Structure of self-aggregated alamethicin in ePC membranes detected by pulsed electron-electron double resonance and electron spin echo envelope modulation spectroscopies

Biophysical Journal

Volumn 96, Issue 8, 2009, Pages 3197-3209

  Milov, Alexander D ^a   Samoilova, Rimma I ^a   Tsvetkov, Yuri D ^a   De Zotti, Marta ^b   Formaggio, Fernando ^b   Toniolo, Claudio ^b   Handgraaf, Jan Willem ^c   Raap, Jan ^d  

^a INSTITUTE OF CHEMICAL KINETICS AND COMBUSTION   (Russian Federation)

^b UNIVERSITY OF PADOVA   (Italy)

^c Culgi BV   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALAMETHICIN; GLUTAMIC ACID DERIVATIVE; LIPID; NITROXIDE; PEPTIDE; PHOSPHATIDYLCHOLINE;

ANALYTIC METHOD; ARTICLE; DIPOLE; ELECTRON SPIN ECHO ENVELOPE MODULATION SPECTROSCOPY; MAGNETISM; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR STABILITY; PROTEIN AGGREGATION; PROTEIN STRUCTURE; PULSED ELECTRON ELECTRON DOUBLE RESONANCE SPECTROSCOPY; QUALITATIVE ANALYSIS; SPECTROSCOPY; SPIN LABELING; ALGORITHM; AMINO ACID SEQUENCE; ARTIFICIAL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

ALAMETHICIN; ALGORITHMS; AMINO ACID SEQUENCE; MEMBRANES, ARTIFICIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLCHOLINES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SPECTRUM ANALYSIS;

EID: 67649394753     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.01.026     Document Type: Article

References (75)

