, A. 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 (1995).
13. Nakamura, F., Amieva, M. R. & Furthmayr, H. Phosphorylation of threonine 558 in the carboxyl-terminal actin-binding domain of moesin by thrombin activation of human platelets. J. Biol. Chem. 270, 31377-31385 (1995).
14. Yonemura, S., Matsui, T. & Tsukita, S. Rho-dependent and-independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 11 5, 2569-2580 (2002).
15. Fievet, B. T. et al. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659 (2004).
16. Belkina, N. V., Liu, Y., Hao, J. J., Karasuyama, H. & Shaw, S. LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proc. Natl Acad. Sci. USA 106, 4707-4712 (2009).
17. Matsui, T. et al. 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 (1998).
18. Ng, T. et al. Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 20, 2723-2741 (2001).
19. Simons, P. C., Pietromonaco, S. F., Reczek, D., Bretscher, A. & Elias, L. C-terminal threonine phosphorylation activates ERM proteins to link the cell's cortical lipid bilayer to the cytoskeleton. Biochem. Biophys. Res. Commun. 253, 561-565 (1998).
20. ten Klooster, J. P. et al. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell 16, 551-562 (2009).
21. McCartney, B. M. & Fehon, R. G. 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 (1996).
22. Hipfner, D. R., Keller, N. & Cohen, S. M. Slik Sterile-20 kinase regulates Moesin activity to promote epithelial integrity during tissue growth. Genes Dev. 18, 2243-2248 (2004).
23. Hughes, S. C. & Fehon, R. G. Phosphorylation and activity of the tumor suppressor Merlin and the ERM protein Moesin are coordinately regulated by the Slik kinase. J. Cell Biol. 175, 305-313 (2006).
24. Verdier, V. et al. Drosophila Rho-kinase (DRok) is required for tissue morphogenesis in diverse compartments of the egg chamber during oogenesis. Dev. Biol. 297, 417-432 (2006).
25. Polesello, C., Delon, I., Valenti, P., Ferrer, P. & Payre, F. Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nature Cell Biol. 4, 782-789 (2002).
26. Karagiosis, S. A. & Ready, D. F. Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131, 725-732 (2004).
27. Chambers, D. N. & Bretscher, A. Ezrin mutants affecting dimerization and activation. Biochemistry 44, 3926-3932 (2005).
28. Yang, H. S. & Hinds, P. W. Increased Ezrin expression and activation by CDK5 coincident with acquisition of the senescent phenotype. Mol. Cell 11, 1163-1176 (2003).
29. Pearson, M., Reczek, D., Bretscher, A. & Karplus, P. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101, 259-270 (2000).
30. Krieg, J. & Hunter, T. Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J. Biol. Chem. 267, 19258-19265 (1992).
31. Dransfield, D. T., Bradford, A. J. & Goldenring, J. R. Distribution of A-kinase anchoring proteins in parietal cells. Biochim. Biophys. Acta 1269, 215-220 (1995).
32. McClatchey, A. I. & Fehon, R. G. Merlin and the ERM proteins \ regulators of receptor distribution and signaling at the cell cortex. Trends Cell Biol. 19, 198-206 (2009).
33. Yonemura, S. et al. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 140, 885-895 (1998).
34. Weinman, E. J., Hall, R. A., Friedman, P. A., Liu-Chen, L. Y. & Shenolikar, S. The association of NHERF adaptor proteins with G protein-coupled receptors and receptor tyrosine kinases. Annu. Rev. Physiol. 68, 491-505 (2006).
35. Lalonde, D. & Bretscher, A. The scaffold protein PDZK1 undergoes a head-to-tail intramolecular association that negatively regulates its interaction with EBP50. Biochemistry 48, 2261-2271 (2009).
36. Cheng, H. et al. Autoinhibitory interactions between the PDZ2 and C-terminal domains in the scaffolding protein NHERF1. Structure 17, 660-669 (2009).
37. Morales, F. C. et al. NHERF1/EBP50 head-to-tail intramolecular interaction masks association with PDZ domain ligands. Mol. Cell. Biol. 27, 2527-2537 (2007).
38. Smith, W. J., Nassar, N., Bretscher, A., Cerione, R. A. & Karplus, P. A. Structure of the active N-terminal domain of ezrin. Conformational and mobility changes identify keystone interactions. J. Biol. Chem. 278, 4949-4956 (2003).
