NMR methods for studying membrane-active antimicrobial peptides

Concepts in Magnetic Resonance Part A: Bridging Education and Research

Volumn 23, Issue 2, 2004, Pages 89-120

  Strandberg, Erik ^a   Ulrich, Anne S ^a,b,c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

^c Forschungszentrum   (Germany)

Author keywords

Amphiphilic antimicrobial peptides; Biomembranes; Isotope labeling; Lipid bilayers; Lipid peptide interactions; Peptide structure determination; Solid state NMR

Indexed keywords

ANTIINFECTIVE AGENT; CARBON 13; FLUORINE; HYDROGEN; LIPID; NITROGEN 15; PEPTIDE DERIVATIVE; PHOSPHORUS 31;

DRUG STRUCTURE; LIPID BILAYER; LIPID MEMBRANE; NUCLEAR MAGNETIC RESONANCE; REVIEW; SOLID STATE;

EID: 17844376024     PISSN: 15466086     EISSN: 15525023     Source Type: Journal    
DOI: 10.1002/cmr.a.20024     Document Type: Review

References (247)

1. Saberwal G, Nagaraj R. 1994. Cell-lytic and antibacterial peptides that act by perturbing the barrier function of membranes. Facets of their conformational features, structure-function correlations and membrane-perturbing abilities. Biochim Biophys Acta 1197:109-131.
2. Epand RM, Vogel HJ. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim Biophys Acta 1462:11-28.
3. Hancock RE, Chapple DS. 1999. Peptide antibiotics. Antimicrob Agents Chemother 43:1317-1323.
4. Van 't Hof W, Veerman EC, Helmerhorst EJ, Amerongen AV. 2001. Antimicrobial peptides: properties and applicability. Biol Chem 382:597-619.
5. Petersen NO, Kroon PA, Kainoshio M, Chan SI. 1975. Thermal phase transitions in deuterated lecithin bilayers. Chem Phys Lipids 14:343-349.
6. 2H-NMR, FTIR, DSC, and neutron-scattering study. Biophys J 61:1025-1035.
7. Crowe LM, Crowe JH. 1991. Solution effects on the thermotropic phase transition of unilamellar liposomes. Biochim Biophys Acta 1064:267-274.
8. Killian JA. 1992. Gramicidin and gramicidin-lipid interactions. Biochim Biophys Acta 1113:391-425.
9. Cross TA. 1997. Solid-state nuclear magnetic resonance characterization of gramicidin channel structure. Methods Enzymol 289:672-696.
10. Wallace BA. 1998. Recent advances in the high resolution structures of bacterial channels: gramicidin A. J Struct Biol 121:123-141.
11. Wallace BA. 1999. X-ray crystallographic structures of gramicidin and their relation to the Streptomyces lividans potassium channel structure. Novartis Found Symp 225:23-32; discussion 33-37.
12. Wallace BA. 2000. Common structural features in gramicidin and other ion channels. Bioessays 22:227-234.
13. Roux B. 2002. Computational studies of the gramicidin channel. Accounts Chem Res 35:366-375.
14. Matsuzaki K. 1999. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim Biophys Acta 1462:1-10.
15. Shai Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim Biophys Acta 1462:55-70.
16. Sitaram N, Nagaraj R. 1999. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim Biophys Acta 1462:29-54.
17. Huang HW. 2000. Action of antimicrobial peptides: two-state model. Biochemistry 39:8347-8352.
18. McElhaney RN, Prenner EJ, editors. 1999. Special Issue: the interaction of antimicrobial peptides with model lipid bilayers and biological membranes. Biochim Biophys Acta 1462:1-234.
19. Devaux PF, Seigneuret M. 1985. Specificity of lipid-protein interactions as determined by spectroscopic techniques. Biochim Biophys Acta 822:63-125.
20. Wade D, Boman A, Wahlin B, Drain CM, Andreu D, Boman HG, Merrifield RB. 1990. All-D amino acid-containing channel-forming antibiotic peptides. Proc Natl Acad Sci USA 87:4761-4765.
21. Bessalle R, Kapitkovsky A, Gorea A, Shalit I, Fridkin M. 1990. All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett 274:151-155.
22. Merrifield EL, Mitchell SA, Ubach J, Boman HG, Andreu D, Merrifield RB. 1995. D-enantiomers of 15-residue cecropin A-melittin hybrids. Int J Pept Protein Res 46:214-220.
23. Vogel H, Jahnig F. 1986. Models for the structure of outer-membrane proteins of Escherichia coli derived from raman spectroscopy and prediction methods. J Mol Biol 190:191-199.
24. Schulz GE. 2002. The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565: 308-317.
25. Wüthrich K. NMR of proteins and nucleic acids. New York: Wiley; 1986. 292 p.
26. Aue WP, Bartholdi E, Ernst RR. 1976. 2-dimensional spectroscopy: application to nuclear magnetic resonance. J Chem Phys 64:2229-2246.
27. Braunschweiler L, Ernst RR. 1983. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J Magn Reson 53:521-528.
28. Jeener J, Meier BH, Bachmann P, Ernst RR. 1979. Investigation of exchange processes by 2-dimensional NMR spectroscopy. J Chem Phys 71:4546-4553.
29. Lauterwein J, Bosch C, Brown LR, Wüthrich K. 1979. Physicochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim Biophys Acta 556:244-264.
30. Van den Hooven HW, Fogolari F, Rollema HS, Konings RN, Hilbers CW, Van de Ven FJ. 1993. NMR and circular dichroism studies of the lantibiotic nisin in non-aqueous environments. FEBS Lett 319:189-194.