1. Leitgeb, B., L. Szekeres, L. Manczinger, C. Vágvölgyi, and L. Kredics. 2007. The history of alamethicin: a review of the most extensively studied peptaibol. Chem. Biodivers. 4:1027-1051.
2. Mueller, P., and P. O. Rudin. 1968. Action potentials induced in biomolecular lipid membranes. Nature. 217:713-719.
3. Boheim, G. 1974. Statistical analysis of alamethicin in a lipid membrane. J. Membr. Biol. 19:277-303.
4. Sansom, M. S. P. 1993. Alamethicin and related peptaibols - model ion channels. Eur. Biophys. J. 22:105-124.
5. Baumann, G., and P. Mueller. 1974. A molecular model of membrane excitability. J. Supramol. Struct. 2:538-577.
6. Huang, H. W., and Y. Wu. 1991. Lipid-alamethicin interactions influence alamethicin orientation. Biophys. J. 60:1079-1087.
7. Boheim, G. W., W. Hanke, and G. Jung. 1983. Alamethicin pore formation: voltage-dependent flip-flop of α-helix dipoles. Biophys. Struct. Mech. 9:181-191.
8. Fox, R. O., and F. M. Richards. 1982. A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1.5 Å resolution. Nature. 300:325-330.
9. Hall, J. E., I. Vodyanov, T. M. Balasubramanian, and G. R. Marshall. 1994. Alamethicin, a rich model for channel behavior. Biophys. J. 45:233-247.
10. Cascio, M., and B. A. Wallace. 1988. Conformation of alamethicin in phospholipid vesicles: implications for insertion models. Proteins Struct. Funct. Genet. 4:889-898.
11. Pispisa, B., L. Stella, C. Mazzuca, and M. Venanzi. 2006. Reviews in Fluorescence. C. D. Geddes and J. R. Lakowicz, editors. Springer, New York.
12. Kropacheva, T. N., and J. Raap. 2007. Enzymatic reaction in a vesicular microreactor: peptaibol-facilitated substrate transport. Chem. Biodivers. 4:1388-1394.
13. Dempsey, C. E., and L. J. Handcock. 1996. Hydrogen bond stabilities in membrane-reconstituted alamethicin from amide-resolved hydrogen-exchange measurements. Biophys. J. 70:1777-1788.
14. 31P Solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes. Biochemistry. 40:9428-9437.
15. 15N solid-state nuclear magnetic resonance. Biophys. J. 81:1684-1698.
16. 31P solid-state NMR spectroscopy. Biophys. J. 113:3034-3042.
17. He, K., S. J. Ludtke, H. W. Huang, and D. L. Worcester. 1995. Antimicrobial peptide pores in membranes detected by neutron in-plane scattering. Biochemistry. 34:15614-15618.
18. Salnikov, E. S., M. De Zotti, F. Formaggio, X. Li, C. Toniolo, et al. 2009. Alamethicin topology in phospholipid membranes by oriented solid-state NMR and EPR spectroscopies: a comparison. J. Phys. Chem. B. 113:3034-3042.
19. Keller, S. L., S. M. Gruner, and K. Garwisch. 1996. Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim. Biophys. Acta. 1278:241-246.
20. Angelova, A., R. Ionov, M. H. J. Koch, and J. Rapp. 2000. Interaction of the peptide antibiotic alamethicin with bilayer- and non-bilayer-forming lipids: influence of increasing alamethicin concentration on the lipid supramolecular structures. Arch. Biochem. Biophys. 378:93-106.
21. Spaar, A., C. Münster, and T. Salditt. 2004. Conformation of peptides in membranes studied by X-ray grazing incidence scattering. Biophys. J. 87:396-407.
22. Li, C., and T. Salditt. 2006. Structure of magainin and alamethicin in model membranes studied by X-ray reflectivity. Biophys. J. 91:3285-3300.
23. Constantin, D., G. Brotons, A. Jarre, C. Li, and T. Salditt. 2007. Interaction of alamethicin pores in DMPC bilayers. Biophys. J. 92:3978-3987.
24. Qian, S., W. Wang, L. Yang, and H. W. Huang. 2008. Structure of the alamethicin pore reconstructed by X-ray diffraction analysis. Biophys. J. 94:3512-3522.
25. Archer, S. J., J. F. Ellena, and D. S. Cafiso. 1991. Dynamics and aggregation of the peptide ion channel alamethicin. Biophys. J. 60:389-398.
26. Marsh, D., M. Jost, C. Peggion, and C. Toniolo. 2007. TOAC spin-labels in the backbone of alamethicin: EPR studies in lipid membranes. Biophys. J. 92:473-481.
27. Marsh, D., M. Jost, C. Peggion, and C. Toniolo. 2007. Lipid chain length dependence for incorporation of alamethicin in membranes: EPR studies on TOAC-spin-labeled analogues. Biophys. J. 92:4002-4011.
28. Bartucci, R., R. Guzzi, M. De Zotti, C. Toniolo, L. Sportelli, et al. 2008. Backbone dynamics of alamethicin bound to lipid membranes: spin-echo electron paramagnetic resonance of TOAC-spin-labels. Biophys. J. 94:2698-2705.
