Binding of moesin and ezrin to membranes containing phosphatidylinositol (4,5) bisphosphate: A comparative study of the affinity constants and conformational changes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 11, 2012, Pages 2839-2849

  Maniti, Ofelia ^a   Khalifat, Nada ^b   Goggia, Kriti ^a   Dalonneau, Fabien ^a   Guérin, Christophe ^c   Blanchoin, Laurent ^c   Ramos, Laurence ^b   Picart, Catherine ^a  

^a GRENOBLE INSTITUTE OF TECHNOLOGY   (France)

^b UNIVERSITÉ MONTPELLIER 2   (France)

^c CEA GRENOBLE   (France)

Author keywords

ERM protein; Fluorescence spectroscopy; Infrared spectroscopy; Membrane protein interaction; Phosphoinositide; Vesicles

Indexed keywords

EZRIN; MOESIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RADIXIN;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; BIOMIMETICS; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; FLUORESCENCE SPECTROSCOPY; INFRARED SPECTROSCOPY; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

BIOMIMETICS; CYTOSKELETAL PROTEINS; MEMBRANES, ARTIFICIAL; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; PROTEOLYSIS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84864465448     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.07.004     Document Type: Article

References (40)

1. R.G. Fehon, A.I. McClatchey, and A. Bretscher Organizing the cell cortex: the role of ERM proteins Nat. Rev. Mol. Cell Biol. 11 2010 276 287
2. V. Niggli, and J. Rossy Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton Int. J. Biochem. Cell Biol. 40 2008 344 349 (Pubitemid 351241219)
3. Y. Doi, M. Itoh, S. Yonemura, S. Ishihara, H. Takano, T. Noda, and S. Tsukita 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 1999 2315 2321
4. S. Kikuchi, M. Hata, K. Fukumoto, Y. Yamane, T. Matsui, A. Tamura, S. Yonemura, H. Yamagishi, D. Keppler, S. Tsukita, and S. Tsukita Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes Nat. Genet. 31 2002 320 325
5. I. Saotome, M. Curto, and A.I. McClatchey Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine Dev. Cell 6 2004 855 864 (Pubitemid 38745419)
6. B.E. Elliott, J.A. Meens, S.K. SenGupta, D. Louvard, and M. Arpin The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells Breast Cancer Res. 7 2005 R365 R373
7. K.W. Hunter Ezrin, a key component in tumor metastasis Trends Mol. Med. 10 2004 201 204 (Pubitemid 38581790)
8. C. Khanna, X. Wan, S. Bose, R. Cassaday, O. Olomu, A. Mendoza, C. Yeung, R. Gorlick, S.M. Hewitt, and L.J. Helman The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis Nat. Med. 10 2004 182 186 (Pubitemid 38524889)
9. Y. Yu, J. Khan, C. Khanna, L. Helman, P.S. Meltzer, and G. Merlino Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators Nat. Med. 10 2004 175 181 (Pubitemid 38524888)
10. A. Estecha, L. Sanchez-Martin, A. Puig-Kroger, R.A. Bartolome, J. Teixido, R. Samaniego, and P. Sanchez-Mateos Moesin orchestrates cortical polarity of melanoma tumour cells to initiate 3D invasion J. Cell Sci. 122 2009 3492 3501
11. T. Ilani, C. Khanna, M. Zhou, T.D. Veenstra, and A. Bretscher Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin J. Cell Biol. 179 2007 733 746 (Pubitemid 350146258)
12. M.H. Shaffer, R.S. Dupree, P. Zhu, I. Saotome, R.F. Schmidt, A.I. McClatchey, B.D. Freedman, and J.K. Burkhardt Ezrin and moesin function together to promote T cell activation J. Immunol. 182 2009 1021 1032
13. M. Barrero-Villar, J.R. Cabrero, M. Gordon-Alonso, J. Barroso-Gonzalez, S. Alvarez-Losada, M.A. Munoz-Fernandez, F. Sanchez-Madrid, and A. Valenzuela-Fernandez Moesin is required for HIV-1-induced CD4-CXCR4 interaction, F-actin redistribution, membrane fusion and viral infection in lymphocytes J. Cell Sci. 122 2009 103 113
14. M.A. Pearson, D. Reczek, A. Bretscher, and P.A. Karplus Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain Cell 101 2000 259 270
15. C. Barret, C. Roy, P. Montcourrier, P. Mangeat, and V. Niggli Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2)) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution J. Cell Biol. 151 2000 1067 1080
16. B.T. Fievet, A. Gautreau, C. Roy, L. Del Maestro, P. Mangeat, D. Louvard, and M. Arpin Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin J. Cell Biol. 164 2004 653 659 (Pubitemid 38282949)
17. M. Hirao, N. Sato, T. Kondo, S. Yonemura, M. Monden, T. Sasaki, Y. Takai, S. Tsukita, and S. Tsukita 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 1996 37 51 (Pubitemid 26337735)
