The alignment of a voltage-sensing peptide in dodecylphosphocholine micelles and in oriented lipid bilayers by nuclear magnetic resonance and molecular modeling

Biophysical Journal

Volumn 77, Issue 4, 1999, Pages 2102-2113

  Mattila, Kimmo ^a,b   Kinder, Rudolf ^a   Bechinger, Burkhard ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b IT Center for Science   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHORYLCHOLINE;

ARTICLE; LIPID BILAYER; MICELLE; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN LIPID INTERACTION;

EID: 0032874786     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77051-7     Document Type: Article

References (77)

1. Alder, G. M., W. M. Arnold, C. L. Bashford, A. F. Drake, C. A. Pasternak, and U. Zimmermann. 1991. Divalent cation-sensitive pores formed by natural and synthetic melittin and by triton X-100. Biochim. Biophys. Acta. 1061:111-120.
2. Anderson, H. C. 1983. RATTLE: a "velocity" version of the Shake algorithm for molecular dynamics calculations. J. Comp. Phys. 52: 24-34.
3. a-fluorenyllmethoxycarbonylamino-acids on polyamide supports. Synthesis of substance P and of acyl carrier proteins 65-74 decapeptide. J. Chem. Soc. Perkin Trans. I. 538-546.
4. Balaram, P., K. Krishna, M. Sukumar, I. R. Mellor, and M. S. Sansom. 1992. The properties of ion channels formed by zervamicins. Eur. Biophys. J. 21:117-128.
5. Bechinger, B. 1996. Towards membrane protein design: pH dependent topology of histidine-containing polypeptides. J. Mol. Biol. 263: 768-775.
6. Bechinger, B. 1997a. Structure and dynamics of the M13 coat protein signal sequence in membranes. Proteins: Struct., Funct., Genet. 27: 481-492.
7. Bechinger, B. 1997b. Structure and functions of channel-forming polypeptides: magainins, cecropins, melittin and alamethicin. J. Membr. Biol. 156:197-211.
8. Bechinger, B., L. M. Gierasch, M. Montai, M. Zasloff, and S. J. Opella. 1996. Orientations of helical peptides in membrane bilayers by solid-state NMR spectroscopy. Solid State Nucl. Magn. Reson. 7:185-192.
9. Bechinger, B., Y. Kim, L. E. Chirlian, J. Gesell, J.-M. Neumann, M. Montal, J. Tomich, M. Zasloff, and S. J. Opella. 1991. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J. Biomol. NMR. 1:167-173.
10. Bechinger, B., R. Kinder, M. Helmle, T. B. Vogt, U. Harzer, and S. Schinzel. 1999b. Peptide structural analysis by solid-state NMR spectroscopy. Biopolymers. In press.
11. Bechinger, B., and S. J. Opella. 1991. Flat-coil probe for NMR spectroscopy of oriented membrane samples. J. Magn. Reson. 95:585-588.
12. Bechinger, B., J. M. Ruysschaert, and E. Goormaghtigh. 1999a. Membrane helix orientation from linear dichroism of infrared attenuated total reflection spectra. Biophys. J. 76:552-563.
13. Ben-Efraim, I., and Y. Shai. 1996. Secondary structure, membrane localization, and coassembly within phospholipid membranes of synthetic segments derived from the N- and C-termini regions of the ROMK1 K+ channel. Protein Sci. 5:2287-2297.
14. Berneche, S., M. Nina, and B. Roux. 1998. Molecular dynamics simulation of melittin in a dimyristoylphosphatidylcholine bilayer membrane. Biophys. J. 75:1603-1618.
15. Betz, H. 1990. Homology and analogy in transmembrane channel design: lessons from synaptic membrane proteins. Biochemistry. 29:3591-3599.
16. Biggin, P. C., J. Breed, H. S. Son, and M. S. P. Sansom. 1997. Simulation studies of alamethicin-bilayer interactions. Biophys. J. 72:627-636.
