Co-translational processing of glycoprotein 3 from equine arteritis virus: N-Glycosylation adjacent to the signal peptide prevents cleavage

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35437-35451

  Matczuk, Anna Karolina ^a   Kunec, Dušan ^a   Veit, Michael ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; GLYCOPROTEINS; GLYCOSYLATION; PEPTIDES; VIRUSES;

CELLULAR PROTEINS; MEMBRANE PROTEINS; N-GLYCOSYLATION; SIGNAL PEPTIDE; SIGNAL PEPTIDE CLEAVAGES;

PROTEINS;

ASPARAGINE; GLYCOPROTEIN 3; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN; GP3 PROTEIN, EQUINE ARTERITIS VIRUS; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; DEGLYCOSYLATION; ENDOPLASMIC RETICULUM; EQUINE VIRAL ARTERITIS VIRUS; HYDROPHOBICITY; IMMUNOPRECIPITATION; MICROSOME; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SECRETION; AMINO ACID SUBSTITUTION; ANIMAL; BINDING SITE; BIOLOGY; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENETICS; GLYCOSYLATION; HORSE; HUMAN; METABOLISM; MOLECULAR GENETICS; SITE DIRECTED MUTAGENESIS;

ARTERIVIRUS; EQUINE ARTERITIS VIRUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARTERITIS VIRUS, EQUINE; ASPARAGINE; BINDING SITES; CHO CELLS; COMPUTATIONAL BIOLOGY; CRICETULUS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HORSES; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN MODIFICATION, TRANSLATIONAL; PROTEIN SORTING SIGNALS; RECOMBINANT PROTEINS; VIRAL ENVELOPE PROTEINS;

EID: 84894370723     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505420     Document Type: Article

References (105)

1. Bretscher, A. (1983) Purification of an 80,000-dalton protein that is a component of the isolated microvillus cytoskeleton, and its localization in nonmuscle cells. J. Cell Biol. 97, 425-432
2. Fehon, R. G., McClatchey, A. I., and Bretscher, A. (2010) Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287
3. Saotome, I., Curto, M., and McClatchey, A. I. (2004) Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6, 855-864
4. Bonilha, V. L., Rayborn, M. E., Saotome, I., McClatchey, A. I., and Hollyfield, J. G. (2006) Microvilli defects in retinas of ezrin knockout mice. Exp. Eye Res. 82, 720-729
5. Karagiosis, S. A., and Ready, D. F. (2004) Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development. 131, 725-732
6. Bonilha, V. L., Finnemann, S. C., and Rodriguez-Boulan, E. (1999) Ezrin promotes morphogenesis of apical microvilli and basal infoldings in retinal pigment epithelium. J. Cell Biol. 147, 1533-1548
7. Viswanatha, R., Ohouo, P. Y., Smolka, M. B., and Bretscher, A. (2012) Local phosphocycling mediated by LOK/SLK restricts ezrin function to the apical aspect of epithelial cells. J. Cell Biol. 199, 969-984
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
9. Hirao, M., Sato, N., Kondo, T., Yonemura, S., Monden, M., Sasaki, T., Takai, Y., Tsukita, S., and Tsukita, S. (1996) 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
10. Niggli, V., Andréoli, 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
11. Matsui, T., Yonemura, S., Tsukita, S., and Tsukita, S. (1999) Activation of ERM proteins in vivo by Rho involves phosphatidylinositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9, 1259-1262
12. Yonemura, S., Matsui, T., Tsukita, S., 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
13. Gautreau, A., Louvard, D., and Arpin, M. (2000) Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J. Cell Biol. 150, 193-203
14. 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. U.S.A. 99, 12813-12818
15. Garbett, D., and Bretscher, A. (2012) PDZ interactions regulate rapid turnover of the scaffolding protein EBP50 in microvilli. J. Cell Biol. 198, 195-203