31. Damberg P, Jarvet J, Gräslund A. 2001. Micellar systems as solvents in peptide and protein structure determination. Methods Enzymol 339:271-285.
32. Blazyk J, Wiegand R, Klein J, Hammer J, Epand RM, Epand RF, Maloy WL, Kari UP. 2001. A novel linear amphipathic β-sheet cationic antimicrobial peptide with enhanced selectivity for bacterial lipids. J Biol Chem 276:27899-27906.
33. Sanders CR, 2nd, Landis GC. 1995. Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 34:4030-4040.
34. Vold RR, Prosser RS, Deese AJ. 1997. Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides. J Biomol NMR 9:329-335.
35. Okada A, Wakamatsu K, Miyazawa T, Higashijima T. 1994. Vesicle-bound conformation of melittin: transferred nuclear Overhauser enhancement analysis in the presence of perdeuterated phosphatidylcholine vesicles. Biochemistry 33:9438-9446.
36. Wakamatsu K, Takeda A, Tachi T, Matsuzaki K. 2002. Dimer structure of magainin 2 bound to phospholipid vesicles. Biopolymers 64:314-327.
37. Dempsey CE, Butler GS. 1992. Helical structure and orientation of melittin in dispersed phospholipid membranes from amide exchange analysis in situ. Biochemistry 31:11973-11977.
38. Dempsey CE. 1994, Amide-resolved hydrogen-deuterium exchange measurements from membrane-reconstituted polypeptides using exchange trapping and semiselective two-dimensional NMR. J Biomol NMR 4:879-884.
39. Maurer T, Lucke C, Ruterjans H. 1991. Investigation of the membrane-active peptides melittin and glucagon by photochemically induced dynamic-nuclear-polarization (photo-CIDNP) NMR. Eur J Biochem 196: 135-141.
40. Kaptein R. 1982. Photo-CIDNP studies of proteins. In: Berliner L and Reuben J. Biological magnetic resonance. New York: Plenum Press. p 145-191.
41. 1H NMR studies on melittin channels activated by tricyclic tranquilizers. Biophys J 63:569-572.
42. 35Cl-NMR study. Biochim Biophys Acta 1372:370-378.
43. Ulrich AS. 2002. Biophysical aspects of using liposomes as delivery vehicles. Bioscience Reports 22: 129-150.
44. Moll F, 3rd, Cross TA. 1990. Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D. Biophys J 57:351-362.
45. Byström T, Strandberg E, Kovacs FA, Cross TA, Lindblom G. 2000. Influence of transmembrane peptides on bilayers of phosphatidylcholines with different acyl chain lengths studied by solid-state NMR. Biochim Biophys Acta 1509:335-345.
46. Hallock KJ, Wildman KH, Lee DK, Ramamoorthy A. 2002. An innovative procedure using a sublimable solid to align lipid bilayers for solid-state NMR studies. Biophys J 82:2499-2503.
47. Glaser RW, Ulrich AS. 2003. Susceptibility corrections in solid-state NMR experiments with oriented membrane samples. Part I: applications. J Magn Reson 164:104-114.
48. 2H solid state NMR. Biophys J 86:3709-3721.
49. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim Biophys Acta 515:105-140.
50. Cullis PR, de Kruijff B. 1979. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta 559:399-420.
51. Pinheiro TJ, Watts A. 1994. Resolution of individual lipids in mixed phospholipid membranes and specific lipid-cytochrome c interactions by magic-angle spinning solid-state phosphorus-31 NMR. Biochemistry 33:2459-2467.
52. Ulrich AS, Heyn MP, Watts A. 1992. Structure determination of the cyclohexene ring of retinal in bacteriorhodopsin by solid-state deuterium NMR. Biochemistry 31:10390-10399.
53. 2H-NMR. Biochim Biophys Acta 737:117-171.
54. Seelig J. 1977. Deuterium magnetic resonance: theory and application to lipid membranes. Q Rev Biophys 10:353-418.
55. 2H NMR. In: Asakura T. Solid state NMR. Amsterdam: Elsevier Science. p 190-211.
56. Seelig J, Macdonald PM, Scherer PG. 1987. Phospholipid head groups as sensors of electric charge in membranes. Biochemistry 26:7535-7541.
57. 15N-NMR in oriented lipid bilayers. Eur J Biochem 268:302-309.
58. Dufourc EJ, Smith IC, Dufourcq J. 1986. Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR. Biochemistry 25:6448-6455.
59. 31P-NMR and DSC. Chem Phys Lipids (in press).
60. Powles JG, Strange JH. 1963. Zero time resolution nuclear magnetic resonance transients in solids. Proc Phys Soc 82:6-15.
61. Mansfield P. 1965. Multiple-pulse nuclear magnetic resonance transients in solids. Phys Rev 137:A961-A974.
62. Davis JH, Jeffrey KR, Bloom M, Valic MI, Higgs TP. 1976. Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem Phys Lett 42:390-394.
63. Vold RL, Waugh JS, Klein MP, Phelps DE. 1968. Measurement of spin relaxation in complex systems. J Chem Phys 48:3831-3832.
64. 19F NMR structure analysis of membrane-associated peptides. ChemBioChem 4:1151-1163.
65. 19F-NMR analysis of membrane-active peptides. In: NMR spectroscopy of biological solids. Ramamoorthy A, editor. New York: Marcel Dekker. (in press).
