19F NMR screening of unrelated antimicrobial peptides shows that membrane interactions are largely governed by lipids

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 9, 2014, Pages 2260-2268

  Afonin, Sergii ^a   Glaser, Ralf W ^b   Sachse, Carsten ^c   Salgado, Jesús ^d   Wadhwani, Parvesh ^a   Ulrich, Anne S ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Amphiphilic antimicrobial peptides; Bacterial membranes; Lipid composition; Re alignment in membrane; Spontaneous curvature

Indexed keywords

AMPHOPHILE; CHOLESTEROL; GRAMICIDIN S; LIPID; PHOSPHATIDYLCHOLINE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN PGLA; UNCLASSIFIED DRUG; GRAMICIDIN; MEMBRANE LIPID; PGLA PREPROPEPTIDE; PROTEIN PRECURSOR;

ALPHA HELIX; ARTICLE; BACTERIAL MEMBRANE; CELL SURFACE; CELL TYPE; FLUORINE NUCLEAR MAGNETIC RESONANCE; LIPID COMPOSITION; LIPID MEMBRANE; MELTING POINT; OLIGOMERIZATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; STATIC ELECTRICITY; AMINO ACID SEQUENCE; AMPHIPHILIC ANTIMICROBIAL PEPTIDES; BACTERIAL MEMBRANES; BACTERIUM; CELL MEMBRANE; CHEMISTRY; DRUG EFFECT; HUMAN; LIPID BILAYER; NUCLEAR MAGNETIC RESONANCE; PROTEIN SECONDARY STRUCTURE; RE-ALIGNMENT IN MEMBRANE; SOLID STATE (19)F NMR STRUCTURE ANALYSIS; SPONTANEOUS CURVATURE;

ANIMALIA; BACTERIA (MICROORGANISMS);

AMPHIPHILIC ANTIMICROBIAL PEPTIDES; BACTERIAL MEMBRANES; LIPID COMPOSITION; RE-ALIGNMENT IN MEMBRANE; SOLID STATE (19)F NMR STRUCTURE ANALYSIS; SPONTANEOUS CURVATURE;

AMINO ACID SEQUENCE; BACTERIA; CELL MEMBRANE; GRAMICIDIN; HUMANS; LIPID BILAYERS; MEMBRANE LIPIDS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN PRECURSORS; PROTEIN STRUCTURE, SECONDARY;

EID: 84906997364     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.03.017     Document Type: Article

References (79)

1. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (Pubitemid 34100944)
2. L.M. Rossi, P. Rangsamy, J. Zhang, X.Q. Qiu, and G.Y. Wu Research advances in the development of peptide antibiotics J. Pharm. Sci. 97 2008 1060 1070
3. A.R. Koczulla, and R. Bals Antimicrobial peptides: current status and therapeutic potential Drugs 63 2003 389 406 (Pubitemid 36259526)
4. L. Kuhn-Nentwig Antimicrobial and cytolytic peptides of venomous arthropods Cell. Mol. Life Sci. 60 2003 2651 2668 (Pubitemid 38041366)
5. E. de Leeuw, and W. Lu Human defensins: turning defense into offense Infect. Disord. Drug Targets 7 2007 67 70 (Pubitemid 46488262)
6. N.P. West, D.B. Pyne, G. Renshaw, and A.W. Cripps Antimicrobial peptides and proteins, exercise and innate mucosal immunity FEMS Immunol. Med. Microbiol. 48 2006 293 304 (Pubitemid 44736567)
7. J. Harder, R. Glaser, and J.M. Schroder The role and potential therapeutical applications of antimicrobial proteins in infectious and inflammatory diseases Endocr. Metab. Immune Disord. Drug Targets 7 2007 75 82 (Pubitemid 46965217)
8. K.L. Brown, and R.E.W. Hancock Cationic host defense (antimicrobial) peptides Curr. Opin. Immunol. 18 2006 24 30 (Pubitemid 43049644)
9. H. Jenssen, P. Hamill, and R.E.W. Hancock Peptide antimicrobial agents Clin. Microbiol. Rev. 19 2006 491 511 (Pubitemid 44137212)
10. R.E.W. Hancock, and A. Rozek Role of membranes in the activities of antimicrobial cationic peptides FEMS Microbiol. Lett. 206 2002 143 149 (Pubitemid 34117610)
11. D. Wade, A. Boman, B. Wahlin, C.M. Drain, D. Andreu, H.G. Boman, and R.B. Merrifield All-D amino acid-containing channel-forming antibiotic peptides Proc. Natl. Acad. Sci. U. S. A. 87 1990 4761 4765
12. R. Bessalle, A. Kapitkovsky, A. Gorea, I. Shalit, and M. Fridkin All-D-magainin: chirality, antimicrobial activity and proteolytic resistance FEBS Lett. 274 1990 151 155 (Pubitemid 20378143)
13. N. Papo, and Y. Shai Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides 24 2003 1693 1703 (Pubitemid 38198076)
14. E. Glukhov, M. Stark, L.L. Burrows, and C.M. Deber Basis for selectivity of cationic antimicrobial peptides for bacterial versus mammalian membranes J. Biol. Chem. 280 2005 33960 33967 (Pubitemid 41443116)
15. R.M. Epand, and R.F. Epand Bacterial membrane lipids in the action of antimicrobial agents J. Pept. Sci. 17 2011 298 305
16. K. Matsuzaki, K. Sugishita, N. Fujii, and K. Miyajima Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2 Biochemistry 34 1995 3423 3429
17. K. Matsuzaki Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes Biochim. Biophys. Acta 1462 1999 1 10
18. Y. Shai Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides Biochim. Biophys. Acta 1462 1999 55 70
19. L. Yang, T.M. Weiss, R.I. Lehrer, and H.W. Huang Crystallization of antimicrobial pores in membranes: magainin and protegrin Biophys. J. 79 2000 2002 2009
20. 19F NMR label to monitor and to control peptide aggregation in membranes J. Am. Chem. Soc. 130 2008 16515 16517
21. 19 F NMR J. Am. Chem. Soc. 134 2012 6512 6515
22. 3 in membranes Phys. Chem. Chem. Phys. 15 2013 8962 8971
23. E. Strandberg, and A.S. Ulrich NMR methods for studying membrane-active antimicrobial peptides Concepts Magn. Reson. A 23A 2004 89 120 (Pubitemid 40646213)
24. 19F NMR methods for studying biomembranes Prog. NMR Spectr. 46 2005 1 21 (Pubitemid 40357060)
25. A. Drechsler, and F. Separovic Solid-state NMR structure determination IUBMB Life. 55 2003 515 523 (Pubitemid 37462707)
26. M. Hong Oligomeric structure, dynamics, and orientation of membrane proteins from solid-state NMR Structure 14 2006 1731 1740 (Pubitemid 44855624)
27. 19F-nuclear magnetic resonance analysis of membrane-active peptides A. Ramamoorthy, NMR Spectroscopy of Biological Solids 2006 Taylor & Francis 215 236
28. 19F-NMR V. Soloshonok, K. Mikami, T. Yamazaki, J.T. Welch, J. Honek, Current Fluoroorganic Chemistry 2007 American Chemical Society Washington, DC
