Phosphatidylinositol 4,5-bisphosphate-induced conformational change of ezrin and formation of ezrin oligomers

Biochemistry

Volumn 49, Issue 43, 2010, Pages 9318-9327

  Carvalho, Kevin ^a,b   Khalifat, Nada ^a   Maniti, Ofelia ^d   Nicolas, Claire ^b,d   Arold, Stefan ^c,e   Picart, Catherine ^b,d   Ramos, Laurence ^a  

^a UNIVERSITÉ MONTPELLIER 2   (France)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^d LABORATOIRE DES MATÉRIAUX ET DU GÉNIE PHYSIQUE   (France)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISPHOSPHATES; CELLULAR EVENTS; CONFORMATIONAL CHANGE; CYTOSKELETONS; DYNAMIC STRUCTURE; IN-VITRO; IN-VIVO; MEMBRANE BINDING; N-TERMINALS; PHOSPHATIDYLINOSITOL; PLASMA MEMBRANES; UNIMOLECULAR; WILD TYPES;

CELL MEMBRANES; CYTOLOGY; OLIGOMERS; PRESSURE EFFECTS;

CLARIFICATION;

EZRIN; MUTANT PROTEIN; OLIGOMER; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; FLUORESCENCE SPECTROSCOPY; IN VITRO STUDY; IN VIVO STUDY; ISOTHERMAL TITRATION CALORIMETRY; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN;

CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; MEMBRANE PROTEINS; MUTANT PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 78049271908     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101141d     Document Type: Article

References (43)

1. Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M., and Gratacap, M. (2001) Phosphoinositides: Key players in cell signalling, in time and space Cell. Signalling 13, 377-387
2. Yin, H. L. and Janmey, P. A. (2003) Phosphoinositide regulation of the actin cytoskeleton Annu. Rev. Physiol. 65, 761-789
3. 2 in cell migration Trends Cell Biol. 16, 276-284
4. Niggli, V. (2005) Regulation of protein activities by phosphoinositide phosphates Annu. Rev. Cell Dev. Biol. 21, 57-79
5. 2 regulation of surface membrane traffic Curr. Opin. Cell Biol. 13, 493-499
6. Simonsen, A., Wurmser, A. E., Emr, S. D., and Stenmark, H. (2001) The role of phosphoinositides in membrane transport Curr. Opin. Cell Biol. 13, 485-492
7. McLaughlin, S. and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics Nature 438, 605-611
8. Mazzotti, G., Zini, N., Rizzi, E., Rizzoli, R., Galanzi, A., Ognibene, A., Santi, S., Matteucci, A., Martelli, A. M., and Maraldi, N. M. (1995) Immunocytochemical detection of phosphatidylinositol 4,5-bisphosphate localization sites within the nucleus J. Histochem. Cytochem. 43, 181-191
9. 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
10. Mangeat, P., Roy, C., and Martin, M. (1999) ERM proteins in cell adhesion and membrane dynamics Trends Cell Biol. 9, 187-192
11. Tsukita, S. and Yonemura, S. (1999) Cortical actin organization: Lessons from ERM (ezrin/radixin/moesin) proteins J. Biol. Chem. 274, 34507-34510
12. Yonemura, 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
13. 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
14. 2-terminal domain of ezrin correlates with its altered cellular distribution J. Cell Biol. 151, 1067-1080
15. Simons, P. C., Pietromonaco, S. F., Reczek, D., Bretscher, A., and Elias, L. (1998) 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
16. 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
17. Berryman, M., Gary, R., and Bretscher, A. (1995) Ezrin oligomers are major cytoskeletal components of placental microvilli: A proposal for their involvement in cortical morphogenesis J. Cell Biol. 131, 1231-1242
18. Bretscher, A., Gary, R., and Berryman, M. (1995) Soluble ezrin purified from placenta exists as stable monomers and elongated dimers with masked C-terminal ezrin-radixin-moesin association domains Biochemistry 34, 16830-16837
19. 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
20. Zhu, L., Liu, Y., and Forte, J. G. (2005) Ezrin oligomers are the membrane-bound dormant form in gastric parietal cells Am. J. Physiol. 288, C1242-C1254
21. Chambers, D. N. and Bretscher, A. (2005) Ezrin mutants affecting dimerization and activation Biochemistry 44, 3926-3932
22. Wang, J., Gambhir, A., Hangyas-Mihalyne, G., Murray, D., Golebiewska, U., and McLaughlin, S. (2002) Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions J. Biol. Chem. 277, 34401-34412
23. Hokanson, D. E. and Ostap, E. M. (2006) Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate Proc. Natl. Acad. Sci. U.S.A. 103, 3118-3123
24. Liu, A. P. and Fletcher, D. A. (2006) Actin polymerization serves as a membrane domain switch in model lipid bilayers Biophys. J. 91, 4064-4070
25. Gokhale, N. A., Abraham, A., Digman, M. A., Gratton, E., and Cho, W. (2005) Phosphoinositide specificity of and mechanism of lipid domain formation by annexin A2-p11 heterotetramer J. Biol. Chem. 280, 42831-42840
26. Wagner, M. L. and Tamm, L. K. (2001) Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers Biophys. J. 81, 266-275
27. Herrig, A., Janke, M., Austermann, J., Gerke, V., Janshoff, A., and Steinem, C. (2006) Cooperative adsorption of ezrin on PIP2-containing membranes Biochemistry 45, 13025-13034
28. 2 of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex J. Cell Biol. 150, 1311-1320
29. 2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins Biochemistry 45, 5725-5732
30. Moens, P. D. and Bagatolli, L. A. (2007) Profilin binding to sub-micellar concentrations of phosphatidylinositol (4,5) bisphosphate and phosphatidylinositol (3,4,5) trisphosphate Biochim. Biophys. Acta 1768, 439-449
31. Roy, C., Martin, M., and Mangeat, P. (1997) A dual involvement of the amino-terminal domain of ezrin in F- and G-actin binding J. Biol. Chem. 272, 20088-20095
32. 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 (Part 9) 2509-2521
33. Huang, F. L. and Huang, K. P. (1991) Interaction of protein kinase C isozymes with phosphatidylinositol 4,5-bisphosphate J. Biol. Chem. 266, 8727-8733
34. Blin, G., Margeat, E., Carvalho, K., Royer, C. A., Roy, C., and Picart, C. (2008) Quantitative analysis of the binding of ezrin to large unilamellar vesicles containing phosphatidylinositol 4,5 bisphosphate Biophys. J. 94, 1021-1033
35. Pain, R. H. (2005) Determining the fluorescence spectrum of a protein, Current Protocols in Protein Science, Chapter 7, Unit 7.7, Wiley, New York.
36. Gorbatyuk, V. Y., Nosworthy, N. J., Robson, S. A., Bains, N. P., Maciejewski, M. W., Dos Remedios, C. G., and King, G. F. (2006) Mapping the phosphoinositide-binding site on chick cofilin explains how PIP2 regulates the cofilin-actin interaction Mol. Cell 24, 511-522
37. Liepina, I., Czaplewski, C., Janmey, P., and Liwo, A. (2003) Molecular dynamics study of a gelsolin-derived peptide binding to a lipid bilayer containing phosphatidylinositol 4,5-bisphosphate Biopolymers 71, 49-70
38. Smith, W. J., Nassar, N., Bretscher, A., Cerione, R. A., and Karplus, P. A. (2003) Structure of the active N-terminal domain of Ezrin. Conformational and mobility changes identify keystone interactions J. Biol. Chem. 278, 4949-4956
39. Li, Q., Nance, M. R., Kulikauskas, R., Nyberg, K., Fehon, R., Karplus, P. A., Bretscher, A., and Tesmer, J. J. (2007) Self-masking in an intact ERM-merlin protein: An active role for the central α-helical domain J. Mol. Biol. 365, 1446-1459
40. 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
41. Saarikangas, J., Zhao, H., and Lappalainen, P. (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides Physiol. Rev. 90, 259-289
42. Charras, G. T., Hu, C. K., Coughlin, M., and Mitchison, T. J. (2006) Reassembly of contractile actin cortex in cell blebs J. Cell Biol. 175, 477-490
43. Carvalho, K., Ramos, L., Roy, C., and Picart, C. (2008) Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: Characterization and functionality Biophys. J. 95, 4348-4360