16. Chambers D.N. Bretscher A. (2005) Ezrin mutants affecting dimerization and activation. Biochemistry 44, 3926-3932
17. Hanono, A., Garbett, D., Reczek, D., Chambers, D. N., and Bretscher, A. (2006) EPI64 regulates microvillar subdomains and structure. J. Cell Biol. 175, 803-813
18. Garbett, D., LaLonde, D. P., and Bretscher, A. (2010) The scaffolding protein EBP50 regulates microvillar assembly in a phosphorylation-dependent manner. J. Cell Biol. 191, 397-413
19. Morales, F. C., Takahashi, Y., Kreimann, E. L., and Georgescu, M. M. (2004) Ezrin-radixin-moesin (ERM)-binding phosphoprotein 50 organizes ERM proteins at the apical membrane of polarized epithelia. Proc. Natl. Acad. Sci. U.S.A. 101, 17705-17710
20. Yonemura, S., Tsukita, S., and Tsukita, S. (1999) Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins. J. Cell Biol. 145, 1497-1509
21. Finnerty, C. M., Chambers, D., Ingraffea, J., Faber, H. R., Karplus, P. A., and Bretscher, A. (2004) The EBP50-moesin interaction involves a binding site regulated by direct masking on the FERM domain. J. Cell Sci. 117, 1547-1552
22. Barret, C., Roy, C., Montcourrier, P., Mangeat, P., and Niggli, V. (2000) Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP2) binding site in the NH2-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067-1080
23. Ben-Aissa, K., Patino-Lopez, G., Belkina, N. V., Maniti, O., Rosales, T., Hao, J. J., Kruhlak, M. J., Knutson, J. R., Picart, C., and Shaw, S. (2012) Activation of moesin, a protein that links actin cytoskeleton to the plasma membrane, occurs by phosphatidylinositol 4,5-bisphosphate (PIP2) binding sequentially to two sites and releasing an autoinhibitory linker. J. Biol. Chem. 287, 16311-16323
24. 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
25. Hamada, K., Shimizu, T., Yonemura, S., Tsukita, S., Tsukita, S., and Hakoshima, T. (2003) 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
26. Terawaki, S., Maesaki, R., and Hakoshima, T. (2006) Structural basis for NHERF recognition by ERM proteins. Structure 14, 777-789
27. Takatsu, H., Baba, K., Shima, T., Umino, H., Kato, U., Umeda, M., Nakayama, K., and Shin, H. W. (2011) ATP9B, a P4-ATPase (a putative aminophospholipid translocase), localizes to the trans-Golgi network in a CDC50 protein-independent manner. J. Biol. Chem. 286, 38159-38167
28. Reczek, D., Berryman, M., and Bretscher, A. (1997) Identification of EBP50: A PDZ-containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J. Cell Biol. 139, 169-179
29. Smolka, M. B., Albuquerque, C. P., Chen, S. H., and Zhou, H. (2007) Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. U.S.A. 104, 10364-10369
30. Reczek, D., and Bretscher, A. (1998) 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
31. Gary, R., and Bretscher, A. (1993) Heterotypic and homotypic associations between ezrin and moesin, two putative membrane-cytoskeletal linking proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 10846-10850
32. Berryman, M., and Bretscher, A. (2000) Identification of a novel member of the chloride intracellular channel gene family (CLIC5) that associates with the actin cytoskeleton of placental microvilli. Mol. Biol. Cell 11, 1509-1521
33. Neisch, A. L., Formstecher, E., and Fehon, R. G. (2013) Conundrum, an ARHGAP18 orthologue, regulates RhoA and proliferation through interactions with moesin. Mol. Biol. Cell 24, 1420-1433
34. Sullivan, A., Uff, C. R., Isacke, C. M., and Thorne, R. F. (2003) PACE-1, a novel protein that interacts with the C-terminal domain of ezrin. Exp. Cell Res. 284, 224-238
