NMR analyses of the interaction between the FYVE domain of Early Endosome Antigen 1 (EEA1) and phosphoinositide embedded in a lipid bilayer

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 34936-34945

  Yokogawa, Mariko ^a   Kobashigawa, Yoshihiro ^a   Yoshida, Naoki ^a   Ogura, Kenji ^a   Harada, Kohsuke ^a   Inagaki, Fuyuhiko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BI-LAYER; CELLULAR PROCESS; CHEMICAL SHIFT PERTURBATIONS; CROSS-SATURATION; EARLY ENDOSOME ANTIGEN 1; MODEL SYSTEM; NANO SCALE; NANODISCS; NMR ANALYSIS; PARAMAGNETIC RELAXATION ENHANCEMENTS; PHOSPHOINOSITIDES; PROTEIN-MEMBRANE INTERACTIONS; QUANTITATIVE EVALUATION; RELATIVE ORIENTATION; STRUCTURAL CHANGE; STRUCTURAL INSIGHTS;

ANTIGENS; LIPID BILAYERS; PARAMAGNETISM; PHOSPHOLIPIDS;

PROTEINS;

EARLY ENDOSOME ANTIGEN 1; MEMBRANE LIPID; PHOSPHATIDYLINOSITIDE;

ARTICLE; EMBEDDING; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SURFACE CHARGE;

HUMANS; LIPID BILAYERS; NANOSTRUCTURES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLINOSITOLS; PROTEIN STRUCTURE, TERTIARY; VESICULAR TRANSPORT PROTEINS;

EID: 84867408256     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398255     Document Type: Article

References (35)

