Structure and dynamics of helix-0 of the N-BAR domain in lipid micelles and bilayers

Biophysical Journal

Volumn 95, Issue 9, 2008, Pages 4315-4323

  Löw, Christian ^a   Weininger, Ulrich ^a   Lee, Hwankyu ^b   Schweimer, Kristian ^c   Neundorf, Ines ^d   Beck Sickinger, Annette G ^d   Pastor, Richard W ^c   Balbach, Jochen ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c UNIVERSITY OF BAYREUTH   (Germany)

^d UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; BIN1 PROTEIN, HUMAN; DETERGENT; NUCLEAR PROTEIN; PROTON; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE; METABOLISM; MICELLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; TIME;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMIDES; DETERGENTS; HUMANS; HYDROPHOBICITY; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANES; MICELLES; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTONS; STATIC ELECTRICITY; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 58149164579     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.134155     Document Type: Article

References (52)

1. David, C., P. S. McPherson, O. Mundigl, and P. de Camilli. 1996. A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA. 93:331-335.
2. Shupliakov, O., P. Low, D. Grabs, H. Gad, H. Chen, C. David, K. Takei, P. De Camilli, and L. Brodin. 1997. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science. 276:259-263.
3. Ren, G., P. Vajjhala, J. S. Lee, B. Winsor, and A. L. Munn. 2006. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70:37-120.
4. Di Paolo, G., S. Sankaranarayanan, M. R. Wenk, L. Daniell, E. Perucco, B. J. Caldarone, R. Flavell, M. R. Picciotto, T. A. Ryan, O. Cremona, and P. De Camilli. 2002. Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron. 33:789-804.
5. Zhang, B., and A. C. Zelhof. 2002. Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp. Traffic. 3:452-460.
6. Lee, E., M. Marcucci, L. Daniell, M. Pypaert, O. A. Weisz, G. C. Ochoa, K. Farsad, M. R. Wenk, and P. De Camilli. 2002. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science. 297:1193-1196.
7. McMahon, H. T., and J. L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 438:590-596.
8. Dawson, J. C., J. A. Legg, and L. M. Machesky. 2006. Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16:493-498.
9. Shimada, A., H. Niwa, K. Tsujita, S. Suetsugu, K. Nitta, K. Hanawa-Suetsugu, R. Akasaka, Y. Nishino, M. Toyama, L. Chen, Z. J. Liu, B. C. Wang, M. Yamamoto, T. Terada, A. Miyazawa, A. Tanaka, S. Sugano, M. Shirouzu, K. Nagayama, T. Takenawa, and S. Yokoyama. 2007. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell. 129:761-772.
10. Henne, W. M., H. M. Kent, M. G. Ford, B. G. Hegde, O. Daumke, P. J. Butler, R. Mittal, R. Langen, P. R. Evans, and H. T. McMahon. 2007. Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure. 15:839-852.
11. Nicot, A. S., A. Toussaint, V. Tosch, C. Kretz, C. Wallgren-Pettersson, E. Iwarsson, H. Kingston, J. M. Garnier, V. Biancalana, A. Oldfors, J. L. Mandel, and J. Laporte. 2007. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat. Genet. 39:1134-1139.
12. Casal, E., L. Federici, W. Zhang, J. Fernandez-Recio, E. M. Priego, R. N. Miguel, J. B. DuHadaway, G. C. Prendergast, B. F. Luisi, and E. D. Laue. 2006. The crystal structure of the BAR domain from human Bin1/amphiphysin II and its implications for molecular recognition. Biochemistry. 45:12917-12928.
13. Peter, B. J., H. M. Kent, I. G. Mills, Y. Vallis, P. J. Butler, P. R. Evans, and H. T. McMahon. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 303:495-499.
14. Fernandes, F. M., L. M. Loura, F. J. Chichon, J. L. Carrascosa, A. Fedorov, and M. Prieto. 2008. Role of Helix-0 of the N-BAR domain in membrane curvature generation. Biophys. J. 94:3065-3073.
15. Takei, K., V. I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39.
16. Blood, P. D., and G. A. Voth. 2006. Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc. Natl. Acad. Sci. USA. 103:15068-15072.
17. Farsad, K., N. Ringstad, K. Takei, S. R. Floyd, K. Rose, and P. De Camilli. 2001. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155:193-200.
18. Ford, M. G., I. G. Mills, B. J. Peter, Y. Vallis, G. J. Praefcke, P. R. Evans, and H. T. McMahon. 2002. Curvature of clathrin-coated pits driven by epsin. Nature. 419:361-366.
19. Lee, M. C., L. Orci, S. Hamamoto, E. Futai, M. Ravazzola, and R. Schekman. 2005. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell. 122:605-617.
20. Gallop, J. L., C. C. Jao, H. M. Kent, P. J. Butler, P. R. Evans, R. Langen, and H. T. McMahon. 2006. Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25:2898-2910.
