The role of spontaneous lipid curvature in the interaction of interfacially active peptides with membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 9, 2014, Pages 2250-2259

  Koller, Daniel ^a   Lohner, Karl ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

Antimicrobial peptide; Inverse hexagonal phase; Membrane curvature; Membrane disruption; Membrane interface; Non lamellar (cubic) phase

Indexed keywords

ALAMETHICIN; BETA 17; CELL PENETRATING PEPTIDE; CRP 4; LANCOVUTIDE; LANTHIOPEPTIN; M2 PEPTIDE; MELITTIN; MEMBRANE PROXIMAL EXTERNAL REGION; MSI 367; MSI 594; MSI 843; NISIN; NK 2; ORITAVANCIN; OXKI 1; OXKI 2; PENETRATIN; PEXIGANAN; PHENYLENE ETHYLENE; POLYPEPTIDE ANTIBIOTIC AGENT; POLYPHEMUSIN 1; PROTEGRIN 1; RL 16; RMAF 4; SURFACTIN; TEMPORIN B; TEMPORIN L; TP 1; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTIBIOTIC RESISTANCE; ANTINEOPLASTIC ACTIVITY; BIOLOGICAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; CYTOLYSIS; ELECTROSTATIC REPULSION; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; INCREASED INTERFACE PRESSURE; INCREASED SURFACE PRESSURE; LIPID COMPOSITION; LIPID MONOLAYER; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN STRUCTURE; REVIEW; STATIC ELECTRICITY; STRUCTURE ACTIVITY RELATION;

ANTIMICROBIAL PEPTIDE; INVERSE HEXAGONAL PHASE; MEMBRANE CURVATURE; MEMBRANE DISRUPTION; MEMBRANE INTERFACE; NON-LAMELLAR (CUBIC) PHASE;

AMINO ACIDS; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; CALORIMETRY, DIFFERENTIAL SCANNING; CELL MEMBRANE; HUMANS; HYDROGEN BONDING; LIPID BILAYERS; LIPIDS;

EID: 84903727207     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.05.013     Document Type: Review

References (140)