1. Odorizzi, G., Babst, M., and Emr, S. D. (2000) Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25, 229-235 (Pubitemid 30236220)
2. Hurley, J. H., and Meyer, T. (2001) Subcellular targeting by membrane lipids. Curr. Opin. Cell Biol. 13, 146-152 (Pubitemid 32209214)
3. 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 (Pubitemid 32709773)
4. Bravo, J., Karathanassis, D., Pacold, C. M., Pacold, M. E., Ellson, C. D., Anderson, K. E., Butler, P. J., Lavenir, I., Perisic, O., Hawkins, P. T., Stephens, L., and Williams, R. L. (2001) The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol. Cell 8, 829-839
5. Zhou, C. Z., Li de La Sierra-Gallay, I., Quevillon-Cheruel, S., Collinet, B., Minard, P., Blondeau, K., Henckes, G., Aufrère, R., Leulliot, N., Graille, M., Sorel, I., Savarin, P., de la Torre, F., Poupon, A., Janin, J., and van Tilbeurgh, H. (2003) Crystal structure of the yeast Phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate. J. Biol. Chem. 278, 50371-50376
6. Kutateladze, T. G., Capelluto, D. G., Ferguson, C. G., Cheever, M. L., Kutateladze, A. G., Prestwich, G. D., and Overduin, M. (2004) Multivalent mechanism of membrane insertion by the FYVE domain. J. Biol. Chem. 279, 3050-3057 (Pubitemid 38114298)
7. Lee, S. A., Kovacs, J., Stahelin, R. V., Cheever, M. L., Overduin, M., Setty, T. G., Burd, C. G., Cho, W., and Kutateladze, T. G. (2006) Molecular mechanism of membrane docking by the Vam7p PX domain. J. Biol. Chem. 281, 37091-37101 (Pubitemid 46042179)
8. Sankaran, V. G., Klein, D. E., Sachdeva, M. M., and Lemmon, M. A. (2001) High-affinity binding of a FYVE domain to phosphatidylinositol 3-phosphate requires intact phospholipid but not FYVE domain oligomerization. Biochemistry 40, 8581-8587 (Pubitemid 32667265)
9. 2 binding site on p47phox PX domain revealed by NMR. J. Biol. Chem.
10. Stahelin, R. V., Long, F., Diraviyam, K., Bruzik, K. S., Murray, D., and Cho, W. (2002) Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J. Biol. Chem. 277, 26379-26388 (Pubitemid 34967131)
11. Kohda, D., and Inagaki, F. (1992) Structure of epidermal growth factor bound to perdeuterated dodecylphosphocholine micelles determined by two-dimensional NMR and simulated annealing calculations. Biochemistry 31, 677-685
12. Zamoon, J., Mascioni, A., Thomas, D. D., and Veglia, G. (2003) NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 85, 2589-2598 (Pubitemid 37210804)
13. Kami, K., Rajesh, S., and Overduin, M. (2009) Phospholipid-interacting proteins by solution-state NMR spectroscopy. Methods Mol. Biol. 462, 291-306
14. Ritchie, T. K., Grinkova, Y. V., Bayburt, T. H., Denisov, I. G., Zolnerciks, J. K., Atkins, W. M., and Sligar, S. G. (2009) Chapter 11 - Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 464, 211-231
15. Bayburt, T. H., and Sligar, S. G. (2010) Membrane protein assembly into nanodiscs. FEBS Lett. 584, 1721-1727
16. Kobashigawa, Y., Harada, K., Yoshida, N., Ogura, K., and Inagaki, F. (2011) Phosphoinositide-incorporated lipid-protein nanodiscs: A tool for studying protein-lipid interactions. Anal. Biochem. 410, 77-83
17. Dumas, J. J., Merithew, E., Sudharshan, E., Rajamani, D., Hayes, S., Lawe, D., Corvera, S., and Lambright, D. G. (2001) Multivalent endosome targeting by homodimeric EEA1. Mol. Cell 8, 947-958 (Pubitemid 34031798)
18. Kobashigawa, Y., Kumeta, H., Ogura, K., and Inagaki, F. (2009) Attachment of an NMR-invisible solubility enhancement tag using a sortase-mediated protein ligation method. J. Biomol. NMR 43, 145-150
19. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
20. Mulder, F. A., Schipper, D., Bott, R., and Boelens, R. (1999) Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292, 111-123 (Pubitemid 29425657)
21. Nishida, N., and Shimada, I. (2012) An NMR method to study protein-protein interactions. Methods Mol. Biol. 757, 129-137
22. Matsuo, H., Walters, K. J., Teruya, K., Tanaka, T., Gassner, G. T., Lippard, S. J., Kyogoku, Y., and Wagner, G. (1999) Identification by NMR spectroscopy of residues at contact surfaces in large, slowly exchanging macromolecular complexes. J. Am. Chem. Soc. 121, 9903-9904 (Pubitemid 29517442)
23. Shimada, I. (2005) NMR techniques for identifying the interface of a larger protein-protein complex: cross-saturation and transferred cross-saturation experiments. Methods Enzymol. 394, 483-506
24. Takeuchi, K., Takahashi, H., Sugai, M., Iwai, H., Kohno, T., Sekimizu, K., Natori, S., and Shimada, I. (2004) Channel-forming membrane permeabilization by an antibacterial protein, sapecin: determination of membrane-buried and oligomerization surfaces by NMR. J. Biol. Chem. 279, 4981-4987 (Pubitemid 38199094)
25. Jung, H. H., Jung, H. J., Milescu, M., Lee, C. W., Lee, S., Lee, J. Y., Eu, Y. J., Kim, H. H., Swartz, K. J., and Kim, J. I. (2010) Structure and orientation of a voltage-sensor toxin in lipid membranes. Biophys. J. 99, 638-646
26. Nakamura, T., Takahashi, H., Takeuchi, K., Kohno, T., Wakamatsu, K., and Shimada, I. (2005) Direct determination of a membrane-peptide interface using the nuclear magnetic resonance cross-saturation method. Biophys. J. 89, 4051-4055 (Pubitemid 41725625)
27. Matsuda, T., Nakajima, N., Yamazaki, T., and Nakamura, H. (2004) CADICAD complex structure derived from saturation transfer experiment and simulated annealing without using pairwise NOE information. J. Mol. Recognit. 17, 41-50 (Pubitemid 38231463)
28. He, J., Vora, M., Haney, R. M., Filonov, G. S., Musselman, C. A., Burd, C. G., Kutateladze, A. G., Verkhusha, V. V., Stahelin, R. V., and Kutateladze, T. G. (2009) Membrane insertion of the FYVE domain is modulated by pH. Proteins 76, 852-860
29. Kutateladze, T., and Overduin, M. (2001) Structural mechanism of endosome docking by the FYVE domain. Science 291, 1793-1796 (Pubitemid 32198985)
30. Gaullier, J. M., Ronning, E., Gillooly, D. J., and Stenmark, H. (2000) Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues. J. Biol. Chem. 275, 24595-24600 (Pubitemid 30626557)
31. Kutateladze, T. G., Ogburn, K. D., Watson, W. T., de Beer, T., Emr, S. D., Burd, C. G., and Overduin, M. (1999) Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol. Cell 3, 805-811 (Pubitemid 29323059)
32. Malmberg, N. J., and Falke, J. J. (2005) Use of EPR power saturation to analyze the membrane-docking geometries of peripheral proteins: applications to C2 domains. Annu. Rev. Biophys. Biomol. Struct. 34, 71-90 (Pubitemid 40847719)
33. 2+ ligands and membrane binding residues. J. Biol. Chem. 273, 17544-17552
34. Málková, S., Long, F., Stahelin, R. V., Pingali, S. V., Murray, D., Cho, W., and Schlossman, M. L. (2005) X-ray reflectivity studies of cPLA2α-C2 domains adsorbed onto Langmuir monolayers of SOPC. Biophys. J. 89, 1861-1873 (Pubitemid 41233541)
35. Hong, M., and Su, Y. (2011) Structure and dynamics of cationic membrane peptides and proteins: insights from solid-state NMR. Protein Sci. 20, 641-655