35. Granés, F., Urena, J. M., Rocamora, N., and Vilaró, S. (2000) Ezrin links syndecan-2 to the cytoskeleton. J. Cell Sci. 113, 1267-1276
36. Granés, F., Berndt, C., Roy, C., Mangeat, P., Reina, M., and Vilaró, S. (2003) Identification of a novel ezrin-binding site in syndecan-2 cytoplasmic domain. FEBS Lett. 547, 212-216
37. 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
38. Hughes, S. C., and Fehon, R. G. (2006) 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
39. Belkina, N. V., Liu, Y., Hao, J. J., Karasuyama, H., and Shaw, S. (2009)LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 106, 4707-4712
40. Alberts, A. S. (2001) Identification of a carboxyl-terminal diaphanousrelated formin homology protein autoregulatory domain. J. Biol. Chem. 276, 2824-2830
41. Spence, H. J., Chen, Y. J., Batchelor, C. L., Higginson, J. R., Suila, H., Carpen, O., and Winder, S. J. (2004) Ezrin-dependent regulation of the actin cytoskeleton by -dystroglycan. Hum. Mol. Genet. 13, 1657-1668
42. Chuang, J. Z., Chou, S. Y., and Sung, C. H. (2010) Chloride intracellular channel 4 is critical for the epithelial morphogenesis of RPE cells and retinal attachment. Mol. Biol. Cell 21, 3017-3028
43. Berryman, M. A., and Goldenring, J. R. (2003) CLIC4 is enriched at cellcell junctions and colocalizes with AKAP350 at the centrosome and midbody of cultured mammalian cells. Cell Motil. Cytoskeleton 56, 159-172
44. Oshiro, N., Fukata, Y., and Kaibuchi, K. (1998) Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J. Biol. Chem. 273, 34663-34666
45. Bretscher, A., Reczek, D., and Berryman, M. (1997) Ezrin: A protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 110, 3011-3018
46. Gorelik, J., Shevchuk, A. I., Frolenkov, G. I., Diakonov, I. A., Lab, M. J., Kros, C. J., Richardson, G. P., Vodyanoy, I., Edwards, C. R., Klenerman, D., and Korchev, Y. E. (2003) Dynamic assembly of surface structures in living cells. Proc. Natl. Acad. Sci. U.S.A. 100, 5819-5822
47. Hughes, S. C., Formstecher, E., and Fehon, R. G. (2010) Sip1, the Drosophila orthologue of EBP50/NHERF1, functions with the sterile 20 family kinase Slik to regulate moesin activity. J. Cell Sci. 123, 1099-1107
48. Batchelor, C. L., Higginson, J. R., Chen, Y. J., Vanni, C., Eva, A., and Winder, S. J. (2007) Recruitment of Dbl by ezrin and dystroglycan drives membrane proximal Cdc42 activation and filopodia formation. Cell Cycle 6, 353-363
49. LaLonde, D. P., Garbett, D., and Bretscher, A. (2010) A regulated complex of the scaffolding proteins PDZK1 and EBP50 with ezrin contribute to microvillar organization. Mol. Biol. Cell 21, 1519-1529
50. Wang, Z., and Schey, K. L. (2011) Aquaporin-0 interacts with the FERM domain of ezrin/radixin/moesin proteins in the ocular lens. Invest. Ophthalmol. Vis. Sci. 52, 5079-5087
51. Pilot, F., Philippe, J. M., Lemmers, C., and Lecuit, T. (2006) Spatial con- trol of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 442, 580-584
52. Luo, Y., Zheng, C., Zhang, J., Lu, D., Zhuang, J., Xing, S., Feng, J., Yang, D., and Yan, X. (2012) Recognition of CD146 as an ERM-binding protein offers novel mechanisms for melanoma cell migration. Oncogene 31, 306-321
53. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., Tsukita, S., and Tsukita, S. (1998) 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
54. Cannon, J. L., Mody, P. D., Blaine, K. M., Chen, E. J., Nelson, A. D., Sayles, L. J., Moore, T. V., Clay, B. S., Dulin, N. O., Shilling, R. A., Burkhardt, J. K., and Sperling, A. I. (2011) CD43 interaction with ezrin-radixin-moesin (ERM) proteins regulates T-cell trafficking and CD43 phosphorylation. Mol. Biol. Cell 22, 954-963