1. R.E.W. Hancock Review cationic peptides: effectors in innate immunity and novel antimicrobials Lancet Infect. Dis. 1 2001 156 164
2. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (Pubitemid 34100944)
3. K. Lohner New strategies for novel antibiotics: peptides targeting bacterial cell membranes Gen. Physiol. Biophys. 28 2009 105 116
4. S.E. Blondelle, and K. Lohner Optimization and high-throughput screening of antimicrobial peptides Curr. Pharm. Des. 16 28 2010 3204 3211
5. R. Rathinakumar, and W.C. Wimley High-throughput discovery of broad-spectrum peptide antibiotics FASEB J. 24 9 2010 3232 3238
6. R. Rathinakumar, W.F. Walkenhorst, and W.C. Wimley Broad-spectrum antimicrobial peptides by rational combinatorial design and high-throughput screening: the importance of interfacial activity J. Am. Chem. Soc. 131 22 2009 7609 7617
7. K. Hilpert, R. Volkmer-Engert, T. Walter, and R.E.W. Hancock High-throughput generation of small antibacterial peptides with improved activity Nat. Biotechnol. 23 8 2005 1008 1012 (Pubitemid 41114036)
8. K. Hilpert, and R.E.W. Hancock Use of luminescent bacteria for rapid screening and characterization of short cationic antimicrobial peptides synthesized on cellulose using peptide array technology Nat. Protoc. 2 7 2007 1652 1660
9. A. Cherkasov, K. Hilpert, C.D. Fjell, M. Waldbrook, S.C. Mullaly, R. Volkmer, and R.E.W. Hancock Use of artificial intelligence in the design of small peptide antibiotics effective against a broad spectrum of highly antibiotic-resistant superbugs ACS Chem. Biol. 4 1 2009 65 74
10. C.D. Fjell, H. Jenssen, K. Hilpert, W. a Cheung, N. Panté, R.E.W. Hancock, and A. Cherkasov Identification of novel antibacterial peptides by chemoinformatics and machine learning J. Med. Chem. 52 7 2009 2006 2015
11. B. Bechinger, and K. Lohner Detergent-like actions of linear amphipathic cationic antimicrobial peptides Biochim. Biophys. Acta 1758 9 2006 1529 1539 (Pubitemid 44436087)
12. B. Bechinger Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape Curr. Opin. Colloid Interface Sci. 14 5 2009 349 355
13. W.C. Wimley, and K. Hristova Antimicrobial peptides: successes, challenges and unanswered questions J. Membr. Biol. 239 1-2 2011 27 34
14. W.C. Wimley Describing the mechanism of antimicrobial peptide action with the interfacial activity model ACS Chem. Biol. 5 10 2010 905 917
15. Y. Jin, J. Hammer, M. Pate, Y. Zhang, F. Zhu, E. Zmuda, and J. Blazyk Antimicrobial activities and structures of two linear cationic peptide families with various amphipathic β-sheet and α-helical potentials antimicrobial activities and structures of two linear cationic peptide families with various amphipathic β-sheet a Antimicrob. Agents Chemother. 49 12 2005 4957 4964 (Pubitemid 41778906)
16. K. Hilpert, M.R. Elliott, R. Volkmer-Engert, P. Henklein, O. Donini, Q. Zhou, D.F.H. Winkler, and R.E.W. Hancock Sequence requirements and an optimization strategy for short antimicrobial peptides Chem. Biol. 13 10 2006 1101 1107 (Pubitemid 44557074)
17. J. Rausch, J. Marks, R. Rathinakumar, and W. Wimley Beta-sheet pore-forming peptides selected from a rational combinatorial library: mechanism of pore formation in lipid vesicles and activity in biological membranes Biochemistry 46 43 2007 12124 12139 (Pubitemid 350022368)
18. B.P. Mowery, S.E. Lee, D.A. Kissounko, R.F. Epand, R.M. Epand, B. Weisblum, S.S. Stahl, and S.H. Gellman Mimicry of antimicrobial host-defense peptides by random copolymers J. Am. Chem. Soc. 129 50 2007 15474 15476
19. B. Findlay, G.G. Zhanel, and F. Schweizer Cationic amphiphiles, a new generation of antimicrobials inspired by the natural antimicrobial peptide scaffold Antimicrob. Agents Chemother. 54 10 2010 4049 4058
20. 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 3 2005 241 256 (Pubitemid 40488604)
21. J.M. Henderson, and K.Y.C. Lee Promising antimicrobial agents designed from natural peptide templates Curr. Opin. Solid State Mater. Sci. 17 2013 175 192
22. R.M. Epand Lipid polymorphism and protein-lipid interactions Biochim. Biophys. Acta 1376 3 1998 353 368 (Pubitemid 28517885)
23. D.W. Hoskin, and A. Ramamoorthy Studies on anticancer activities of antimicrobial peptides Biochim. Biophys. Acta 1778 2 2009 357 375
24. S. Riedl, B. Rinner, M. Asslaber, H. Schaider, S. Walzer, A. Novak, K. Lohner, and D. Zweytick In search of a novel target - phosphatidylserine exposed by non-apoptotic tumor cells and metastases of malignancies with poor treatment efficacy Biochim. Biophys. Acta 1808 11 2011 2638 2645
25. K. Splith, and I. Neundorf Antimicrobial peptides with cell-penetrating peptide properties and vice versa Eur. Biophys. J. 40 4 2011 387 397
26. S.T. Henriques, M.N. Melo, and M.A.R.B. Castanho Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 399 1 Oct. 2006 1 7 (Pubitemid 44505401)
