Structural basis of adhesion-molecule recognition by ERM proteins revealed by the crystal structure of the radixin-ICAM-2 complex

EMBO Journal

Volumn 22, Issue 3, 2003, Pages 502-514

  Hamada, Keisuke ^a,d   Shimizu, Toshiyuki ^a,e   Yonemura, Shigenobu ^c,f   Tsukita, Shoichiro ^c   Tsukita, Sachiko ^c   Hakoshima, Toshio ^a,b  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d RIKEN HARIMA INSTITUTE   (Japan)

^e YOKOHAMA CITY UNIVERSITY   (Japan)

^f RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Cell adhesion; Cytoskeleton; Recognition; Signal transduction; X ray

Indexed keywords

CELL ADHESION MOLECULE; EZRIN; INTERCELLULAR ADHESION MOLECULE 2; MOESIN; PHOSPHOTYROSINE; RADIXIN;

ARTICLE; CRYSTAL STRUCTURE; CYTOSKELETON; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; BETA CATENIN; BLOOD PROTEINS; CELL ADHESION MOLECULES; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTATION; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS;

EID: 0037415682     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg039     Document Type: Article

References (61)

1. 1 ATPase. Acta Crystallogr. D, 52, 30-42.
2. Allenspach, E.J. et al. (2001) ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity, 15, 739-750.
3. Amieva, M.R. and Furthmayr, H. (1995) Subcellular localization of moesin in dynamic filopodia, retraction fibers and other structures involved in substrate exploration, attachment and cell-cell contacts. Exp. Cell Res., 219, 180-196.
4. Andreoli, C., Martin, M., Le Borgne, R., Reggio, H. and Mangeat,P. (1994) Ezrin has properties to self-associate at the plasma membrane. J. Cell Sci., 107, 2509-2521.
5. Arpin, M., Algrain, M. and Louvard, D. (1994) Membrane-actin microfilament connections: an increasing diversity of players related to band 4.1. Curr. Opin. Cell Biol., 6, 136-141.
6. Barreiro, O., Yánez-Mó, M., Serrador, J.M., Montoya, M.C., Vicente-Manzanares, M., Tejedor, R., Furthmayr, H. and Sánchez-Madrid, F. (2002) Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol., 157, 1233-1245.
7. 2-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol., 151, 1067-1080.
8. Bretscher, A. (1999) Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr. Opin. Cell Biol., 11, 109-116.
9. Bretscher, A., Chambers, D., Nguyen, R. and Reczek, D. (2000) ERM- Merlin and EBP50 protein families in plasma membrane organization and function. Annu. Rev. Cell. Dev. Biol., 16, 113-143.
10. Brünger, A.T. et al. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D, 54, 905-921.
11. Calderwood, D.A., Zent, R., Grant, R., Rees, D.J., Hynes, R.O. and Ginsberg, M.H. (1999) The Talin head domain binds to integrin β subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem., 274, 28071-28074.
12. Chishti, A.H. et al. (1998) The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci., 23, 281-282.
13. Delon, J., Kaibuchi, K. and Germain, R.N. (2001) Exclusion of CD43 from the immunological synapse is mediated by phosphorylation-regulated relocation of the cytoskeletal adaptor moesin. Immunity, 15, 691-701.
14. Dickson, T.C., Mintz, C.D., Benson, D.L. and Salton, S.R.J. (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell Biol., 157, 1105-1112.
15. Dhe-Paganon, S., Ottinger, E.A., Nolte, R.T., Eck, M.J. and Shoelson, S.E. (1999) Crystal structure of the pleckstrin homology-phosphotyrosine binding (PH-PTB) targeting region of insulin receptor substrate 1. Proc. Natl Acad. Sci. USA, 96, 8378-8383.
16. Dorner, C., Ciossek, T., Müller, S., Møller, N.P.H., Ullrich, A. and Lammers,R. (1998) Characterization of KIF1C, a new kinesin-like protein involved in vesicle transport from the Golgi apparatus to the endoplasmic reticulum. J. Biol. Chem., 273, 20267-20275.
17. Eck, M.J., Dhe-Paganon, S., Trüb, T., Nolte, R.T. and Shoelson, S.E. (1996) Structure of the IRS-1 PTB domain bound to the juxtamembrane region of the insulin receptor. Cell, 85, 695-705.
18. Franck, Z., Gary, R. and Bretscher, A. (1993) Moesin, like ezrin, colocalizes with actin in the cortical cytoskeleton in cultured cells, but its expression is more variable. J. Cell Sci., 105, 219-231.
19. 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.
20. Girault, J.A., Labesse, G., Momon, J.P. and Callebaut, I. (1999) The N-termini of FAK and JAKs contain divergent band 4.1 domains. Trends Biochem. Sci., 24, 54-57.
21. Hamada, K., Shimizu, T., Matsui, T., Tsukita, Sh., Tsukita, Sa. and Hakoshima, T. (2000) Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J., 19, 4449-4462.
22. Hamada, K., Shimizu, T., Matsui, T., Tsukita, Sh., Tsukita, Sa. and Hakoshima, T. (2001) Crystallographic characterization of the radixin FERM domain bound to the cytosolic tail of the adhesion molecule ICAM-2. Acta Crystallogr. D, 57, 891-892.
23. 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.
24. Helander, T.S., Carpen, 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.