55. 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
56. Serrador, J. M., Nieto, M., Alonso-Lebrero, J. L., del Pozo, M. A., Calvo, J., Furthmayr, H., Schwartz-Albiez, R., Lozano, F., González- Amaro, R., Sánchez-Mateos, P., and Sánchez-Madrid, F. (1998) CD43 interacts with moesin and ezrin and regulates its redistribution to the uropods of T lymphocytes at the cell-cell contacts. Blood 91, 4632-4644
57. Legg, J. W., and Isacke, C. M. (1998) Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr. Biol. 8, 705-708
58. Legg, J. W., Lewis, C. A., Parsons, M., Ng, T., and Isacke, C. M. (2002) A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4, 399-407
59. Li, Y., Harada, T., Juang, Y. T., Kyttaris, V. C., Wang, Y., Zidanic, M., Tung, K., and Tsokos, G. C. (2007) Phosphorylated ERM is responsible for increasedTcell polarization, adhesion, and migration in patients with systemic lupus erythematosus. J. Immunol. 178, 1938-1947
60. Mori, T., Kitano, K., Terawaki, S., Maesaki, R., Fukami, Y., and Hakoshima, T. (2008) Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 283, 29602-29612
61. 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
62. Tsukita, S., Oishi, K., Sato, N., Sagara, J., Kawai, A., and Tsukita, S. (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126, 391-401
63. Takahashi, K., Sasaki, T., Mammoto, A., Hotta, I., Takaishi, K., Imamura, H., Nakano, K., Kodama, A., and Takai, Y. (1998) Interaction of radixin with Rho smallGprotein GDP/GTP exchange protein Dbl. Oncogene 16, 3279-3284
64. Tran Quang, C., Gautreau, A., Arpin, M., and Treisman, R. (2000) Ezrin function is required for ROCK-mediated fibroblast transformation by the Net and Dbl oncogenes. EMBO J. 19, 4565-4576
65. Prag, S., Parsons, M., Keppler, M. D., Ameer-Beg, S. M., Barber, P., Hunt, J., Beavil, A. J., Calvert, R., Arpin, M., Vojnovic, B., and Ng, T. (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
66. Yang, H. S., and Hinds, P. W. (2006) Phosphorylation of ezrin by cyclindependent kinase 5 induces the release of RhoGDPdissociation inhibitor to inhibit Rac1 activity in senescent cells. Cancer Res. 66, 2708-2715
67. Ognibene, M., Vanni, C., Segalerba, D., Mancini, P., Merello, E., Torrisi, M. R., Bosco, M. C., Varesio, L., and Eva, A. (2011) The tumor suppressor hamartin enhances Dbl protein transforming activity through interaction with ezrin. J. Biol. Chem. 286, 29973-29983
68. Martín, M., Simon-Assmann, P., Kedinger, M., Martin, M., Mangeat, P., Real, F. X., and Fabre, M. (2006) DCC regulates cell adhesion in human colon cancer derived HT-29 cells and associates with ezrin. Eur. J. Cell Biol. 85, 769-783
69. Antoine-Bertrand, J., Ghogha, A., Luangrath, V., Bedford, F. K., and Lamarche- Vane, N. (2011) The activation of ezrin-radixin-moesin proteins is regulated by netrin-1 through Src kinase and RhoA/Rho kinase activities and mediates netrin-1-induced axon outgrowth. Mol. Biol. Cell 22, 3734-3746
70. Lue, R. A., Brandin, E., Chan, E. P., and Branton, D. (1996) Two independent domains of hDlg are sufficient for subcellular targeting: the PDZ1-2 conformational unit and an alternatively spliced domain. J. Cell Biol. 135, 1125-1137
71. Lasserre, R., Charrin, S., Cuche, C., Danckaert, A., Thoulouze, M. I., de Chaumont, F., Duong, T., Perrault, N., Varin-Blank, N., Olivo-Marin, J. C., Etienne-Manneville, S., Arpin, M., Di Bartolo, V., and Alcover, A. (2010) Ezrin tunes T-cell activation by controlling Dlg1 and microtubule positioning at the immunological synapse. EMBO J. 29, 2301-2314
72. LaLonde, D. P., and Bretscher, A. (2009) The scaffold protein PDZK1 undergoes a head-to-tail intramolecular association that negatively regulates its interaction with EBP50. Biochemistry 48, 2261-2271