29. 19F-NMR of peptides in native membranes Top. Curr. Chem. 306 2008 89 118
30. 19F-NMR labels for structural studies of membrane-bound peptides V. Gouverneur, K. Müller, Fluorine in Pharmaceutical and Medicinal Chemistry: From Biophysical Aspects to Clinical Applications 2012 Imperial College Press 91 138
31. M. Auger Biological membrane structure by solid-state NMR Curr. Issues Mol. Biol. 2 2000 119 124
32. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes Biochim. Biophys. Acta 515 1978 105 140 (Pubitemid 8398025)
33. A. Ramamoorthy Preface Biochim. Biophys. Acta 1758 2006 1177 (and titles there in, Special issue "Membrane Biophysics of Antimicrobial Peptides") (Pubitemid 44436090)
34. S. Afonin, D. Juretić, F. Separovic, and A.S. Ulrich Special issue on membrane-active peptides Eur. Biophys. J. 40 2011 347 348 (and titles there in, Special issue on membrane-active peptides)
35. S.L. Grage, S. Afonin, and A.S. Ulrich Dynamic transitions of membrane-active peptides Methods Mol. Biol. 618 2010 183 207
36. 3-phenylglycine labels J. Magn. Reson. 168 2004 153 163
37. 19F-NMR Biophys. J. 88 2005 3392 3397 (Pubitemid 40586589)
38. 2H-NMR Biochim. Biophys. Acta 1758 2006 1330 1342 (Pubitemid 44436073)
39. P. Tremouilhac, E. Strandberg, P. Wadhwani, and A.S. Ulrich Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin J. Biol. Chem. 281 2006 32089 32094 (Pubitemid 46036763)
40. J. Bürck, S. Roth, P. Wadhwani, S. Afonin, N. Kanithasen, E. Strandberg, and A.S. Ulrich Conformation and membrane orientation of amphiphilic helical peptides by oriented circular dichroism Biophys. J. 95 2008 3872 3881
41. 19F NMR spectroscopy J. Am. Chem. Soc. 130 2008 16512 16514
42. E. Strandberg, P. Tremouilhac, P. Wadhwani, and A.S. Ulrich Synergistic transmembrane insertion of the heterodimeric PGLa/magainin 2 complex studied by solid-state NMR Biochim. Biophys. Acta 1788 2009 1667 1679
43. E. Strandberg, J. Zerweck, P. Wadhwani, and A.S. Ulrich Synergistic insertion of antimicrobial magainin-family peptides in membranes depends on the lipid spontaneous curvature Biophys. J. 104 2013 L9 L11
44. E. Strandberg, D. Tiltak, S. Ehni, P. Wadhwani, and A.S. Ulrich Lipid shape is a key factor for membrane interactions of amphipathic helical peptides Biochim. Biophys. Acta 1818 2012 1764 1776
45. 19F-NMR J. Biomol. NMR 21 2001 191 208 (Pubitemid 33133421)
46. S. Afonin, U.H.N. Dürr, P. Wadhwani, J. Salgado, and A.S. Ulrich Solid state NMR structure analysis of the antimicrobial peptide gramicidin s in lipid membranes: concentration-dependent re-alignment and self-assembly as a β-barrel Top. Curr. Chem. 273 2008 139 154
47. W.L. Maloy, and U.P. Kari Structure-activity studies on magainins and other host defense peptides Biopolymers 37 1995 105 122
48. J.P. Ulmschneider, J.C. Smith, M.B. Ulmschneider, A.S. Ulrich, and E. Strandberg Reorientation and dimerization of the membrane-bound antimicrobial peptide PGLa from microsecond all-atom MD simulations Biophys. J. 103 2012 472 482
49. Wang et al. in "current issue of BBA".
50. M. Berditsch, S. Afonin, and A.S. Ulrich The ability of Aneurinibacillus migulanus (Bacillus brevis) to produce the antibiotic gramicidin S is correlated with phenotype variation Appl. Environ. Microbiol. 73 2007 6620 6628 (Pubitemid 47623722)
51. G.G. Gause, and M.G. Brazhnikova Gramicidin S and its use in the treatment of infected wounds Nature 154 1944 703
52. N. Izumiya, T. Kato, H. Aoyaga, M. Waki, and M. Kondo Synthetic Aspects of Biologically Active Cyclic Peptides: Gramicidin S and Tyrocidines 1979 Halsted Press NY
53. 19F-NMR structure analysis of membrane-bound peptides J. Pept. Sci. 13 2007 614 623 (Pubitemid 47490326)
54. 19F NMR structure analysis of membrane-associated peptides ChemBioChem 4 2003 1151 1163 (Pubitemid 37462816)
55. 19 F NMR spectroscopy Angew. Chem. Int. Ed. 45 2006 5659 5661 (Pubitemid 44366771)
