Modeling a spin-labeled fusion peptide in a membrane: Implications for the interpretation of EPR experiments

Biophysical Journal

Volumn 92, Issue 1, 2007, Pages 10-22

  Sammalkorpi, Maria ^a,b   Lazaridis, Themis ^b  

^a Princeton University   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; MUTANT PROTEIN; NITROXIDE; PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ELECTRON SPIN RESONANCE; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SPIN LABELING;

EID: 33846013206     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.092809     Document Type: Article

References (46)

1. Hubbell, W. L., and C. Altenbach. 1994. Investigation of structure and dynamics in membrane-proteins using site-directed spin labeling. Curr. Opin. Struct. Biol. 4:566-573.
2. Hubbell, W. L., A. Gross, R. Langen, and M. A. Lietzov. 1998. Recent advances in site-directed spin labeling of proteins. Curr. Opin. Struct. Biol. 8:649-656.
3. Borbat, P. P., A. J. Costa-Filho, K. A. Earle, J. K. Moscicki, and J. H. Freed. 2001. Electron spin resonance in studies of membranes and proteins. Science. 291:266-269.
4. Möbius, K., A. Savitsky, C. Wegener, M. Plato, M. Fuchs, A. Schnegg, A. A. Dubinskii, Y. A. Grishin, I. A. Grigor'ev, M. Kühn, D. Duché, H. Zimmermann, and H.-J. Steinhoff. 2005. Combining high-field EPR with site-directed spin-labeling reveals unique information on proteins in action. Magn. Reson. Chem. 43:S4-S19.
5. Hubbell, W. L., H. S. Mchaourab, C. Altenbach, and M. A. Lietzov. 1996. Watching proteins move using site-directed spin-labeling. Structure. 4:779-783.
6. Hubbell, W. L., S. Cafiso, and C. Altenbach. 2000. Identifying conformational changes with site-directed spin-labeling. Nat. Struct. Biol. 7:735-739.
7. Columbus, L., and W. L. Hubbell. 2002. A new spin on protein dynamics. Trends Biochem. Sci. 27:288-295.
8. 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.
9. Fajer, P. G. 2000. Electron spin resonance spectroscopy labeling in peptide and protein analysis. In Encyclopedia of Analytical Chemistry. John Wiley Sons, Chichester, UK.
10. Thorgeirsson, T. E., W. Xiao, L. S. Brown, R. Needleman, J. K. Lanyi, and Y.-K. Shin. 1997. Transient channel-opening in bacteriorhodopsin: an EPR study. J. Mol. Biol. 273:951-957.
11. + channel studied by EPR spectroscopy. Nat. Struct. Biol. 5:459-469.
12. Liu, Y. S., P. Sompornpisut, and E. Perozo. 2001. Structure of the KcsA channel intracellular gate in the open state. Nat. Struct. Biol. 8:883-887.
13. Merianos, H. J., N. Cadieux, C. H. Lin, R. J. Kadner, and D. S. Cafiso. 2000. Substrate-induced exposure of an energy-coupling motif of a membrane transporter. Nat. Struct. Biol. 7:205-209.
14. Mchaourab, H. S., M. A. Lietzov, K. Hideg, and W. L. Hubbell. 1996. Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry. 35:7692-7704.
15. Lietzow, M. A., and W. L. Hubbell. 2004. Motion of spin-label side chains in cellular retinol-binding protein: correlation with structure and nearest-neighbor interactions in an ant parallel β-sheet. Biochemistry. 43:3137-3151.
16. Cornea, R. L., L. R. Jones, J. M. Autry, and D. D. Thomas. 1997. Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers. Biochemistry. 36:2960-2967.
17. Macosco, J. C., C.-H. Kim, and Y.-K. Shin. 1997. The membrane topology of the fusion peptide region of influenza hemagglutinin determined by spin-labeling EPR. J. Mol. Biol. 267:1139-1148.
18. Pfeiffer, M., T. Rink, K. Gerwert, D. Oesterhelt, and H.-J. Steinhoff. 1999. Site-directed spin-labeling reveals the orientation of the amino acid side-chains in the E-F loop of bacteriorhodopsin. J. Mol. Biol. 287:163-171.
19. Frazier, A. A., C. R. Roller, J. J. Havelka, A. Hinderliter, and D. S. Cafiso. 2003. Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin-labeling. Biochemistry. 42:96-105.
20. Langen, R., K. J. Oh, D. Cascio, and W. L. Hubbell. 2000. Crystal structure of spin-labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry. 39:8396-8405.
21. Baumann, B. A. J., H. Liang, K. Sale, B. D. Hambly, and P. G. Fajer. 2004. Myosin regulatory domain orientation in skeletal muscle fibers: application of novel electron paramagnetic resonance spectral decomposition and molecular modeling methods. Biophys. J. 86:3030-3041.