73. Zwaenepoel, I., Naba, A., Da Cunha, M. M., Del Maestro, L., Formstecher, E., Louvard, D., and Arpin, M. (2012) Ezrin regulates microvillus morphogenesis by promoting distinct activities of Eps8 proteins. Mol. Biol. Cell 23, 1080-1094
74. Naba, A., Reverdy, C., Louvard, D., and Arpin, M. (2008) Spatial recruitment and activation of the Fes kinase by ezrin promotes HGF-induced cell scattering. EMBO J. 27, 38-50
75. Helander, T. S., Carpén, O., Turunen, O., Kovanen, P. E., Vaheri, A., and Timonen, T. (1996) ICAM-2 redistributed by ezrin as a target for killer cells. Nature 382, 265-268
76. Heiska, L., Alfthan, K., Grönholm, M., Vilja, P., Vaheri, A., and Carpén, O. (1998) Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2). Regulation by phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 273, 21893-21900
77. Serrador, J. M., Alonso-Lebrero, J. L., del Pozo, M. A., Furthmayr, H., Schwartz-Albiez, R., Calvo, J., Lozano, F., and Sánchez-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
78. Alonso-Lebrero, J. L., Serrador, J. M., Domínguez-Jiménez, C., Barreiro, O., Luque, A., del Pozo, M. A., Snapp, K., Kansas, G., Schwartz-Albiez, R., Furthmayr, H., Lozano, F., and Sánchez-Madrid, F. (2000) Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood 95, 2413-2419
79. Oh, H. M., Lee, S., Na, B. R., Wee, H., Kim, S. H., Choi, S. C., Lee, K. M., and Jun, C. D. (2007) RKIKK motif in the intracellular domain is critical for spatial and dynamic organization of ICAM-1: functional implication for the leukocyte adhesion and transmigration. Mol. Biol. Cell 18, 2322-2335
80. Dickson, T. C., Mintz, C. D., Benson, D. L., and Salton, S. R. (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell Biol. 157, 1105-1112
81. Sakurai, T., Gil, O. D., Whittard, J. D., Gazdoiu, M., Joseph, T., Wu, J., Waksman, A., Benson, D. L., Salton, S. R., and Felsenfeld, D. P. (2008) Interactions between the L1 cell adhesion molecule and ezrin support traction-force generation and can be regulated by tyrosine phosphorylation. J. Neurosci. Res. 86, 2602-2614
82. Matsui, K., Parameswaran, N., Bagheri, N., Willard, B., and Gupta, N. (2011) Proteomics analysis of the ezrin interactome in B cells reveals a novel association with Myo18a-. J. Proteome Res. 10, 3983-3992
83. Denker, S. P., Huang, D. C., Orlowski, J., Furthmayr, H., and Barber, D. L. (2000) Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H- translocation. Mol. Cell 6, 1425-1436
84. Denker, S. P., and Barber, D. L. (2002) Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J. Cell Biol. 159, 1087-1096
85. Cha, B., Tse, M., Yun, C., Kovbasnjuk, O., Mohan, S., Hubbard, A., Arpin, M., and Donowitz, M. (2006) The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: dual role in NHE3 trafficking and mobility in the brush border. Mol. Biol. Cell 17, 2661-2673
86. Mykkänen, O. M., Grönholm, M., Rönty, M., Lalowski, M., Salmikangas, P., Suila, H., and Carpén, O. (2001) Characterization of human palladin, a microfilament-associated protein. Mol. Biol. Cell 12, 3060-3073
87. Rachlin, A. S., and Otey, C. A. (2006) Identification of palladin isoforms and characterization of an isoform-specific interaction between Lasp-1 and palladin. J. Cell Sci. 119, 995-1004
88. Henning, M. S., Stiedl, P., Barry, D. S., McMahon, R., Morham, S. G., Walsh, D., and Naghavi, M. H. (2011) PDZD8 is a novel moesin-interacting cytoskeletal regulatory protein that suppresses infection by herpes simplex virus type .Virology 415, 114-121