66. Opella SJ, Ma C, Marassi FM. 2001. Nuclear magnetic resonance of membrane-associated peptides and proteins. Methods Enzymol 339:285-313.
67. Marassi FM, Opella SJ. 2003. Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci 12:403-411.
68. 13C NMR. Magn Res Chem 24:835-852.
69. Cornilescu G, Delaglio F, Bax A. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302.
70. Sternberg U, Witter R, Ulrich AS. 2004. 3D structure elucidation using NMR chemical shifts. In: Webb GA, editor. Annual report on NMR spectroscopy 52. New York: Academic Press. p 53-104.
71. Mesleh MF, Lee S, Veglia G, Thiriot DS, Marassi FM, Opella SJ. 2003. Dipolar waves map the structure and topology of helices in membrane proteins. J Am Chem Soc 125:8928-8935.
72. Kovacs FA, Denny JK, Song Z, Quine JR, Cross TA. 2000. Helix tilt of the M2 transmembrane peptide from influenza A virus: an intrinsic property. J Mol Biol 295:117-125.
73. 2H NMR. Biophys J 83:1479-1488.
74. 3-phenylglycine labels. J Magn Reson 168:153-163.
75. 19F-NMR methods for studying biomembranes. Progr NMR Spectrosc (in press).
76. Wu CH, Ramamoorthy A, Opella SJ. 1994. High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J Magn Reson Ser A 109:270-272.
77. Ramamoorthy A, Wei YF, Lee D-K. 2004. PISEMA solid-state NMR spectroscopy. In: Webb GA, editor. Annual report on NMR spectroscopy 52. New York: Academic Press; p 1-52.
78. 15N solid-state NMR investigation in uniaxially aligned phospholipid bilayers. Biochemistry 37:16-22.
79. 15N-labeled helical membrane proteins in oriented lipid bilayers. J Magn Reson 144:156-161.
80. Vogt TCB, Schinzel S, Bechinger B. 2003. Biosynthesis of isotopically labeled gramicidins and tyrocidins by Bacillus brevis. J Biomol NMR 26:1-11.
81. Marassi FM. 2002. NMR of peptides and proteins in oriented membranes. Concepts Magn Reson 14:212-224.
82. Marassi FM, Opella SJ. 2000. A solid-state NMR index of helical membrane protein structure and topology. J Magn Reson 144:150-155.
83. Wang J, Denny J, Tian C, Kim S, Mo Y, Kovacs F, Song Z, Nishimura K, Gan Z, Fu R, Quine JR, Cross TA. 2000. Imaging membrane protein helical wheels. J Magn Reson 144:162-167.
84. Marcotte I, Wegener KL, Lam YH, Chia BCS, de Planque MRR, Bowie JH, Auger M, Separovic F. 2003. Interaction of antimicrobial peptides from Australian amphibians with lipid membranes. Chem Phys Lipids 122:107-120.
85. 1H dipolar correlation solid state NMR experiments. J Biomol NMR 26:283-295.
86. Smith R, Separovic F, Milne TJ, Whittaker A, Bennett FM, Cornell BA, Makriyannis A. 1994. Structure and orientation of the pore-forming peptide, melittin, in lipid bilayers. J Mol Biol 241:456-466.
87. Lam YH, Wassall SR, Morton CJ, Smith R, Separovic F. 2001. Solid-state NMR structure determination of melittin in a lipid environment. Biophys J 81:2752-2761.
88. Gabrys CM, Yang J, Weliky DP. 2003. Analysis of local conformation of membrane-bound and polycrystalline peptides by two-dimensional slow-spinning rotor-synchronized MAS exchange spectroscopy. J Biomol NMR 26:49-68.
89. Hirsh DJ, Hammer J, Maloy WL, Blazyk J, Schaefer J. 1996. Secondary structure and location of a magainin analogue in synthetic phospholipid bilayers. Biochemistry 35:12733-12741.
90. 13C NMR spectroscopy. Biophys J 78: 2405-2417.
91. Henzler Wildman KA, Lee DK, Ramamoorthy A. 2003. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42:6545-6558.
92. Murata M, Nagayama K, Ohnishi S. 1987. Membrane fusion activity of succinylated melittin is triggered by protonation of its carboxyl groups. Biochemistry 26: 4056-4062.
93. Buffy JJ, Waring AJ, Lehrer RI, Hong M. 2003. Immobilization and aggregation of the antimicrobial peptide protegrin-1 in lipid bilayers investigated by solid-state NMR. Biochemistry 42:13725-13734.
94. Yamaguchi S, Hong T, Waring A, Lehrer RI, Hong M. 2002. Solid-state NMR investigations of peptide-lipid interaction and orientation of a β-sheet antimicrobial peptide, protegrin. Biochemistry 41:9852-9862.
95. 2+. Biophys J 85:2363-2373.
96. Raleigh DP, Levitt MH, Griffin RG. 1988. Rotational resonance in solid-state NMR. Chem Phys Lett 146: 71-76.
97. Griffin RG. 1998. Dipolar recoupling in MAS spectra of biological solids. Nat Struct Biol 5(Suppl):508-512.
98. Gullion T, Schaefer J. 1989. Rotational-echo double-resonance NMR. J Magn Reson 81:196-200.
99. Toke O, Maloy WL, Kim SJ, Blazyk J, Schaefer J. 2004. Secondary structure and lipid contact of a peptide antibiotic in phospholipid bilayers by REDOR. Biophys J 87:662-674.
100. 3 aggregates in phospholipid bilayers by solid-state NMR. Biophys J 87:675-687.