17. Breed, J., I. D. Kerr, R. Sankararamakrishnan, and M. S. Sansom. 1995. Packing interactions of Aib-containing helices: molecular modeling of parallel dimers of simple hydrophobic helices and of alamethicin. Biopolymers. 35:639-655.
18. Brown, L. R., C. Bosch, and K. Wüthrich. 1981. Location and orientation relative to the micelle surface for glucagon in mixed micelles with dodecylphosphocholine; EPR and NMR studies. Biochim. Biophys. Acta. 642:296-312.
19. Brullemans, M., O. Helluin, J. Y. Dugast, G. Molle, and H. Duclohier. 1994. Implication of segment S45 in the permeation pathway of voltage-dependent sodium channels. Eur. Biophys. J. 23:39-49.
20. Chen, L. Q., V. Santarelli, R. Horn, and R. G. Kallen. 1996. A unique role for the S4 segment of domain 4 in the inactivation of sodium channels. J. Gen. Physiol. 108:549-556.
21. Christensen, B., J. Fink, R. B. Merrifield, and D. Mauzerall. 1988. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc. Natl. Acad. Sci. USA. 85:5072-5076.
22. Cruciani, R. A., J. L. Barker, G. Raghunathan, H. R. Guy, M. Zasloff, and E. F. Stanley. 1992. Magainin 2, a natural antibiotic from frog skin, forms ion channels in lipid bilayer membranes. Eur. J. Pharmacol. 226:287-296.
23. Dempsey, C. E., R. B. Sessions, A. Halsall, J. Takei, N. Gibbs, and M. T. Young. 1998. Helical structure and dynamics in membrane polypeptides. Biochem. Soc. Trans. 26:444-450.
24. Doak, D. G., D. Mulvey, K. Kawaguchi, J. Villalain, and I. D. Campbell. 1996. Structural studies of synthetic peptides dissected from the voltage-gated sodium channel. J. Mol. Biol. 258:672-687.
25. Ducarme, P., M. Rahman, and R. Brasseur. 1998. IMPALA: a simple restraint field to simulate the biological membrane in molecular structure studies. Proteins. 30:357-371.
26. Duclohier, H., G. Molle, and G. Spach. 1989. Antimicrobial peptide magainin I from Xenopus skin forms onion-permeable channels in planar lipid bilayers. Biophys. J. 56:1017-1021.
27. Engelman, D. M., T. A. Steitz, and A. Goldman. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15:321-353.
28. Gazit, E., A. Boman, H. G. Boman, and Y. Shai. 1995. Interaction of the mammalian antibacterial peptide cecropin P1 with phospholipid vesicles. Biochemistry. 34:11479-11488.
29. 10-helical peptide standard. J. Am. Chem. Soc. 120:4763-4770.
30. Grice, A. L., I. D. Kerr, and M. S. P. Sansom. 1997. Ion channels formed by HIV-1 Vpu: a modelling and simulation study. FEBS Lett. 405: 299-304.
31. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110:7870-7872.
32. Guba, W., and H. Kessler. 1994. A novel computational mimetic of biological membranes in molecular dynamics simulations. J. Phys. Chem. 98:23-27.
33. Hanke, W., C. Methfessel, H. U. Wilmsen, E. Katz, G. Jung, and G. Boheim. 1983. Melittin and a chemically modified trichotoxin form alamethicin-type multi-state pores. Biochim. Biophys. Acta. 727: 108-114.
34. Haris, P. I., B. Ramesh, S. Brazier, and D. Chapman. 1994. The conformational analysis of a synthetic S4 peptide corresponding to a voltage-gated potassium ion channel protein. FEBS Lett. 349:371-374.
35. 10-helical peptides and their interactions with phospholipid bilayers and ion channel formation. J. Mol. Biol. 269:4928-4933.
36. Jähnig, F. 1981. Critical effects from lipid-protein interaction in membranes. I. Theoretical description. Biophys. J. 36:329-345.