89. D'Angelo, R., Aresta, S., Blangy, A., Del Maestro, L., Louvard, D., and Arpin, M. (2007) 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
90. Orlando, R. A., Takeda, T., Zak, B., Schmieder, S., Benoit, V. M., Mc- Quistan, T., Furthmayr, H., and Farquhar, M. G. (2001) The glomerular epithelial cell anti-adhesin podocalyxin associates with the actin cytoskeleton through interactions with ezrin. J. Am. Soc. Nephrol. 12, 1589-1598
91. Snapp, K. R., Heitzig, C. E., and Kansas, G. S. (2002) Attachment of the PSGL-1 cytoplasmic domain to the actin cytoskeleton is essential for leukocyte rolling on P-selectin. Blood 99, 4494-4502
92. Serrador, J. M., Urzainqui, A., Alonso-Lebrero, J. L., Cabrero, J. R., Montoya, M. C., Vicente-Manzanares, M., Yáñez-Mó, M., and Sánchez-Madrid, F. (2002) A juxta-membrane amino acid sequence of P-selectin glycoprotein ligand-1 is involved in moesin binding and ezrin/radixin/ moesin-directed targeting at the trailing edge of migrating lymphocytes. Eur. J. Immunol. 32, 1560-1566
93. Takai, Y., Kitano, K., Terawaki, S., Maesaki, R., and Hakoshima, T. (2007) Structural basis of PSGL-1 binding to ERM proteins. Genes Cells 12, 1329-1338
94. Domínguez-Luis, M., Lamana, A., Vazquez, J., García-Navas, R., Mollinedo, F., Sánchez-Madrid, F., Díaz-González, F., and Urzainqui, A. (2011) The metalloprotease ADAM8 is associated with and regulates the function of the adhesion receptor PSGL-1 through ERM proteins. Eur. J. Immunol. 41, 3436-3442
95. Spertini, C., Baïsse, B., and Spertini, O. (2012) Ezrin-radixin-moesinbinding sequence of PSGL-1 glycoprotein regulates leukocyte rolling on selectins and activation of extracellular signal-regulated kinases. J. Biol. Chem. 287, 10693-10702
96. Ramel, D., Wang, X., Laflamme, C., Montell, D. J., and Emery, G. (2013) Rab11 regulates cell-cell communication during collective cell movements. Nat. Cell Biol. 15, 317-324
97. Sperka, T., Geissler, K. J., Merkel, U., Scholl, I., Rubio, I., Herrlich, P., and Morrison, H. L. (2011) Activation of Ras requires the ERM-dependent link of actin to the plasma membrane. PLoS One 6, e27511
98. 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
99. Koltzscher, M., Neumann, C., König, S., and Gerke, V. (2003) Ca2-dependent binding and activation of dormant ezrin by dimeric S100P. Mol. Biol. Cell 14, 2372-2384
100. Austermann, J., Nazmi, A. R., Müller-Tidow, C., and Gerke, V. (2008) Characterization of the Ca2-regulated ezrin-S100P interaction and its role in tumor cell migration. J. Biol. Chem. 283, 29331-29340
101. Bonilha, V. L., and Rodriguez-Boulan, E. (2001) Polarity and developmental regulation of two PDZ proteins in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 42, 3274-3282
102. Chirivino, D., Del Maestro, L., Formstecher, E., Hupé, P., Raposo, G., Louvard, D., and Arpin, M. (2011) The ERM proteins interact with the HOPS complex to regulate the maturation of endosomes. Mol. Biol. Cell 22, 375-385
103. Jin, C., Ge, L., Ding, X., Chen, Y., Zhu, H., Ward, T., Wu, F., Cao, X., Wang, Q., and Yao, X. (2006) PKA-mediated protein phosphorylation regulates ezrin-WWOX interaction. Biochem. Biophys. Res. Commun. 341, 784-791
104. Zaarour, R. F., Chirivino, D., Del Maestro, L., Daviet, L., Atfi, A., Louvard, D., and Arpin, M. (2012) Ezrin ubiquitylation by the E3 ubiquitin ligase, WWP1, and consequent regulation of hepatocyte growth factor receptor activity. PLoS One 7, e37490
105. Wan, X., Kim, S. Y., Guenther, L. M., Mendoza, A., Briggs, J., Yeung, C., Currier, D., Zhang, H., Mackall, C., Li, W. J., Tuan, R. S., Deyrup, A. T., Khanna, C., and Helman, L. (2009) -4 integrin promotes osteosarcoma metastasis and interacts with ezrin. Oncogene 28, 3401-3411