101. Dempsey CE, Cryer GD, Watts A. 1987. The interaction of amino-deuteromethylated melittin with phospholipid membranes studied by deuterium NMR. FEBS Lett 218:173-177.
102. 2H-solid state NMR. Diploma thesis. University of Karlsruhe, Germany. p 31.
103. 2H NMR study of peptide phosphorylation effects in a bilayer environment. Biochemistry 37:7504-7508.
104. Whiles JA, Glover KJ, Vold RR, Komives EA. 2002. Methods for studying transmembrane peptides in bicelles: consequences of hydrophobic mismatch and peptide sequence. J Magn Reson 158:149-156.
105. 2H-NMR. Biochemistry 33: 5370-5375.
106. Ulrich AS, Wallat I, Heyn MP, Watts A. 1995. Realignment of the retinal chromophore in the M-photointermediate of bacteriorhodopsin. Nature Struct Biol 2:190-192.
107. Dempsey CE, Handcock LJ. 1996. Hydrogen bond stabilities in membrane-reconstituted alamethicin from amide-resolved hydrogen-exchange measurements. Biophys J 70:1777-1788.
108. 2H NMR spectroscopy. J Magn Reson 155:244-250.
109. 19F solid state NMR. In: Holmes J. Encyclopedia of spectroscopy and spectrometry. London: Academic Press. p 813-825.
110. 19F-labeled tryptophan in gramicidin A in oriented membranes. Biophys J 83:3336-3350.
111. 19F-NMR. J Biomol NMR 21:191-208.
112. 19F homonuclear dipolar couplings, obtained by multipulse solid-state NMR on static and oriented systems. J Magn Reson 138:98-106.
113. 19F dipolar couplings within a trifluoromethyl group are revealed by static multipulse NMR in the solid state. J Magn Reson 146:81-88.
114. 19F-NMR. Ph.D. thesis. Friedrich-Schiller- Universität Jena, Germany. p 99.
115. 19F NMR. Magn Reson Chem 42:195-203.
116. 19F-Festkörper-NMR-Untersuchungen zur Orientierung und Dynamik des antimikrobiellen Peptids PGLa in Lipidmembranen. Diploma thesis. Friedrich-Schiller-Universität Jena, Germany. p 97.
117. 19F NMR study. Biophys J 80:1406-1416.
118. 13C-NMR and circular-dichroism study. Eur J Biochem 54:395-409.
119. 1H NMR study of the solution structure of alamethicin. Biochemistry 26:1043-1050.
120. Chandrasekhar K, Das MK, Kumar A, Balaram P. 1988. Molecular conformation of alamethicin in dimethylsulfoxide solution. A 2D NMR study. Int J Pept Prot Res 32:167-174.
121. Wille B, Franz B, Jung G. 1989. Location and dynamics of alamethicin in unilamellar vesicles and thylakoids as model systems. A spin label study. Biochim Biophys Acta 986:47-60.
122. 13C NMR: implications for the mechanism of gating of a voltage-dependent channel. Biochemistry 31:5136-5144.
123. 1H NMR spectroscopy. Biochemistry 31:3135-3143.
124. 13C-labelling of alamethicin, an ion-channel-forming peptide. Eur J Biochem 243:283-291.
125. Rozek T, Wegener KL, Bowie JH, Olver IN, Carver JA, Wallace JC, Tyler MJ. 2000. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. The solution structure of aurein 1.2. Eur J Biochem 267: 5330-5341.
126. Wong H, Bowie JH, Carver JA. 1997. The solution structure and activity of caerin 1.1, an antimicrobial peptide from the Australian green tree frog, Litoria splendida. Eur J Biochem 247:545-557.
127. Chia BCS, Carver JA, Lindner RA, Bowie JH, Wong H, Lie W. 2000. Caerin 4.1, an antibiotic peptide from the Australian tree frog, Litoria caerulea. The NMR-derived solution structure. Aust J Chem 53:257-265.
128. Wegener KL, Carver JA, Bowie JH. 2003. The solution structures and activity of caerin 1.1 and caerin 1.4 in aqueous trifluoroethanol and dodecylphosphocholine micelles. Biopolymers 69:42-59.
129. Pukala TL, Brinkworth CS, Carver JA, Bowie JH. 2004. Investigating the importance of the flexible hinge in caerin 1.1: solution structures and activity of two synthetically modified caerin peptides. Biochemistry 43:937-944.
130. Holak TA, Engstrom A, Kraulis PJ, Lindeberg G, Bennich H, Jones TA, Gronenborn AM, Clore GM. 1988. The solution conformation of the antibacterial peptide cecropin A: a nuclear magnetic resonance and dynamical simulated annealing study. Biochemistry 27:7620-7629.
131. Sipos D, Andersson M, Ehrenberg A. 1992. The structure of the mammalian antibacterial peptide cecropin P1 in solution, determined by proton-NMR. Eur J Biochem 209:163-169.
132. Srisailam S, Arunkumar AI, Wang W, Yu C, Chen HM. 2000. Conformational study of a custom antibacterial peptide cecropin B1: implications of the lytic activity. Biochim Biophys Acta 1479:275-285.
133. Srisailam S, Kumar TKS, Arunkumar AI, Leung KW, Yu C, Chen HM. 2001. Crumpled structure of the custom hydrophobic lytic peptide cecropin B3. Eur J Biochem 268:4278-4284.