29. Milov, A. D., Yu. D. Tsvetkov, F. Formaggio, M. Crisma, C. Toniolo, et al. 2001. The secondary structure of a membrane-modifying peptide in a supramolecular assembly studied by PELDOR and CW-ESR spectroscopies. J. Am. Chem. Soc. 123:3784-3789.
30. Milov, A. D., Yu. D. Tsvetkov, E. Y. Gorbunova, L. G. Mustaeva, T. V. Ovchinnikova, et al. 2007. Solvent effects on the secondary structure of the membrane-active zervamicin determined by PELDOR spectroscopy. Chem. Biodivers. 4:1243-1255.
31. Milov, A. D., R. I. Samoilova, Yu. D. Tsvetkov, M. De Zotti, C. Toniolo, et al. 2008. PELDOR conformational analysis of bis-labeled alamethicin aggregated in phospholipid vesicles. J. Phys. Chem. B. 112:13469-13472.
32. Milov, A. D., Yu. D. Tsvetkov, F. Formaggio, M. Crisma, C. Toniolo, et al. 2000. Self-assembling properties of membrane-modifying peptides studied by PELDOR and CW-ESR spectroscopies. J. Am. Chem. Soc. 122:3843-3848.
33. Milov, A. D., M. I. Samoilova, Yu. D. Tsvetkov, M. Jost, C. Peggion, et al. 2007. Supramolecular structure of self-assembling alamethicin analog studied by ESR and PELDOR. Chem. Biodivers. 4:1275-1298.
34. Milov, A. D., R. I. Samoilova, Yu. D. Tsvetkov, F. Formaggio, C. Toniolo, et al. 2007. Self-aggregation of spin-labeled alamethicin in ePC vesicles studied by pulsed electron-electron double resonance. J. Am. Chem. Soc. 129:9260-9261.
35. Toniolo, C. 1989. Structure of conformationally constrained peptides: from model compounds to bioactive peptides. Biopolymers. 28:247-257.
36. Toniolo, C., M. Crisma, F. Formaggio, and C. Peggion. 2001. Control of peptide conformation by the Thorpe-Ingold effect (Cα-tetrasubstitution). Biopolymers. 60:396-419.
37. Toniolo, C., M. Crisma, and F. Formaggio. 1998. TOAC, a nitroxide spin-labeled, achiral, Cα-tetrasubstituted α-amino acid, is an excellent tool in materials science and biochemistry. Biopolymers. 47:153-158.
38. Peggion, C., M. Jost, W. M. de Borggraeve, M. Crisma, F. Formaggio, et al. 2007. Conformational analysis of TOAC-labeled alamethicin F50/5 analogues. Chem. Biodivers. 4:1256-1274.
39. Crisma, M., C. Peggion, C. Baldini, E. J. MacLean, N. Vedovato, et al. 2007. Crystal structure of a spin-labeled, channel-forming, alamethicin analogue. Angew. Chem. Int. Ed. 46:2047-2050.
40. Vedovato, N., C. Baldini, C. Toniolo, and G. Rispoli. 2007. Pore-forming properties of alamethicin F50/5 inserted in a biological membrane. Chem. Biodivers. 4:1338-1346.
41. Woolley, G. A., and B. A. Wallace. 1993. Temperature dependence of the interaction of alamethicin helices in membranes. Biochemistry. 32:9819-9825.
42. Milov, A. D., K. M. Salikhov, and M. D. Shirov. 1981. Application of ELDOR in electron-spin echo for paramagnetic center space distribution in solids. Fiz. Tverd. Tela. 23:975-982.
43. Milov, A. D., A. G. Maryasov, and Yu. D. Tsvetkov. 1998. Pulsed electron double resonance (PELDOR) and its applications in free-radicals research. Appl. Magn. Reson. 15:107-143.
44. Jeschke, G., A. Koch, U. Jonas, and A. Godt. 2002. Direct conversion of EPR dipolar time evolution data to distance distributions. J. Magn. Reson. 155:72-82.
45. Milov, A. D., Yu. D. Tsvetkov, F. Formaggio, S. Oancea, C. Toniolo, et al. 2003. Aggregation of spin-labeled trichogin GA IV dimers: distance distribution between spin-labels in frozen solutions by PELDOR data. J. Phys. Chem. B. 107:13719-13727.
46. Jeschke, G., G. Panek, A. Godt, A. Bender, and H. Paulsen. 2004. Data analysis procedures for pulse ELDOR measurements of broad distance distributions. Appl. Magn. Reson. 26:223-244.
47. Bowman, M. K., A. G. Maryasov, N. Kim, and V. J. DeRose. 2004. Visualization of distance distribution from pulsed double electron-electron resonance data. Appl. Magn. Reson. 26:23-40.
48. Milov, A. D., B. D. Naumov, and Yu. D. Tsvetkov. 2004. The effect of microwave pulse duration on the distance distribution function between spin-labels obtained by PELDOR data analysis. Appl. Magn. Reson. 26:587-599.
49. Chiang, Y. W., P. P. Borbat, and J. H. Freed. 2005. The determination of pair distributions by pulsed ESR using Tikhonov regularization. J. Magn. Reson. 172:279-295.
50. Bode, B. E., D. Margraf, J. Plackmeyer, G. Dürner, T. F. Prisner, et al. 2007. Counting the monomers in nanometer-sized oligomers by pulsed electron-electron double resonance. J. Am. Chem. Soc. 129:6736-6745.