37. Jähnig, F. 1983. Thermodynamics and kinetics of protein incorporation into membranes. Proc. Natl. Acad. Sci. USA. 80:3691-3695.
38. Jorgensen, W. L., J. D. Chandraeskar, J. D. Maruda, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
39. Kontis, K. J., A. Rounaghi, and A. L. Goldin. 1997. Sodium channel activation gating is affected by substitutions of voltage sensor positive charges in all four domains. J. Gen. Physiol. 110:391-401.
40. Kra-Oz, Z., G. Spira, Y. Palti, and H. Meiri. 1992. Involvement of different S4 parts in the voltage dependency of Na channel gating. J. Membr. Biol. 129:189-198.
41. Lear, J. D., Z. R. Wasserman, and W. F. DeGrado. 1988. Synthetic amphiphilic peptide models for protein ion channels. Science. 240: 1177-1181.
42. Logothetis, D. E., S. Movahedi, C. Satler, K. Lindpaintner, and B. Nadal-Ginard. 1992. Incremental reductions of positive charge within the S4 region of a voltage-gated K+ channel result in corresponding decreases in gating charge. Neuron. 8:531-540.
43. Macura, S., and R. R. Ernst. 1980. Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy. Mol. Phys. 41:95.
44. Mannuzzu, L. M., M. M. Moronne, and E. Y. Isacoff. 1996. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 271:213-216.
45. Mellor, I. R., and M. S. P. Sansom. 1990. Ion-channel properties of mastoparan, a 14-residue peptide from wasp venom, and of MP3, a 12-residue analogue. Proc. R. Soc. Lond. B. 239:383-400.
46. Milik, M., and J. Skolnick. 1993. Insertion of peptide chains into lipid membranes: an off-lattice Monte Carlo dynamics model. Proteins. 15: 10-25.
47. Montal, M. 1990. Molecular anatomy and molecular design of channel proteins. FASEB J. 4:2623-2635.
48. Moroder, L., R. Romano, W. Guba, D. F. Mierke, H. Kessler, C. Delporte, J. Winand, and J. Christophe. 1993. New evidence for a membrane-bound pathway in hormone receptor binding. Biochemistry. 32: 13551-13559.
49. Mulvey, D., G. F. King, R. M. Cooke, D. G. Doak, T. S. Harvey, and I. D. Campbell. 1989. High resolution 1H NMR study of the solution structure of the S4 segment of the sodium channel protein. FEBS Lett. 257:113-117.
50. Nelson, J. W., and N. R. Kallenbach. 1986. Stabilization of the ribonuclease S-peptide alpha-helix by trifluoroethanol. Proteins. 1:211-217.
51. Noda, M., S. Shimizu, T. Tanabe, T. Takai, T. Kayano, T. Ikeda, H. Takahashi, H. Nakayama, Y. Kanaoka, N. Minamino, K. Kangawa, H. Matsuo, M. A. Raftery, T. Hirose, S. Inayama, H. Hayashida, T. Miyata, and S. Numa. 1984. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature. 312:121-127.
52. Oblatt-Montal, M., L. K. Bühler, T. Iwamoto, J. M. Tomich, and M. Montal. 1993. Synthetic peptides and four-helix bundle proteins as model systems for the pore-forming structure of channel proteins. J. Biol. Chem. 268:14601-14607.
53. Papavoine, C. H., J. M. Aelen, R. N. Konings, C. W. Hilbers, and F. J. Van de Ven. 1995. NMR studies of the major coat protein of bacteriophage M13. Structural information of gVIIIp in dodecylphosphocholine micelles. Eur. J. Biochem. 232:490-500.
54. Pellegrini, M., A. Bisello, M. Rosenblatt, M. Chorev, and D. F. Mierke. 1998. Binding domain of human parathyroid hormone receptor: from conformation to function. Biochemistry. 37:12737-12743.
55. Pines, A., M. G. Gibby, and J. S. Waugh. 1973. Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59:569-590.
56. Piotto, M., V. Saudek, and V. Sklenar. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:661-665.