134. Kessler H, Mierke DF, Saulitis J, Seip S, Steuernagel S, Wein T, Will M. 1992. The structure of Ro 09-0198 in different environments. Biopolymers 32:427-433.
135. 1H-NMR. J Biochem (Tokyo) 119:226-230.
136. Wegener KL, Wabnitz PA, Carver JA, Bowie JH, Chia BCS, Wallace JC, Tyler MJ. 1999. Host defence peptides from the skin glands of the Australian blue mountains tree-frog Litoria citropa. Solution structure of the antibacterial peptide citropin 1.1. Eur J Biochem 265:627-637.
137. Doyle J, Brinkworth CS, Wegener KL, Carver JA, Llewellyn LE, Olver IN, Bowie JH, Wabnitz PA, Tyler MJ. 2003. nNOS inhibition, antimicrobial and anticancer activity of the amphibian skin peptide, citropin 1.1 and synthetic modifications. The solution structure of a modified citropin 1.1. Eur J Biochem 270:1141-1153.
138. Yu C, Hwang JF, Yeh CJ, Chuang LC. 1992. Solution conformation of gramicidin S determined by nuclear magnetic resonance and distance geometry calculation. J Chin Chem Soc-Taip 39:231-234.
139. Higashijima T, Miyazawa T, Kawai M, Nagai LJ. 1986. Gramicidin S analogs with a D-Ala, Gly, or L-Ala residue in place of the D-Phe residue: molecular conformations and interactions with phospholipid membrane. Biopolymers 25:2295-2307.
140. Chia BC, Carver JA, Mulhern TD, Bowie JH. 2000. Maculatin 1.1, an anti-microbial peptide from the Australian tree frog, Litoria genimaculata. Solution structure and biological activity. Eur J Biochem 267:1894-1908.
141. Marion D, Zasloff M, Bax A. 1988. A two-dimensional NMR study of the antimicrobial peptide magainin 2. FEBS Lett 227:21-26.
142. Strom R, Crifo C, Viti V, Guidoni L, Podo F. 1978. Variations in circular dichroism and proton-NMR relaxation properties of melittin upon interaction with phospholipids. FEBS Lett 96:45-50.
143. 1H-NMR studies of monomeric melittin in aqueous solution. Biochim Biophys Acta 622:219-230.
144. 1H-NMR studies of self-aggregation of melittin in aqueous solution. Biochim Biophys Acta 622:231-244.
145. Podo F, Strom R, Crifo C, Zulauf M. 1982. Dependence of melittin structure on its interaction with multivalent anions and with model membrane systems. Int J Pept Protein Res 19:514-527.
146. 1H-NMR study in methanol. Eur J Biochem 173:139-146.
147. 15N NMR. Biochemistry 34:13196-13202.
148. Bhattacharjya S, Venkatraman J, Kumar A, Balaram P. 1999. Fluoroalcohols as structure modifiers in peptides and proteins: hexafluoroacetone hydrate stabilizes a helical conformation of melittin at low pH. J Pept Res 54:100-111.
149. Prasch T, Naumann T, Markert RL, Sattler M, Schubert W, Schaal S, Bauch M, Kogler H, Griesinger C. 1997. Constitution and solution conformation of the antibiotic mersacidin determined by NMR and molecular dynamics. Eur J Biochem 244:501-512.
150. 1H NMR resonance assignment in aqueous and dimethyl sulphoxide solution. J Chem Soc Perkin Trans 1 2359-2367.
151. 13C-labeled media from Anabaena sp. for universal isotopic labeling of bacteriocins: NMR resonance assignments of leucocin A from Leuconostoc gelidum and nisin A from Lactococcus lactis. Biochemistry 32:310-318.
152. Sawai MV, Waring AJ, Kearney WR, McCray PB, Forsyth WR, Lehrer RI, Tack BF. 2002. Impact of single-residue mutations on the structure and function of ovispirin/novispirin antimicrobial peptides. Protein Eng 15:225-232.
153. Zagorski MG, Norman DG, Barrow CJ, Iwashita T, Tachibana K, Patel DJ. 1991. Solution structure of pardaxin P-2. Biochemistry 30:8009-8017.
154. Aumelas A, Mangoni M, Roumestand C, Chiche L, Despaux E, Grassy G, Calas B, Chavanieu A. 1996. Synthesis and solution structure of the antimicrobial peptide protegrin-1. Eur J Biochem 237:575-583.
155. Fahrner RL, Dieckmann T, Harwig SS, Lehrer RI, Eisenberg D, Feigon J. 1996. Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes. Chem Biol 3:543-550.
156. Lai JR, Huck BR, Weisblum B, Gellman SH. 2002. Design of non-cysteine-containing antimicrobial β-hairpins: structure-activity relationship studies with linear protegrin-1 analogues. Biochemistry 41:12835-12842.
157. Wade D, Silberring J, Soliymani R, Heikkinen S, Kilpelainen I, Lankinen H, Kuusela P. 2000. Antibacterial activities of temporin A analogs. FEBS Lett 479:6-9.
158. Balashova TA, Shenkarev ZO, Tagaev AA, Ovchinnikova TV, Raap J, Arseniev AS. 2000. NMR structure of the channel-former zervamicin IIB in isotropic solvents. FEBS Lett 466:333-336.
159. 15N NMR relaxation. FEBS Lett 495:52-55.
160. 15N NMR assignment. J Pept Sci 9:817-826.
161. 1H NMR. Evidence for conformational heterogeneity in a voltage-gated peptide. Biochemistry 33: 4036-4045.