39. Hamada, K., Shimizu, T., Matsui, T., Tsukita, S. & Hakoshima, T. Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J. 19, 4449-4462 (2000).
40. Edwards, S. D. & Keep, N. H. The 2.7 Å crystal structure of the activated FERM domain of moesin: an analysis of structural changes on activation. Biochemistry 40, 7061-7068 (2001).
41. Takai, Y., Kitano, K., Terawaki, S., Maesaki, R. & Hakoshima, T. Structural basis of PSGL-1 binding to ERM proteins. Genes Cells 12, 1329-1338 (2007).
42. Takai, Y., Kitano, K., Terawaki, S., Maesaki, R. & Hakoshima, T. Structural basis of the cytoplasmic tail of adhesion molecule CD43 and its binding to ERM proteins. J. Mol. Biol. 381, 634-644 (2008).
43. Hamada, K., Shimizu, T., Yonemura, S., Tsukita, S. & Hakoshima, T. Structural basis of adhesion-molecule recognition by ERM proteins revealed by the crystal structure of the radixin-ICAM-2 complex. EMBO J. 22, 502-514 (2003).
44. Mori, T. et al. Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 283, 29602-29612 (2008).
45. Terawaki, S., Kitano, K. & Hakoshima, T. Structural basis for type II membrane protein binding by ERM proteins revealed by the radixin-neutral endopeptidase 24.11 (NEP) complex. J. Biol. Chem. 282, 19854-19862 (2007).
46. Finnerty, C. M. et al. The EBP50-moesin interaction involves a binding site regulated by direct masking on the FERM domain. J. Cell Sci. 11 7, 1547-1552 (2004).
47. Terawaki, S., Maesaki, R. & Hakoshima, T. Structural basis for NHERF recognition by ERM proteins. Structure 14, 777-789 (2006).
48. Jayaraman, B. & Nicholson, L. K. Thermodynamic dissection of the Ezrin FERM/CERMAD interface. Biochemistry 46, 12174-12189 (2007).
49. Reczek, D. & Bretscher, A. The carboxyl-terminal region of EBP50 binds to a site in the amino-terminal domain of ezrin that is masked in the dormant molecule. J. Biol. Chem. 273, 18452-18458 (1998).
50. Li, Q. et al. Self-masking in an intact ERM-merlin protein: an active role for the central α-helical domain. J. Mol. Biol. 365, 1446-1459 (2007).
51. Mackay, D. J., Esch, F., Furthmayr, H. & Hall, A. Rho-and rac-dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J. Cell Biol. 138, 927-938 (1997).
52. Hirao, M. et al. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway. J. Cell Biol. 135, 37-51 (1996).
53. Hatzoglou, A. et al. Gem associates with Ezrin and acts via the Rho-GAP protein Gmip to down-regulate the Rho pathway. Mol. Biol. Cell 18, 1242-1252 (2007).
54. Reczek, D. & Bretscher, A. Identification of EPI64, a TBC/rabGAP domain-containing microvillar protein that binds to the first PDZ domain of EBP50 and E3KARP. J. Cell Biol. 153, 191-206 (2001).
55. Hamada, K. et al. Crystallization and preliminary crystallographic studies of RhoGDI in complex with the radixin FERM domain. Acta Crystallogr. D Biol. Crystallogr. 57, 889-890 (2001).
56. D'Angelo, R. et al. Interaction of ezrin with the novel guanine nucleotide exchange factor PLEKHG6 promotes RhoG-dependent apical cytoskeleton rearrangements in epithelial cells. Mol. Biol. Cell 18, 4780-4793 (2007).
57. Molnar, C. & de Celis, J. F. Independent roles of Drosophila Moesin in imaginal disc morphogenesis and hedgehog signalling. Mech. Dev. 123, 337-351 (2006).
58. Lee, J. H. et al. Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation. J. Cell Biol. 167, 327-337 (2004).
59. Takahashi, K. et al. 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 (1997).
60. Takahashi, K. et al. Interaction of radixin with Rho small G protein GDP/GTP exchange protein Dbl. Oncogene 16, 3279-3284 (1998).