51. Dikanov, S. A., and Yu. D. Tsvetkov. 1992. Electron Spin Echo Envelope Modulation (ESEEM) Spectroscopy. CRC Press, Boca Raton, FL.
52. Salnikov, E. S., D. A. Erilov, A. D. Milov, Yu. D. Tsvetkov, C. Peggion, et al. 2006. Location and aggregation of the spin-labeled peptide trichogin GA IV in a phospholipid membrane as revealed by pulsed EPR. Biophys. J. 91:1532-1540.
53. Marsh, D. 2001. Polarity and permeation profiles in lipid membranes. Proc. Natl. Acad. Sci. USA. 98:777-782.
54. Bartucci, R., R. Guzzi, D. Marsh, and L. Sportelli. 2003. Intramembrane polarity by electron spin echo spectroscopy of labeled lipids. Biophys. J. 84:1025-1030.
55. Erilov, D. A., R. Bartucci, R. Guzzi, A. A. Shubin, A. G. Maryasov, et al. 2005. Water concentration profiles in membranes measured by ESEEM of spin-labeled lipids. J. Phys. Chem. B. 109:12003-12013.
56. Peggion, C., M. Jost, C. Baldini, F. Formaggio, and C. Toniolo. 2007. Total synthesis in solution of TOAC-labeled alamethicin F50/5 analogues. Chem. Biodivers. 4:1183-1199.
57. Szoka, Jr., F., and D. Papahadjopoulos. 1980. Comparative properties and methods of preparation of lipid vesicles (liposomes). Annu. Rev. Biophys. Bioeng. 9:467-508.
58. Bartucci, R., D. A. Erilov, R. Guzzi, L. Sportelli, S. A. Dzuba, et al. 2006. Time-resolved electron spin resonance studies of spin-labeled lipids in membranes. Chem. Phys. Lipids. 141:142-157.
59. Jorgensen, W. L., D. S. Maxwell, and J. Tirado-Rives. 1996. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 117:11225-11236.
60. Maxwell, D. S., J. Tirado-Rives, and W. L. Jorgensen. 1995. A comprehensive study of the rotational energy profiles of organic systems by ab initio MO theory, forming a base for peptide torsional parameters. J. Comput. Chem. 16:984-1010.
61. Parsegian, V. A., N. Fuller, and R. P. Rand. 1979. Measured work of deformation and repulsion of lecithin bilayers. Proc. Natl. Acad. Sci. USA. 76:2750-2754.
62. Murzyn, K., T. Róg, W. Blicharski, M. Dutka, J. Pyka, et al. 2006. Influence of the disulfide bond configuration on the dynamics of the spin-label attached to cytochrome c. Proteins. 62:1088-1100.
63. Rinia, H. A., R. A. Kik, R. A. Demel, M. M. E. Snel, J. A. Killian, et al. 2000. Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers. Biochemistry. 39:5852-5858.
64. Eaton, S. S., and G. R. Eaton. 2000. Biological Magnetic Resonance, Vol. 19 L. J. Berliner, S. S. Eaton, and G. R. Eaton, editors. Kluwer, New York.
65. Maryasov, A. G., and Yu. D. Tsvetkov. 2000. Formation of the pulsed electron-electron double resonance signal in the case of a finite amplitude of microwave fields. Appl. Magn. Reson. 18:583-605.
66. Tikhonov, A. N. 1995. Numerical Methods for the Solution of Ill-Posed Problems. Dordrecht, The Netherlands.
67. Tieleman, D. P., B. Hess, and M. S. P. Sansom. 1998. Analysis and evaluation of channel models. Biophys. J. 83:2393-2407.
68. 15N NMR. Biophys. J. 69:2392-2397.
69. Chen, F.-Y., M.-T. Lee, and H. W. Huang. 2003. Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin. Biophys. J. 84:3751-3758.
70. Stella, L., M. Burattini, C. Mazzuca, A. Palleschi, M. Venanzi, et al. 2007. Alamethicin interaction with lipid membranes: a spectroscopic study on synthetic analogues. Chem. Biodivers. 4:1299-1312.
71. Parker, M. W., J. P. M. Postma, F. Pattus, A. D. Tucker, and D. Tsernoglou. 1992. Refined structure of the pore-forming domain of colicin A at 2.4 Å resolution. J. Mol. Biol. 224:639-657.
72. Lakey, J. H., D. Duché, J.-M. González-Manas, D. Baty, and F. Pattus. 1993. Fluorescence energy transfer distance measurements. The hydrophobic helical hairpin of colicin A in the membrane bound state. J. Mol. Biol. 230:1055-1067.
73. Savitsky, A., M. Kühn, D. Duché, K. Möbius, and H.-J. Steinhoff. 2004. Spontaneous refolding of the pore-forming colicin A toxin upon membrane association as studied by X-band and W-band high-field EPR spectroscopy. J. Phys. Chem. B. 108:9541-9548.
74. Futaki, S., M. Fukuda, M. Omote, K. Yamauchi, T. Yagami, et al. 2001. Alamethicin-leucine zipper hybrid peptide: a prototype for the design of artificial receptors and ion channels. J. Am. Chem. Soc. 123:12127-12134.
75. 1H-NMR studies of self-aggregation of melittin in aqueous solution. Biochim. Biophys. Acta. 622:231-244.