57. Plateau, P., and M. Gueron. 1982. Exchangeable proton NMR without base-line distortion using new strong pulse sequences. J. Am. Chem. Soc. 104:7310-7311.
58. Pullman, A. 1988. Theoretical studies on the formation and properties of bundles of alpha-helices and their aptitude to form ion-channels. Prog. Clin. Biol. Res. 273:113-120.
59. Rapaport, D., M. Danin, E. Gazit, and Y. Shai. 1992. Membrane interactions of the sodium channel S4 segment and its fluorescently-labeled analogues. Biochemistry. 31:8868-8875.
60. Schlieper, P., and E. De Robertis. 1977. Triton X-100 as a channel-forming substance in artificial lipid bilayer membranes. Arch. Biochem. Biophys. 184:204-208.
61. Sigworth, F. J. 1992. Voltage gating of ion channels. Q. Rev. Biophys. 27:1-40.
62. Sonnichsen, F. D., J. E. Van Eyk, R. S. Hodges, and B. D. Sykes. 1992. Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide. Biochemistry. 31:8790-8798.
63. Stankowski, S., U. D. Schwarz, and G. Schwarz. 1988. Voltage-dependent pore activity of the peptide alamethicin correlated with incorporation in the membrane: salt and cholesterol effects. Biochim. Biophys. Acta. 941:11-18.
64. Stühmer, W. 1991. Structure-function studies of voltage-gated ion channels. Annu. Rev. Biophys. Biophys. Chem. 20:65-78.
65. Stühmer, W., F. Conti, H. Suzuki, X. D. Wang, M. Noda, N. Yahagi, H. Kubo, and S. Numa. 1989. Structural parts involved in activation and inactivation of the sodium channel. Nature. 339:597-603.
66. Tosteson, M. T., D. S. Auld, and D. C. Tosteson. 1989. Voltage-gated channels formed in lipid bilayers by a positively charged segment of the Na-channel polypeptide. Proc. Natl. Acad. Sci. USA. 86:707-710.
67. Tosteson, M. T., J. J. Levy, L. H. Caporale, M. Rosenblatt, and D. C. Tosteson. 1987. Solid-phase synthesis of melittin: purification and functional characterization. Biochemistry. 26:6627-6631.
68. Tosteson, M. T., and D. C. Tosteson. 1981. The sting. Melittin forms channels in lipid bilayers. Biophys. J. 36:109-116.
69. Vogt, T. C. B., and B. Bechinger. 1999. The interactions of histidine-containing amphipathic helical peptide antibiotics with lipid bilayers: the effects of charges and pH. J. Biol. Chem. In press.
70. Wang, F., G. H. Naisbitt, L. P. Vernon, and M. Glaser. 1993. Pyrularia thionin binding to and the role of tryptophan-8 in the enhancement of phosphatidylserine domains in erythrocyte membranes. Biochemistry. 32:12283-12289.
71. Welti, R., and M. Glaser. 1994. Lipid domains in model and biological membranes. Chem. Phys. Lipids. 73:121-137.
72. Woodbury, D. J. 1989. Pure lipid vesicles can induce channel-like conductances in planar bilayers. J. Membr. Biol. 109:145-150.
73. Wray, V., R. Kinder, T. Federau, P. Henklein, B. Bechinger, and U. Schubert. 1999. Solution structure and orientation of the transmembrane anchor domain of the HIV-1 encoded virus protein U (Vpu) by high-resolution and solid-state NMR spectroscopy. Biochemistry 38: 5272-5282.
74. Wüthrich, K. 1986. NMR of Proteins and Nucleic Acids. John Wiley and Sons, New York.
75. Wymore, T., and T. C. Wong. 1999a. Molecular dynamics study of substance P peptides in a biphasic membrane mimic. Biophys. J. 76:1199-1212.
76. Wymore, T., and T. C. Wong. 1999b. Molecular dynamics study of substance P peptides in a sodium dodecyl sulfate micelle. Biophys. J. 76:1213-1227.
77. Yang, N., A. L. George, Jr., and R. Horn. 1996. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 16:113-122.