61. Formstecher, E. et al. Protein interaction mapping: a Drosophila case study. Genome Res. 15, 376-384 (2005).
62. Orian-Rousseau, V. et al. Hepatocyte growth factor-induced Ras activation requires ERM proteins linked to both CD44v6 and F-actin. Mol. Biol. Cell 18, 76-83 (2007).
63. Lamprecht, G. & Seidler, U. The emerging role of PDZ adapter proteins for regulation of intestinal ion transport. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G766-G777 (2006).
64. Jankovics, F., Sinka, R., Lukacsovich, T. & Erdelyi, M. Moesin crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr. Biol. 12, 2060-2065 (2002).
65. Micklem, D. R., Adams, J., Grunert, S. & St. Johnston, D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 19, 1366-1377 (2000).
66. Maddox, A. S. & Burridge, K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J. Cell Biol. 160, 255-265 (2003).
67. Charras, G. T., Hu, C. K., Coughlin, M. & Mitchison, T. J. Reassembly of contractile actin cortex in cell blebs. J. Cell Biol. 175, 477-490 (2006).
68. Neisch, A. & Fehon, R. G. FERMing up the plasma membrane. Dev. Cell 14, 154-156 (2008).
69. Pilot, F., Philippe, J. M., Lemmers, C. & Lecuit, T. Spatial control of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 442, 580-584 (2006).
70. Serano, J. & Rubin, G. M. The Drosophila synaptotagmin-like protein bitesize is required for growth and has mRNA localization sequences within its open reading frame. Proc. Natl Acad. Sci. USA 100, 13368-13373 (2003).
71. Gobel, V., Barrett, P. L., Hall, D. H. & Fleming, J. T. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 6, 865-873 (2004).
72. Van Furden, D., Johnson, K., Segbert, C. & Bossinger, O. The C. elegans ezrin-radixin-moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Dev. Biol. 272, 262-276 (2004).
73. Bossinger, O., Klebes, A., Segbert, C., Theres, C. & Knust, E. Zonula adherens formation in Caenorhabditis elegans requires dlg-1, the homologue of the Drosophila gene discs large. Dev. Biol. 230, 29-42 (2001).
74. Kerman, B. E., Cheshire, A. M., Myat, M. M. & Andrew, D. J. Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Dev. Biol. 320, 278-288 (2008).
75. Louvet, S., Aghion, J., Santa-Maria, A., Mangeat, P. & Maro, B. Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Dev. Biol. 177, 568-579 (1996).
76. Christofori, G. New signals from the invasive front. Nature 441, 444-450 (2006).
77. Hunter, K. W. Ezrin, a key component in tumor metastasis. Trends Mol. Med. 10, 201-204 (2004).
78. Ren, L. et al. The actin-cytoskeleton linker protein ezrin is regulated during osteosarcoma metastasis by PKC. Oncogene 28, 792-802 (2009).
79. Jeanes, A., Gottardi, C. J. & Yap, A. S. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27, 6920-6929 (2008).
80. Ponta, H., Sherman, L. & Herrlich, P. A. CD44: from adhesion molecules to signalling regulators. Nature Rev. Mol. Cell Biol. 4, 33-45 (2003).
81. Orian-Rousseau, V. & Ponta, H. Adhesion proteins meet receptors: a common theme? Adv. Cancer Res. 101, 63-92 (2008).
82. Wicki, A. et al. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9, 261-272 (2006).
83. Polyak, K. & Weinberg, R. A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature Rev. Cancer 9, 265-273 (2009).
84. Martin-Villar, E. et al. Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J. Cell Sci. 11 9, 4541-4553 (2006).
85. Meder, D., Shevchenko, A., Simons, K. & Fullekrug, J. Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J. Cell Biol. 168, 303-313 (2005).
86. Sizemore, S., Cicek, M., Sizemore, N., Ng, K. P. & Casey, G. Podocalyxin increases the aggressive phenotype of breast and prostate cancer cells in vitro through its interaction with ezrin. Cancer Res. 67, 6183-6191 (2007).
87. Bourguignon, L. Y. Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin. Cancer Biol. 18, 251-259 (2008).
88. Schmieder, S., Nagai, M., Orlando, R. A., Takeda, T. & Farquhar, M. G. Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J. Am. Soc. Nephrol 15, 2289-2298 (2004).