21. Masuda, M., S. Takeda, M. Sone, T. Ohki, H. Mori, Y. Kamioka, and N. Mochizuki. 2006. Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25:2889-2897.
22. Zimmerberg, J., and M. M. Kozlov. 2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9-19.
23. Bosse-Doenecke, E., U. Weininger, M. Gopalswamy, J. Balbach, S. Möller Knudsen, and R. Rudolph. 2008. High yield production of recombinant native and modified peptides exemplified by ligands for G-protein coupled receptors. Protein Expr. Purif. 58:114-121.
24. Koide, S., W. Jahnke, and P. E. Wright. 1995. Measurement of intrinsic exchange rates of amide protons in a 15N-labeled peptide. J. Biomol. NMR. 6:306-312.
25. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, and A. Bax. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:277-293.
26. Johnson, B. A. 2004. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278:313-352.
27. Linge, J. P., M. Habeck, W. Rieping, and M. Nilges. 2003. ARIA: automated NOE assignment and NMR structure calculation. Bioinformatics. 19:315-316.
28. Cornilescu, G., F. Delaglio, and A. Bax. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:289-302.
29. Laskowski, R. A., J. A. Rullmannn, M. W. MacArthur, R. Kaptein, and J. M. Thornton. 1996. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:477-486.
30. MacKerell, A. D., Jr., M. Feig, and C. L. Brooks 3rd. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25:1400-1415.
31. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. J. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem. 4:187-217.
32. Oostenbrink, C., A. Villa, A. E. Mark, and W. F. van Gunsteren. 2004. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 25:1656-1676.
33. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential functions for proteins. Energy minimization for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
34. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7:306-317.
35. van der Spoel, D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, and H. J. Berendsen. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
36. Schüttelkopf, 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.
37. MacKerell, A. D., Jr. 1995. Molecular dynamics simulation analysis of a sodium dodecyl sulfate micelle in aqueous solution: decreased fluidity of the micelle hydrocarbon interior. J. Phys. Chem. 99:1846-1855.
38. Bales, B. L., and M. Almgren. 1995. Fluorescence quenching of pyrene by copper (II) in sodium dodecyl sulfate micelles. Effect of micelle size as controlled by surfactant concentration. J. Phys. Chem. 99:15153-15162.
39. Faraldo-Gomez, J. D., G. R. Smith, and M. S. Sansom. 2002. Setting up and optimization of membrane protein simulations. Eur. Biophys. J. 31:217-227.
40. Sanner, M. F., A. J. Olson, and J. C. Spehner. 1996. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers. 38:305-320.
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. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
43. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. Dinola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
44. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
45. Gallop, J. L., and H. T. McMahon. 2005. BAR domains and membrane curvature: bringing your curves to the BAR. Biochem. Soc. Symp. 223-231.
46. Han, X., J. H. Bushweller, D. S. Cafiso, and L. K. Tamm. 2001. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:715-720.
47. Liang, B., and L. K. Tamm. 2007. Structure of outer membrane protein G by solution NMR spectroscopy. Proc. Natl. Acad. Sci. USA. 104:16140-16145.
48. Kessler, H., D. F. Mierke, J. Saulitis, S. Seip, S. Steuernagel, T. Wein, and M. Will. 1992. The structure of Ro 09-0198 in different environments. Biopolymers. 32:427-433.
49. Koppitz, M., B. Mathä, and H. Kessler. 1999. Structure investigation of amphiphilic cyclopeptides in isotropic and anisotropic environments-A model study simulating peptide-membrane interactions. J. Pept. Sci. 5:507-518.
50. Neumoin, A., B. Arshava, J. Becker, O. Zerbe, and F. Naider. 2007. NMR studies in dodecylphosphocholine of a fragment containing the seventh transmembrane helix of a G-protein-coupled receptor from Saccharomyces cerevisiae. Biophys. J. 93:467-482.
51. Richnau, N., A. Fransson, K. Farsad, and P. Aspenstrom. 2004. RICH-1 has a BIN/Amphiphysin/Rvsp domain responsible for binding to membrane lipids and tubulation of liposomes. Biochem. Biophys. Res. Commun. 320:1034-1042.
52. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.