18. J.J. Hao, Y. Liu, M. Kruhlak, K.E. Debell, B.L. Rellahan, and S. Shaw Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane J. Cell Biol. 184 2009 451 462
19. S. Yonemura, T. Matsui, S. Tsukita, and S. Tsukita Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo J. Cell Sci. 115 2002 2569 2580 (Pubitemid 34778074)
20. J. Saarikangas, H. Zhao, and P. Lappalainen Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides Physiol. Rev. 90 2010 259 289
21. G. Blin, E. Margeat, K. Carvalho, C.A. Royer, C. Roy, and C. Picart Quantitative analysis of the binding of ezrin to large unilamellar vesicles containing phosphatidylinositol 4,5 bisphosphate Biophys. J. 94 2008 1021 1033 (Pubitemid 351162465)
22. C. Roy, M. Martin, and P. Mangeat A dual involvement of the amino-terminal domain of ezrin in F- and G-actin binding J. Biol. Chem. 272 1997 20088 20095 (Pubitemid 27340115)
23. K. Carvalho, L. Ramos, C. Roy, and C. Picart Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: characterization and functionality Biophys. J. 95 2008 4348 4360
24. K. Carvalho, N. Khalifat, O. Maniti, C. Nicolas, S. Arold, C. Picart, and L. Ramos Phosphatidylinositol 4,5-bisphosphate-induced conformational change of ezrin and formation of ezrin oligomers Biochemistry 49 2010 9318 9327
25. A. Shcherbina, A. Bretscher, D.M. Kenney, and E. Remold-O'Donnell Moesin, the major ERM protein of lymphocytes and platelets, differs from ezrin in its insensitivity to calpain FEBS Lett. 443 1999 31 36 (Pubitemid 29073389)
26. A. Barth Infrared spectroscopy of proteins Biochim. Biophys. Acta 1767 2007 1073 1101 (Pubitemid 47313388)
27. W.K. Surewicz, H.H. Mantsch, and D. Chapman Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment Biochemistry 32 1993 389 394 (Pubitemid 23034873)
28. E. Goormaghtigh, V. Cabiaux, and J.M. Ruysschaert Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. Assignments and model compounds H.J. Hilderson, G.B. Ralston, Subcellular Biochemistry: Physicochemical Methods in the Study of Biomembranes vol. 23 1994 Plenum Press New York 329 361
29. A. Herrig, M. Janke, J. Austermann, V. Gerke, A. Janshoff, and C. Steinem Cooperative adsorption of ezrin on PIP2-containing membranes Biochemistry 45 2006 13025 13034 (Pubitemid 44763425)
30. F. Roch, C. Polesello, C. Roubinet, M. Martin, C. Roy, P. Valenti, S. Carreno, P. Mangeat, and F. Payre Differential roles of PtdIns(4,5)P2 and phosphorylation in moesin activation during Drosophila development J. Cell Sci. 123 2010 2058 2067
31. V. Papayannopoulos, C. Co, K.E. Prehoda, S. Snapper, J. Taunton, and W.A. Lim A polybasic motif allows N-WASP to act as a sensor of PIP(2) density Mol. Cell 17 2005 181 191 (Pubitemid 40138614)
32. A. Seelig, X.L. Blatter, A. Frentzel, and G. Isenberg Phospholipid binding of synthetic talin peptides provides evidence for an intrinsic membrane anchor of talin J. Biol. Chem. 275 2000 17954 17961 (Pubitemid 30414739)
33. S. Bosk, J.A. Braunger, V. Gerke, and C. Steinem Activation of F-actin binding capacity of ezrin: synergism of PIP interaction and phosphorylation Biophys. J. 100 2011 1708 1717
34. Q. Li, M.R. Nance, R. Kulikauskas, K. Nyberg, R. Fehon, P.A. Karplus, A. Bretscher, and J.J. Tesmer Self-masking in an intact ERM-merlin protein: an active role for the central alpha-helical domain J. Mol. Biol. 365 2007 1446 1459 (Pubitemid 46055267)
35. K.P. Hoeflich, S. Tsukita, L. Hicks, C.M. Kay, S. Tsukita, and M. Ikura Insights into a single rod-like helix in activated radixin required for membrane-cytoskeletal cross-linking Biochemistry 42 2003 11634 11641 (Pubitemid 37243623)
36. S.D. Edwards, and N.H. Keep The 2.7 A crystal structure of the activated FERM domain of moesin: an analysis of structural changes on activation Biochemistry 40 2001 7061 7068 (Pubitemid 32554027)
37. K. Hamada, T. Shimizu, T. Matsui, S. Tsukita, and T. Hakoshima Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain EMBO J. 19 2000 4449 4462
38. K. Kitano, F. Yusa, and T. Hakoshima Structure of dimerized radixin FERM domain suggests a novel masking motif in C-terminal residues 295-304 Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 2006 340 345
39. H.S. Saleh, U. Merkel, K.J. Geissler, T. Sperka, A. Sechi, C. Breithaupt, and H. Morrison Properties of an ezrin mutant defective in F-actin binding J. Mol. Biol. 385 2009 1015 1031
40. C. Roubinet, B. Decelle, G. Chicanne, J.F. Dorn, B. Payrastre, F. Payre, and S. Carreno Molecular networks linked by Moesin drive remodeling of the cell cortex during mitosis J. Cell Biol. 195 2011 99 112