22. LaConte, L. E. W., V. Voelz, W. Nelson, M. Entz, and D. D. Thomas. 2002. Molecular dynamics simulation of site-directed spin-labeling: experimental validation in muscle fibers. Biophys. J. 83:1854-1866.
23. 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.
24. Altenbach, C., D. A. Greenhalgh, H. G. Khorana, and W. L. Hubbell. 1994. A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 91:1667-1671.
25. Lüneberg, J., I. Martin, F. Nüssler, J.-M. Ruysschaert, and A. Herrmann. 1995. Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270:27606-27614.
26. Zhou, Z., J. C. Macosco, D. W. Hughes, B. G. Sayer, J. Hawes, and R. M. Epand. 2000. 15N NMR study of the ionization properties of the influenza virus fusion peptide in Zwitterionic phospholipid dispersions. Biophys. J. 78:2418-2425.
27. Dubovskii, V., H. Li, S. Takahashi, A. S. Arseniev, and K. Akasaka. 2000. Structure of an analog of fusion peptide from hemagglutinin. Protein Sci. 9:786-798.
28. Owenius, R., M. Österlund, M. Lindgren, M. Svensson, O. H. Olsen, E. Persson, P.-O. Freskgard, and U. Carlsson. 1999. Properties of spin and fluorescent labels at receptor-ligand interface. Biophys. J. 77:2237-2250.
29. Yu, Y. G., T. E. Thorgeirsson, and Y. K. Shin. 1994. Topology of an amphiphilic mitochondrial signal sequence in the membrane-inserted state: a spin-labeling study. Biochemistry. 33:14221-14226.
30. Sammalkorpi, M., and T. Lazaridis. 2006. Configuration of influenza hemagglutinin fusion peptide monomers and oligomers in membranes. Accepted for publication. Biochim. Biophys. Acta Biomembr.
31. Efremov, R. G., D. E. Nolde, P. E. Volynsky, A. A. Chernyavsky, P. V. Dubovskii, and A. S. Arseniev. 1999. Factors important for fusogenic activity of peptides: molecular modeling study of analogs of fusion peptide of influenza virus hemagglutinin. FEBS Lett. 462:205-210.
32. Bechor, D., and N. Ben-Tal. 2001. Implicit solvent model studies of the interactions of the influenza hemagglutinin fusion peptide with lipid bilayers. Biophys. J. 80:644-655.
33. Spassov, V. Z., L. Yan, and S. Szalma. 2002. Introducing an implicit membrane in Generalized Born/solvent accessibility continuum solvent models. J. Phys. Chem. B. 106:8726-8738.
34. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
35. Neria, E., S. Fischer, and M. Karplus. 1996. Simulation of activation free energies in molecular systems. J. Chem. Phys. 105:1902-1921.
36. Lazaridis, T. 2003. Effective energy function for proteins in lipid membranes. Proteins. 52:176-192.
37. Lazaridis, T., and M. Karplus. 1999. Effective energy function for proteins in solution. Proteins. 35:133-152.
38. Nosé, S. 1984. A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81:511-519.
39. Hoover, W. G. 1984. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
40. Columbus, L., T. Kálai, J. Jekö, K. Hideg, and W. L. Hubbell. 2001. Molecular motion of spin-labeled side chains in α-helices: analysis by variation of side chain structure. Biochemistry. 40:3828-3846.
41. Huang, Q., C.-L. Chen, and A. Herrmann. 2004. Bilayer conformation of fusion peptide of influenza virus hemagglutinin: a molecular dynamics study. Biophys. J. 87:14-22.
42. Vaccaro, L., K. J. Cross, J. Kleinjung, S. K. Straus, D. J. Thomas, S. A. Wharton, J. J. Skehel, and F. Fraternali. 2005. Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers. Biophys. J. 88:25-36.
43. Lagüe, P., B. Roux, and R. W. Pastor. 2005. Molecular dynamics simulations of the influenza hemagglutinin fusion peptide in micelles and bilayers: conformational analysis of peptides and lipids. J. Mol. Biol. 354:1129-1141.
44. Hsu, C.-H., S.-H. Wu, D.-K. Chang, and C. Chen. 2002. Structural characterizations of fusion peptide analogs of influenza virus hemagglutinin. J. Biol. Chem. 277:22725-22733.
45. Morelon, N.-D., G. R. Kneller, M. Ferrand, A. Grand, J. C. Smith, and M. Berc. 1998. Dynamics of alkane chains included in an organic matrix: molecular dynamics simulation and comparison with neutron scattering experiment. J. Chem. Phys. 109:2883-2894.
46. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.