Lipid interaction networks of peripheral membrane proteins revealed by data-driven micelle docking

Biophysical Journal

Volumn 94, Issue 2, 2008, Pages 515-524

  Dancea, Felician ^a   Kami, Keiichiro ^a   Overduin, Michael ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY ENDOSOME ANTIGEN 1; MEMBRANE PROTEIN; DODECYLPHOSPHORYLCHOLINE; DRUG DERIVATIVE; PHOSPHORYLCHOLINE;

ARTICLE; CELL MEMBRANE; MICELLE; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE; PHAGOCYTE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; THREE DIMENSIONAL IMAGING; ZINC FINGER MOTIF; CHEMICAL STRUCTURE; CHEMISTRY; LIPID METABOLISM; METABOLISM; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

LIPID METABOLISM; MEMBRANE PROTEINS; MICELLES; MODELS, MOLECULAR; PHOSPHORYLCHOLINE; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 38349035977     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.115923     Document Type: Article

References (51)

1. Cho, W., and R. V. Stahelin. 2005. Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34:119-151.
2. Lin, Y., R. Nielsen, D. Murray, W. L. Hubbell, C. Mailer, B. H. Robinson, and M. H. Gelb. 1998. Docking phospholipase A2 on membranes using electrostatic potential-modulated spin relaxation magnetic resonance. Science. 279:1925-1929.
3. Frazier, A. A., M. A. Wisner, N. J. Malmberg, K. G. Victor, G. E. Fanucci, E. A. Nalefski, J. J. Falke, and D. S. Cafiso. 2002. Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry. 41:6282-6292.
4. Kohout, S. C., S. Corbalan-Garcia, J. C. Gomez-Fernandez, and J. J. Falke. 2003. C2 domain of protein kinase C alpha: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling. Biochemistry. 42:1254-1265.
5. Malmberg, N. J., and J. J. Falke. 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.
6. Chapman, E. R., and A. F. Davis. 1998. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 273:13995-14001.
7. Perisic, O., H. F. Paterson, G. Mosedale, S. Lara-Gonzalez, and R. L. Williams. 1999. Mapping the phospholipid-binding surface and translocation determinants of the C2 domain from cytosolic phospholipase A2. J. Biol. Chem. 274:14979-14987.
8. Medkova, M., and W. Cho. 1999. Interplay of C1 and C2 domains of protein kinase C-alpha in its membrane binding and activation. J. Biol. Chem. 274:19852-19861.
9. Stahelin, R. V., F. Long, K. Diraviyam, K. S. Bruzik, D. Murray, and W. Cho. 2002. Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J. Biol. Chem. 277:26379-26388.
10. Stahelin, R. V., A. Burian, K. S. Bruzik, D. Murray, and W. Cho. 2003. Membrane binding mechanisms of the PX domains of NADPH oxidase p40phox and p47phox. J. Biol. Chem. 278:14469-14479.
11. Malkova, S., F. Long, R. V. Stahelin, S. V. Pingali, D. Murray, W. Cho, and M. L. Schlossman. 2005. X-ray reflectivity studies of cPLA2(alpha)-C2 domains adsorbed onto Langmuir monolayers of SOPC. Biophys. J. 89:1861-1873.
12. phox-PX. Biochemistry. 45:13566-13575.
13. Allegrini, P. R., G. J. van Scharrenburg, A. J. Slotboom, G. H. de Haas, and J. Seelig. 1985. Side-chain dynamics of two aromatic amino acids in pancreatic phospholipase A2 as studied by deuterium nuclear magnetic resonance. Biochemistry. 24:3268-3273.
14. Tuzi, S., N. Uekama, M. Okada, S. Yamaguchi, H. Saito, and H. Yagisawa. 2003. Structure and dynamics of the phospholipase C-delta1 pleckstrin homology domain located at the lipid bilayer surface. J. Biol. Chem. 278:28019-28025.
15. Roberts, M. F., and A. G. Redfield. 2004. High-resolution 31p field cycling NMR as a probe of phospholipid dynamics. J. Am. Chem. Soc. 126:13765-13777.
16. Vogel, A., K. T. Tan, H. Waldmann, S. E. Feller, M. F. Brown, and D. Huster. 2007. Flexibility of Ras lipid modifications studied by 2H solid-state NMR and molecular dynamics simulations. Biophys. J. 93:2697-2712.
17. Kohda, D., and F. Inagaki. 1992. Structure of epidermal growth factor bound to perdeuterated dodecylphosphocholine micelles determined by two-dimensional NMR and simulated annealing calculations. Biochemistry. 31:677-685.
18. Kutateladze, T., and M. Overduin. 2001. Structural mechanism of endosome docking by the FYVE domain. Science. 291:1793-1796.
19. Zamoon, J., A. Mascioni, D. D. Thomas, and G. Veglia. 2003. NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 85:2589-2598.
20. Del Rio, A., K. Dutta, J. Chavez, I. Ubarretxena-Belandia, and R. Ghose. 2007. Solution structure and dynamics of the N-terminal cytosolic domain of rhomboid intramembrane protease from Pseudomonas aeruginosa: insights into a functional role in intramembrane proteolysis. J. Mol. Biol. 365:109-122.
21. Jaud, S., D. J. Tobias, J. J. Falke, and S. H. White. 2007. Self-induced docking site of a deeply embedded peripheral membrane protein. Biophys. J. 92:517-524.
22. Hritz, J., J. Ulicny, A. Laaksonen, D. Jancura, and P. Miskovsky. 2004. Molecular interaction model for the C1B domain of protein kinase C-gamma in the complex with its activator phorbol-12-myristate-13-acetate in water solution and lipid bilayer. J. Med. Chem. 47:6547-6555.