56. 19F-NMR Biophys. J. 90 2006 1676 1686
57. 19F NMR analysis of the antimicrobial peptide PGLa bound to native cell membranes from bacterial protoplasts and human erythrocytes J. Am. Chem. Soc. 132 2010 8822 8824
58. P. Wadhwani, S. Afonin, M. Ieronimo, J. Buerck, and A.S. Ulrich Optimized protocol for synthesis of cyclic gramicidin S: starting amino acid is key to high yield J. Org. Chem. 71 2006 55 61 (Pubitemid 43128058)
59. A.L. van Geet Calibration of methanol nuclear magnetic resonance thermometer at low temperature Anal. Chem. 42 1970 679 680
60. R.W. Glaser, and A.S. Ulrich Susceptibility corrections in solid-state NMR experiments with oriented membrane samples. Part I: Applications J. Magn. Reson. 164 2003 104 114
61. R. Koynova, and M. Caffrey Phases and phase transitions of the phosphatidylcholines Biochim. Biophys. Acta 1376 1998 91 145 (Pubitemid 28321526)
62. A. Latal, G. Degovics, R.F. Epand, R.M. Epand, and K. Lohner Structural aspects of the interaction of peptidyl-glycylleucine-carboxyamide, a highly potent antimicrobial peptide from frog skin, with lipids Eur. J. Biochem. 248 1997 938 946 (Pubitemid 27400053)
63. K. Lohner, and S.E. Blondelle Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics Comb. Chem. High Throughput Screen. 8 2005 241 256 (Pubitemid 40488604)
64. R.W. Williams, R. Starman, K.M. Taylor, K. Gable, T. Beeler, M. Zasloff, and D. Covell Raman spectroscopy of synthetic antimicrobial frog peptides magainin 2a and PGLa Biochemistry 29 1990 4490 4496 (Pubitemid 20153653)
65. J. Šajbidor Effect of some environmental factors on the content and composition of microbial membrane lipids Crit. Rev. Biotechnol. 17 1997 87 103 (Pubitemid 127716372)
66. P.R. Cullis, and B. de Kruijff Lipid polymorphism and the functional roles of lipids in biological membranes Biochim. Biophys. Acta 559 1979 399 420
67. R.M. Epand, and R.F. Epand Domains in bacterial membranes and the action of antimicrobial agents Mol. Biosyst. 5 2009 580 587
68. M. Cudic, and L. Otvos Jr. Intracellular targets of antibacterial peptides Curr. Drug Targets 3 2002 101 106 (Pubitemid 34296201)
69. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250 (Pubitemid 40298223)
70. M.C. Blok, E.C. van der Neut-Kok, L.L. van Deenen, and J. de Gier The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes Biochim. Biophys. Acta 406 1975 187 196
71. S.W. Hui Geometry of phase-separated domains in phospholipid bilayers by diffraction-contrast electron microscopy Biophys. J. 34 1981 383 395 (Pubitemid 11117926)
72. H.J. Muller, M. Luxnat, and H.J. Galla Lateral diffusion of small solutes and partition of amphipaths in defect structures of lipid bilayers Biochim. Biophys. Acta 856 1986 283 289
73. M.C. Rheinstädter, and O.G. Mouritsen Small-scale structure in fluid cholesterol-lipid bilayers Curr. Opin. Colloid Interface 18 2013 440 447
74. K. Matsuzaki Control of cell selectivity of antimicrobial peptides Biochim. Biophys. Acta 1788 2009 1687 1692
75. G. Wang Determination of solution structure and lipid micelle location of an engineered membrane peptide by using one NMR experiment and one sample Biochim. Biophys. Acta 1768 2007 3271 3281 (Pubitemid 350236078)
76. G. Wang Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles J. Biol. Chem. 283 2009 32637 32643
77. G. Fuertes, D. Giménez, S. Esteban-Martín, O.L. Sánchez-Muñoz, and J. Salgado A lipocentric view of peptide-induced pores Eur. Biophys. J. 40 2011 399 415
78. J. Blazyk, R. Wiegand, J. Klein, J. Hammer, R.M. Epand, R.F. Epand, W.L. Maloy, and U.P. Kari A novel linear amphipathic β-sheet cationic antimicrobial peptide with enhanced selectivity for bacterial lipids J. Biol. Chem. 276 2001 27899 27906
79. D. Bolintineanu, E. Hazrati, T.H. Davis, R.I. Lehrer, and Y.N. Kaznessis Antimicrobial mechanism of pore-forming protegrin peptides: 100 pores to kill E. coli Peptides 31 2010 1 8