162. Yee A, Szymczyna B, O'Neil JD. 1999. Backbone dynamics of detergent-solubilized alamethicin from amide hydrogen exchange measurements. Biochemistry 38:6489-6498.
163. Oh D, Shin SY, Lee S, Kang JH, Kim SD, Ryu PD, Hahm KS, Kim Y. 2000. Role of the hinge region and the tryptophan residue in the synthetic antimicrobial peptides, cecropin A(1-8)-magainin 2(1-12) and its analogues, on their antibiotic activities and structures. Biochemistry 39:11855-11864.
164. Beyer K, Huber T. 1999. Mixed micelle formation between gramicidin-S and a nonionic detergent: a nuclear magnetic resonance model study of peptide/detergent aggregation. Eur Biophys J 28:166-173.
165. Rana FR, Sultany CM, Blazyk J. 1990. Interactions between Salmonella typhimurium lipopolysaccharide and the antimicrobial peptide, magainin 2 amide. FEBS Lett 261:464-467.
166. Veglia G, Zeri AC, Ma C, Opella SJ. 2002. Deuterium/hydrogen exchange factors measured by solution nuclear magnetic resonance spectroscopy as indicators of the structure and topology of membrane proteins. Biophys J 82:2176-2183.
167. Hicks RP, Mones E, Kim H, Koser BW, Nichols DA, Bhattacharjee AK. 2003. Comparison of the conformation and electrostatic surface properties of magainin peptides bound to sodium dodecyl sulfate and dodecylphosphocholine micelles. Biopolymers 68: 459-470.
168. De Bony J, Dufourcq J, Clin B. 1979. Lipid-protein interactions: NMR study of melittin and its binding to lysophosphatidylcholine. Biochim Biophys Acta 552: 531-534.
169. 1H-NMR assignments and global conformational features. Biochim Biophys Acta 647:95-111.
170. Brown LR, Braun W, Kumar A, Wuthrich K. 1982. High resolution nuclear magnetic resonance studies of the conformation and orientation of melittin bound to a lipid-water interface. Biophys J 37:319-328.
171. Inagaki F, Shimada I, Kawaguchi K, Hirano M, Terasawa I, Ikura T, Go N. 1989. Structure of melittin hound to perdeuterated dodecylphosphocholine micelles as studied by two-dimensional NMR and distance geometry calculations. Biochemistry 28:5985-5991.
172. Ikura T, Go N, Inagaki F. 1991. Refined structure of melittin bound to perdeuterated dodecylphosphocholine micelles as studied by 2D-NMR and distance geometry calculation. Proteins 9:81-89.
173. De Jongh HH, Killian JA, De Kruijff B. 1992. A water-lipid interface induces a highly dynamic folded state in apocytochrome c and cytochrome c, which
174. 13C NMR characterization of the structure and dynamics of synthetic melittin and melittin analogs in lipid environments. Biochemistry 31:1301-1313.
175. Yuan P, Fisher PJ, Prendergast FG, Kemple MD. 1996. Structure and dynamics of melittin in lysomyristoyl phosphatidylcholine micelles determined by nuclear magnetic resonance. Biophys J 70:2223-2238.
176. Hsu STD, Breukink E, Bierbaum G, Sahl HG, De Kruijff B, Kaptein R, Van Nuland NAJ, Bonvin AMJJ. 2003. NMR study of mersacidin and lipid II interaction in dodecylphosphocholine micelles. Conformational changes are a key to antimicrobial activity. J Biol Chem 278:13110-13117.
177. Van den Hooven HW, Doeland CC, Van de Kamp M, Konings RN, Hilbers CW, Van de Ven FJ. 1996. Three-dimensional structure of the lantibiotic nisin in the presence of membrane-mimetic micelles of dodecylphosphocholine and of sodium dodecylsulphate. Eur J Biochem 235:382-393.
178. Van den Hooven HW, Spronk CA, Van de Kamp M, Konings RN, Hilbers CW, Van de Van FJ. 1996. Surface location and orientation of the lantibiotic nisin bound to membrane-mimicking micelles of dodecylphosphocholine and of sodium dodecylsulphate. Eur J Biochem 235:394-403.
179. Hsu ST, Breukink E, De Kruijff B, Kaptein R, Bonvin AMJJ, Van Nuland NAJ. 2002. Mapping the targeted membrane pore formation mechanism by solution NMR: The nisin Z and lipid II interaction in SDS micelles. Biochemistry 41:7670-7676.
180. Bechinger B, Zasloff M, Opella SJ. 1998. Structure and dynamics of the antibiotic peptide PGLa in membranes by solution and solid-state nuclear magnetic resonance spectroscopy. Biophys J 74:981-987.
181. Roumestand C, Louis V, Aumelas A, Grassy G, Calas B, Chavanieu A. 1998. Oligomerization of protegrin-1 in the presence of DPC micelles. A proton high-resolution NMR study. FEBS Lett 421:263-267.
182. Shenkarev ZO, Balashova TA, Efremov RG, Yakimenko ZA, Ovchinnikova TV, Raap J, Arseniev AS. 2002. Spatial structure of zervamicin IIB bound to DPC micelles: implications for voltage-gating. Biophys J 82:762-771.
183. Hauser H, Finer EG, Chapman D. 1970. Nuclear magnetic resonance studies of the polypeptide alamethicin and its interaction with phospholipids. J Mol Biol 53:419-433.
184. Lau AL, Chan SI. 1974. Nuclear magnetic resonance studies of the interaction of alamethicin with lecithin bilayers. Biochemistry 13:4942-4948.