23. Xu, G. Y., T. McDonagh, H. A. Yu, E. A. Nalefski, J. D. Clark, and D. A. Cumming. 1998. Solution structure and membrane interactions of the C2 domain of cytosolic phospholipase A2. J. Mol. Biol. 280:485-500.
24. Wang, G., J. T. Sparrow, and R. J. Cushley. 1997. The helix-hingehelix structural motif in human apolipoprotein A-I determined by NMR spectroscopy. Biochemistry. 36:13657-13666.
25. Papavoine, C. H., R. N. Konings, C. W. Hilbers, and F. J. van de Ven. 1994. Location of M13 coat protein in sodium dodecyl sulfate micelles as determined by NMR. Biochemistry. 33:12990-12997.
26. Nakamura, T., H. Takahashi, K. Takeuchi, T. Kohno, K. Wakamatsu, and I. Shimada. 2005. Direct determination of a membrane-peptide interface using the nuclear magnetic resonance cross-saturation method. Biophys. J. 89:4051-4055.
27. Kutateladze, T. G., D. G. Capelluto, C. G. Ferguson, M. L. Cheever, A. G. Kutateladze, G. D. Prestwich, and M. Overduin. 2004. Multivalent mechanism of membrane insertion by the FYVE domain. J. Biol. Chem. 279:3050-3057.
28. Lee, S. A., J. Kovacs, R. V. Stahelin, M. L. Cheever, M. Overduin, T. G. Setty, C. G. Burd, W. Cho, and T. G. Kutateladze. 2006. Molecular mechanism of membrane docking by the Vam7p PX domain. J. Biol. Chem. 281:37091-37101.
29. Brunecky, R., S. Lee, P. W. Rzepecki, M. Overduin, G. D. Prestwich, A. G. Kutateladze, and T. G. Kutateladze. 2005. Investigation of the binding geometry of a peripheral membrane protein. Biochemistry. 44:16064-16071.
30. Solomon, I. 1955. Relaxation processes in a system of two spins. Phys. Rev. 99:559-565.
31. 1H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. J. Am. Chem. Soc. 126:5879-5896.
32. Dominguez, C., R. Boelens, and A. M. Bonvin. 2003. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125:1731-1737.
33. Rice, L. M., and A. T. Brunger. 1994. Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins. 19:277-290.
34. Dumas, J. J., E. Merithew, E. Sudharshan, D. Rajamani, S. Hayes, D. Lawe, S. Corvera, and D. G. Lambright. 2001. Multivalent endosome targeting by homodimeric EEA1. Mol. Cell. 8:947-958.
35. Lu, J., J. Garcia, I. Dulubova, T. C. Sudhof, and J. Rizo. 2002. Solution structure of the Vam7p PX domain. Biochemistry. 41:5956-5962.
36. Tieleman, D. P., D. van der Spoel, and H. J. C. Berendsen. 2000. Molecular dynamics simulations of dodecylphosphocholine micelles at three different aggregate sizes: micellar structure and lipid chain relaxation. J. Phys. Chem. B. 104:6380-6388.
37. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
38. Schuttelkopf, A. W., and D. M. van Aalten. 2004. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60:1355-1363.
39. Linge, J. P., M. A. Williams, C. A. Spronk, A. M. Bonvin, and M. Nilges. 2003. Refinement of protein structures in explicit solvent. Proteins. 50:496-506.
40. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential function for proteins. Energy minimization for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
41. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
42. phox bound to phosphatidylinositol 3-phosphate. Mol. Cell. 8:829-839.
43. Zhou, C. Z., I. L. de La Sierra-Gallay, S. Quevillon-Cheruel, B. Collinet, P. Minard, K. Blondeau, G. Henckes, R. Aufrere, N. Leulliot, M. Graille, I. Sorel, P. Savarin, F. de la Torre, A. Poupon, J. Janin, and H. van Tilbeurgh. 2003. Crystal structure of the yeast Phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate. J. Biol. Chem. 278:50371-50376.
44. Koradi, R., M. Billeter, and K. Wuthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55, 29-32.
45. Hubbard, S. J., and J. M. Thornton. 1993. 'NACCESS', Computer Program. Department of Biochemistry and Molecular Biology, University College London, UK.
46. Gaullier, J. M., E. Ronning, D. J. Gillooly, and H. Stenmark. 2000. Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues. J. Biol. Chem. 275:24595-24600.
47. Kutateladze, T. G., K. D. Ogburn, W. T. Watson, T. de Beer, S. D. Emr, C. G. Burd, and M. Overduin. 1999. Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol. Cell. 3:805-811.
48. Hayakawa, A., S. J. Hayes, D. C. Lawe, E. Sudharshan, R. Tuft, K. Fogarty, D. Lambright, and S. Corvera. 2004. Structural basis for endosomal targeting by FYVE domains. J. Biol. Chem. 279:5958-5966.
49. Lomize, M. A., A. L. Lomize, I. D. Pogozheva, and H. I. Mosberg. 2006. OPM: orientations of proteins in membranes database. Bioinformatics. 22:623-625.
50. Cheever, M. L., T. G. Kutateladze, and M. Overduin. 2006. Increased mobility in the membrane targeting PX domain induced by phosphatidylinositol 3-phosphate. Protein Sci. 15:1873-1882.
51. Grzesiek, S., S. J. Stahl, P. T. Wingfield, and A. Bax. 1996. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry. 35:10256-10261.