25. Hirao, M., Sato, N., Kondo, T., Yonemura, S., Monden, M., Sasaki, T., Takai, Y., Tsukita, Sh. and Tsukita, Sa. (1996) Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rhodependent signaling pathway. J. Cell Biol., 135, 37-51.
26. Huber, A.H. and Weis, W.I. (2001) The structure of the β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell, 105, 391-402.
27. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
28. Jons, T. and Drenckhahn, D. (1992) Identification of the binding interface involved in linkage of cytoskeletal protein 4.1 to the erythrocyte anion exchanger. EMBO J., 11, 2863-2867.
29. Kang, B.S., Cooper, D.R., Devedjiev, Y., Derewenda, U. and Derewenda, Z.S. (2002) The structure of the FERM domain of merlin, the neurofibromatosis type 2 gene product. Acta Crystallogr. D, 58, 381-391.
30. Kraulis, P.J. (1991) MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
31. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton,J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
32. Li, S.C., Zwahlen, C., Vincent, S.J., McGlade, C.J., Kay, L.E., Pawson, T. and Forman-Kay,J.D. (1998) Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity. Nat. Struct. Biol., 5, 1075-1083.
33. Lickert, H., Bauer, A., Kemler, R. and Stappert,J. (2000) Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β-catenin interaction and strengthens cell-cell adhesion. J. Biol. Chem., 275, 5090-5095.
34. Magendantz, M., Henry, M.D., Lander, A. and Solomon,F. (1995) Interdomain interactions of radixin in vitro. J. Biol. Chem., 270, 25324-25327.
35. Mangeat, P., Roy, C. and Martin,M. (1999) ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol., 9, 187-192.
36. 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.
37. Navaza, J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr. A, 50, 157-163.
38. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
39. 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.
40. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
41. 3 cytoplasmic tail. J. Biol. Chem., 274, 28575-28583.
42. 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.
43. Rossmann, M.G. and van Beek,C.G. (1999) Data processing. Acta Crystallogr. D, 55, 1631-1640.
44. Rouleau, G.A. et al. (1993) Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature, 363, 515-521.
45. Sato, N., Yonemura, S., Obinata, T., Tsukita, Sa. and Tsukita, Sh. (1991) Radixin, a barbed end-capping actin-modulating protein, is concentrated at the cleavage furrow during cytokinesis. J. Cell Biol., 113, 321-330.
46. Sato, N., Funayama, N., Nagafuchi, A., Yonemura, S., Tsukita, Sa. and Tsukita, Sh. (1992) A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J. Cell Sci., 103, 131-143.
47. Sato, T., Irie, S., Kitada, S. and Reed,J.C. (1995) FAP-1: a protein tyrosine phosphatase that associates with Fas. Science, 268, 411-415.
48. Schultz, J., Milpetz, F., Bork, P. and Ponting,C.P. (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl Acad. Sci. USA, 95, 5857-5864.
49. 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.
50. Serrador, J.M. et al. (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.
51. Shaw, A.S. (2001) FERMing up the synapse. Immunity, 15, 683-686.
52. Shimizu, T., Seto, A., Maita, N., Hamada, K., Tsukita, Sh., Tsukita, Sa. and Hakoshima, T. (2002) Structural basis or the neurofibromatosis type 2: crystal structure of the Merlin FERM domain. J. Biol. Chem., 277, 10332-10336.
53. Takeuchi, K., Kawashima, A., Nagafuchi, A. and Tsukita, Sh. (1994) Structural diversity of band 4.1 superfamily members. J. Cell Sci., 107, 1921-1928.
54. Trofatter, J.A. et al. (1993) A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell, 72, 791-800.
55. Tsukita, Sa., Oishi, K., Sato, N., Sagara, J., Kawai, A. and Tsukita,Sh. (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol., 126, 391-401.
56. Tsukita, Sa. and Yonemura,S. (1999) Cortical actin organization: lessons from ERM (Ezrin/Radixin/Moesin) proteins. J. Biol. Chem., 274, 34507-34510.
57. 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.
58. Yonemura, S., Nagafuchi, A., Sato, N. and Tsukita, Sh. (1993) Concentration of an integral membrane protein, CD43 (leukosialin, sialophorin), in the cleavage furrow through the interaction of its cytoplasmic domain with actin-based cytoskeletons. J. Cell Biol., 120, 437-449.
59. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., Tsukita, Sa. and Tsukita, Sh. (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.
60. Yonemura, S., Matsui, T., Tsukita, Sh. and Tsukita,Sa. (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.
61. Zhang, Z., Lee, C.H., Mandiyan, V., Borg, J.P., Margolis, B., Schlessinger, J. and Kuriyan,J. (1997) Sequence-specific recognition of the internalization motif of the Alzheimer's amyloid precursor protein by the X11 PTB domain. EMBO J., 16, 6141-6150.