185. Lau AL, Chan SI. 1975. Alamethicin-mediated fusion of lecithin vesicles. Proc Natl Acad Sci USA 72: 2170-2174.
186. Lau AL, Chan SI. 1976. Voltage-induced formation of alamethicin pores in lecithin bilayer vesicles. Biochemistry 15:2551-2555.
187. 1H-NMR spectroscopy. Bioscience Rep 2:921-928.
188. 1H-NMR investigation of the effects of ethanol and general anaesthetics on ion channels and membrane fusion using unilamellar phospholipid membranes. Biochim Biophys Acta 736: 1-10.
189. 2H NMR study. Biochemistry 24:7621-7627.
190. Keller SL, Gruner SM, Gawrisch K. 1996. Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim Biophys Acta 1278:241-246.
191. Balla MS, Bowie JH, Separovic F. 2004. Solid-state NMR study of antimicrobial peptides from Australian frogs in phospholipid membranes. Eur Biophys J 33: 109-116.
192. Jayasinghe S, Barranger-Mathys M, Ellena JF, Franklin C, Cafiso DS. 1998. Structural features that modulate the transmembrane migration of a hydrophobic peptide in lipid vesicles. Biophys J 74:3023-3030.
193. 31P NMR study of the interaction of amphibian antimicrobial peptides with the membranes of live bacteria. Lett Pept Sci 7:151-156.
194. Machaidze G, Ziegler A, Seelig J. 2002. Specific-binding of Ro 09-0198 (cinnamycin) to phosphatidylethanolamine: a thermodynamic analysis. Biochemistry 41:1965-1971.
195. Datema KP, Pauls KP, Bloom M. 1986. Deuterium nuclear magnetic resonance investigation of the exchangeable sites on gramicidin A and gramicidin S in multilamellar vesicles of dipalmitoylphosphatidylcholine. Biochemistry 25:3796-3803.
196. Zidovetzki R, Banerjee U, Harrington DW, Chan SI. 1988. NMR study of the interactions of polymyxin B, gramicidin S, and valinomycin with dimyristoyllecithin bilayers. Biochemistry 27:5686-5692.
197. Prenner EJ, Lewis RN, Neuman KC, Gruner SM, Kondejewski LH, Hodges RS, McElhaney RN. 1997. Nonlamellar phases induced by the interaction of gramicidin S with lipid bilayers. A possible relationship to membrane-disrupting activity. Biochemistry 36:7906-7916.
198. Henzler-Wildman KA, Martinez GV, Brown MF, Ramamoorthy A. 2004. Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43:8459-8469.
199. Bechinger B, Zasloff M, Opella SJ. 1992. Structure and interactions of magainin antibiotic peptides in lipid bilayers: a solid-state nuclear magnetic resonance investigation. Biophys J 62:12-14.
200. Hallock KJ, Lee DK, Ramamoorthy A. 2003. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys J 84:3052-3060.
201. Tsai TC, Jiang RT, Tsai MD. 1984. Phospholipids chiral at phosphorus. Properties of small unilamellar vesicles of chiral thiophosphatidylcholine. Biochemistry 23:5564-5570.
202. II phase formation in cardiolipin model membranes. Biochim Biophys Acta 903:142-154.
203. Batenburg AM, Van Esch JH, Leunissen-Bijvelt J, Verkleij AJ, De Kruijff B. 1987. Interaction of melittin with negatively charged phospholipids: consequences for lipid organization. FEBS Lett 223:148-154.
204. 2. Biochemistry 26:5803-5811.
205. 13C-NMR investigation of the insertion of the bee venom melittin into lecithin vesicles. Eur Biophys J 15:1-12.
206. Batenburg AM, Van Esch JH, De Kruijff B. 1988. Melittin-induced changes of the macroscopic structure of phosphatidylethanolamines. Biochemistry 27:2324-2331.
207. Dempsey C, Bitbol M, Watts A. 1989. Interaction of melittin with mixed phospholipid-membranes composed of dimyristoylphosphatidylcholine and dimyristoylphosphatidylserine studied by deuterium NMR. Biochemistry 28:6590-6596.
208. 31P-NMR. Effects of amphipatic peptidic toxins on phospholipid and biological membranes. Biochimie 71:117-123.
209. Fraser PE, Rand RP, Deber CM. 1989. Bilayer-stabilizing properties of myelin basic protein in dioleoylphosphatidylethanolamine systems. Biochim Biophys Acta 983:23-29.
210. 1H-NMR study of the influence of n-alcohols on the stoichiometry of melittin-induced permeability of phospholipid vesicles. Biochim Biophys Acta 985:106-110.
211. Kuchinka E, Seelig J. 1989. Interaction of melittin with phosphatidylcholine membranes. Binding isotherm and lipid head-group conformation. Biochemistry 28:4216-4221.
212. Beschiaschvili G, Seelig J. 1990. Melittin binding to mixed phosphatidylglycerol/phosphatidylcholine membranes. Biochemistry 29:52-58.
213. 2+ on the permeability of phospholipid vesicles. J Inorg Biochem 40:217-225.
214. Beschiaschvili G, Baeuerle HD. 1991. Effective charge of melittin upon interaction with POPC vesicles. Biochim Biophys Acta 1068:195-200.
215. Dempsey CE, Sternberg B. 1991. Reversible disk-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin. Biochim Biophys Acta 1061:175-184.
216. Smith R, Separovic F, Bennett FC, Cornell BA. 1992. Melittin-induced changes in lipid multilayers. A solid-state NMR study. Biophys J 63:469-474.