89. Samarin, S. & Nusrat, A. Regulation of epithelial apical junctional complex by Rho family GTPases. Front. Biosci. 14, 1129-1142 (2009).
90. Yoshinaga-Ohara, N., Takahashi, A., Uchiyama, T. & Sasada, M. Spatiotemporal regulation of moesin phosphorylation and rear release by Rho and serine/threonine phosphatase during neutrophil migration. Exp. Cell Res. 278, 112-122 (2002).
91. Shcherbina, A., Bretscher, A., Kenney, D. M. & Remold-O'Donnell, E. Moesin, the major ERM protein of lymphocytes and platelets, differs from ezrin in its insensitivity to calpain. FEBS Lett. 443, 31-36 (1999).
92. Faure, S. et al. ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nature Immunol. 5, 272-279 (2004).
93. Delon, J., Kaibuchi, K. & Germain, R. N. Exclusion of CD43 from the immunological synapse is mediated by phosphorylation-regulated relocation of the cytoskeletal adaptor moesin. Immunity 15, 691-701 (2001).
94. Allenspach, E. J. et al. ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity 15, 739-750 (2001).
95. Roumier, A. et al. The membrane-microfilament linker ezrin is involved in the formation of the immunological synapse and in T cell activation. Immunity 15, 715-728 (2001)
96. Shaffer, M. H. et al. Ezrin and moesin function together to promote T cell activation. J. Immunol. 182, 1021-1032 (2009).
97. Ilani, T., Khanna, C., Zhou, M., Veenstra, T. D. & Bretscher, A. Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin. J. Cell Biol. 179, 733-746 (2007).
98. Hao, J. J. et al. Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J. Cell Biol. 184, 451-462 (2009).
99. Krieg, J. & Hunter, T. Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J. Biol. Chem. 267, 19258-19265 (1992).
100. Lankes, W. T. & Furthmayr, H. Moesin: a member of the protein 4.1-talin-ezrin family of proteins. Proc. Natl Acad. Sci. USA 88, 8297-8301 (1991).
101. Kikuchi, S. et al. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nature Genet. 31, 320-325 (2002).
102. Doi, Y. et al. Normal development of mice and unimpaired cell adhesion/cell motility/actin-based cytoskeleton without compensatory up-regulation of ezrin or radixin in moesin gene knockout. J. Biol. Chem. 274, 2315-2321 (1999).
103. Tamura, A. et al. Achlorhydria by ezrin knockdown: defects in the formation/expansion of apical canaliculi in gastric parietal cells. J. Cell Biol. 169, 21-28 (2005).
104. Kitajiri, S. et al. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J. Cell Biol. 166, 559-570 (2004).
105. Okayama, T. et al. Attenuated response to liver injury in moesin-deficient mice: impaired stellate cell migration and decreased fibrosis. Biochim. Biophys. Acta 1782, 542-548 (2008).
106. Hashimoto, S. et al. Dysregulation of lung injury and repair in moesin-deficient mice treated with intratracheal bleomycin. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L566-574 (2008).
107. Liu, Y., Belkina, N. V. & Shaw, S. HIV infection of T cells: actin-in and actin-out. Sci. Signal. 2, pe23 (2009).
108. Barrero-Villar, M. et al. 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 (2009).
109. Kubo, Y. et al. Ezrin, Radixin, and Moesin (ERM) proteins function as pleiotropic regulators of human immunodeficiency virus type 1 infection. Virology 375, 130-140 (2008).
110. Millan, J. & Ridley, A. J. Rho GTPases and leucocyte-induced endothelial remodelling. Biochem. J. 385, 329-337 (2005).
111. Doulet, N. et al. Neisseria meningitidis infection of human endothelial cells interferes with leukocyte transmigration by preventing the formation of endothelial docking structures. J. Cell Biol. 173, 627-637 (2006).
112. Trofatter, J. A. et al. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72, 791-800 (1993).
113. Rouleau, G. A. et al. Alteration in a new gene encoding a putative membrane-organizing protein causes neurofibromatosis type 2. Nature 363, 515-521 (1993).
114. Maeda, M., Matsui, T., Imamura, M. & Tsukita, S. Expression level, subcellular distribution and rho-GDI binding affinity of merlin in comparison with Ezrin/Radixin/Moesin proteins. Oncogene 18, 4788-4797 (1999).