217. Dufourcq J, Dufourc EJ, Maillet JC, Cornut I, Thiaudiere E, Bonmatin JM. 1993. Peptide-induced changes in structure, dynamic and barrier properties of liposomes and membranes. Phosphor Sulfur 77:665-668.
218. 31P NMR methods for investigating phospholipid-based molecular-structure and dynamics. Phosphor Sulfur 77:673-676.
219. Monette M, Van Calsteren MR, Lafleur M. 1993. Effect of cholesterol on the polymorphism of dipalmitoylphosphatidylcholine/melittin complexes: an NMR study. Biochim Biophys Acta 1149:319-328.
220. 31P-NMR study. Biochim Biophys Acta 1234:235-243.
221. Monette M, Lafleur M. 1995. Modulation of melittin-induced lysis by surface charge density of membranes. Biophys J 68:187-195.
222. 31P-NMR study. Biophys J 68:965-977.
223. Monette M, Lafleur M. 1996. Influence of lipid chain unsaturation on melittin-induced micellization. Biophys J 70:2195-2202.
224. Pott T, Dufourcq J, Dufourc EJ. 1996. Fluid or gel phase lipid bilayers to study peptide membrane interactions? Eur Biophys J 25:55-59.
225. Benachir T, Monette M, Grenier J, Lafleur M. 1997. Melittin-induced leakage from phosphatidylcholine vesicles is modulated by cholesterol: a property used for membrane targeting. Eur Biophys J 25: 201-210.
226. 31P two-dimensional exchange solid-state NMR study. Biophys J 74:857-868.
227. Pott T, Paternostre M, Dufourc EJ. 1998. A comparative study of the action of melittin on sphingomyelin and phosphatidylcholine bilayers. Eur Biophys J 27: 237-245.
228. Pott T, Maillet JC, Abad C, Campos A, Dufourcq J, Dufourc EJ. 2001. The lipid charge density at the bilayer surface modulates the effects of melittin on membranes. Chem Phys Lipids 109:209-223.
229. Driessen AJ, Van den Hooven HW, Kuiper W, Van de Kamp M, Sahl HG, Konings RN, Konings WN. 1995. Mechanistic studies of lantibiotic-induced permeabilization of phospholipid vesicles. Biochemistry 34: 1606-1614.
230. El Jastimi R, Lafleur M. 1999. Nisin promotes the formation of non-lamellar inverted phases in unsaturated phosphatidylethanolamines. Biochim Biophys Acta 1418:97-105.
231. El Jastimi R, Edwards K, Lafleur M. 1999. Characterization of permeability and morphological perturbations induced by nisin on phosphatidylcholine membranes. Biophys J 77:842-852.
232. 2H NMR study. Biochemistry 39:11425-11433.
233. Yamaguchi S, Huster D, Waring A, Lehrer RI, Kearney W, Tack BF, Hong M. 2001. Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR spectroscopy. Biophys J 81:2203-2214.
234. Hallock KJ, Lee DK, Omnaas J, Mosberg HI, Ramamoorthy A. 2002. Membrane composition determines pardaxin's mechanism of lipid bilayer disruption. Biophys J 83:1004-1013.
235. Wieprecht T, Apostolov O, Beyermann M, Seelig J. 2000. Membrane binding and pore formation of the antibacterial peptide PGLa: thermodynamic and mechanistic aspects. Biochemistry 39:442-452.
236. Buffy JJ, McCormick MJ, Wi S, Waring A, Lehrer RI, Hong M. 2004. Solid-state NMR investigation of the selective perturbation of lipid bilayers by the cyclic antimicrobial peptide RTD-1. Biochemistry 43:9800-9812.
237. 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes. Biochemistry 40: 9428-9437.
238. 15N NMR. Biophys J 69:2392-2397.
239. 15N solid-state nuclear magnetic resonance. Biophys J 81:1684-1698.
240. Marassi FM, Opella SJ, Juvvadi P, Merrifield RB. 1999. Orientation of cecropin A helices in phospholipid bilayers determined by solid-state NMR spectroscopy. Biophys J 77:3152-3155.
241. Bechinger B, Kim Y, Chirlian LE, Gesell J, Neumann JM, Montal M, Tomich J, Zasloff M, Opella SJ. 1991. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J Biomol NMR 1:167-173.
242. Bechinger B, Zasloff M, Opella SJ. 1993. Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Protein Sci 2:2077-2084.
243. Ramamoorthy A, Marassi FM, Zasloff M, Opella SJ. 1995. Three-dimensional solid-state NMR spectroscopy of a peptide oriented in membrane bilayers. J Biomol NMR 6:329-334.
244. Bechinger B, Gierasch LM, Montal M, Zasloff M, Opella SJ. 1996. Orientations of helical peptides in membrane bilayers by solid state NMR spectroscopy. Solid State Nucl Magn Reson 7:185-191.
245. Lee DK, Santos JS, Ramamoorthy A. 1999. Application of one-dimensional dipolar shift solid-state NMR spectroscopy to study the backbone conformation of membrane-associated peptides in phospholipid bilayers. J Phys Chem B 103:8383-8390.
246. 1H amide chemical shift tensor in structure determination of proteins by solid-state NMR spectroscopy. Appl Magn Reson 17:433-447.
247. Ganapathy S, Eads TM, Chacko VP, Bryant RG. 1985. Elimination of baseline artifacts in solid-state NMR-spectra by spin locking. J Magn Reson 62:314-315.