27. M. Fernández-Vidal, S. Jayasinghe, A.S. Ladokhin, and S.H. White Folding amphipathic helices into membranes: amphiphilicity trumps hydrophobicity J. Mol. Biol. 370 3 2008 459 470 (Pubitemid 46898437)
28. P.F. Almeida, A.S. Ladokhin, and S.H. White Hydrogen-bond energetics drive helix formation in membrane interfaces Biochim. Biophys. Acta 1818 2 2012 178 182
29. W.C. Wimley, K. Hristova, A.S. Ladokhin, L. Silvestro, P.H. Axelsen, and S.H. White Folding of beta-sheet membrane proteins: a hydrophobic hexapeptide model J. Mol. Biol. 277 5 1998 1091 1110 (Pubitemid 28190849)
30. E.F. Haney, L.T. Nguyen, D.J. Schibli, and H.J. Vogel Design of a novel tryptophan-rich membrane-active antimicrobial peptide from the membrane-proximal region of the HIV glycoprotein, gp41 Beilstein J. Org. Chem. 8 2012 1172 1184
31. D.J. Schibli, L.T. Nguyen, S.D. Kernaghan, ∅. Rekdal, and H.J. Vogel Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures Biophys. J. 91 12 2006 4413 4426 (Pubitemid 44904228)
32. D.I. Chan, E.J. Prenner, and H.J. Vogel Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action Biochim. Biophys. Acta 1758 9 2006 1184 1202 (Pubitemid 44444830)
33. H.J. Vogel, D.J. Schibli, W. Jing, E.M. Lohmeier-Vogel, R.F. Epand, and R.M. Epand Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides Biochem. Cell Biol. 80 2002 49 63 (Pubitemid 34194228)
34. T. Ryge, X. Doisy, D. Ifrah, J.E. Olsen, and P.R. Hansen New indolicidin analogues with potent antibacterial activity J. Pept. Res. 64 2004 171 185 (Pubitemid 39446659)
35. A. Killian, and G. von Heijne How proteins adapt to a membrane-water interface Trends Biochem. Sci. 25 9 2000 429 434 (Pubitemid 30662410)
36. I. Schiopu, L. Mereuta, A. Apetrei, Y. Park, K.-S. Hahm, and T. Luchian The role of tryptophan spatial arrangement for antimicrobial-derived, membrane-active peptides adsorption and activity Mol. BioSyst. 8 11 2012 2860
37. K. Matsuzaki, O. Murase, N. Fujii, and K. Miyajima An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation Biochemistry 35 35 1996 11361 11368 (Pubitemid 26299310)
38. H.W. Huang Molecular mechanism of antimicrobial peptides: the origin of cooperativity Biochim. Biophys. Acta 1758 9 2006 1292 1302 (Pubitemid 44436067)
39. Y. Shai Mode of action of membrane active antimicrobial peptides Biopolymers 66 4 2002 236 248 (Pubitemid 36098316)
40. E. Sevcsik, G. Pabst, W. Richter, S. Danner, H. Amenitsch, and K. Lohner Interaction of LL-37 with model membrane systems of different complexity: influence of the lipid matrix Biophys. J. 94 12 2008 4688 4699
41. E. Sevcsik, G. Pabst, A. Jilek, and K. Lohner How lipids influence the mode of action of membrane-active peptides Biochim. Biophys. Acta 1768 10 2007 2586 2595 (Pubitemid 47532036)
42. A. Ben Shaul Molecular theory of chain packing, elasticity and lipid-protein interaction in lipid bilayers Handbook of Biological Physics Vol. 1 1995 Elsevier Amsterdam 359 401
43. D. Marsh Lateral pressure profile, spontaneous curvature frustration, and the incorporation and conformation of proteins in membranes Biophys. J. 93 11 2007 3884 3899 (Pubitemid 350223806)
44. G. Pabst Advances in Planar Lipid Bilayers and Liposomes 1st ed. vol. 18 2013 Elsevier Inc. 81 109
45. W. Helfrich Amphiphilic mesophases made of defects Physics of Defects 1981 North-Holland Publishing Amsterdam 716 755
46. D. Marsh Elastic constants of polymer-grafted lipid membranes Biophys. J. 81 4 2001 2154 2162 (Pubitemid 32917164)
47. S.M. Gruner Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids Proc. Natl. Acad. Sci. U. S. A. 82 11 1985 3665 3669
48. D. Marsh Intrinsic curvature in normal and inverted lipid structures and in membranes Biophys. J. 70 5 1996 2248 2255 (Pubitemid 26133717)
49. B. Kollmitzer, P. Heftberger, M. Rappolt, and G. Pabst Monolayer spontaneous curvature of raft-forming membrane lipids Soft Matter 9 45 2013 10877
50. W. Helfrich Elastic properties of lipid bilayers: theory and possible experiments Z. Naturforsch. C. 28 1973 693 703
51. G. Shearman, O. Ces, R. Templer, and J. Seddon Inverse lyotropic phases of lipids and membrane curvature J. Phys. Condens. Matter 18 28 2006 S1105 S1124
52. J. Zimmerberg, and M.M. Kozlov How proteins produce cellular membrane curvature Nat. Rev. Mol. Cell Biol. 7 1 2006 9 19 (Pubitemid 43361568)
53. J.M. Seddon, and R.H. Templer Structure and Dynamics of Membranes 1995 North-Holland Amsterdam 97 160
54. E.F. Haney, S. Nathoo, H.J. Vogel, and E.J. Prenner Induction of non-lamellar lipid phases by antimicrobial peptides: a potential link to mode of action Chem. Phys. Lipids 163 1 2010 82 93
55. J.A. Op den Kamp Lipid asymmetry in membranes Annu. Rev. Biochem. 48 1979 47 71
56. 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
57. J. Israelachvili, S. Marcelja, and R. Horn Physical principles of membrane organization Biophysics 13 1980 121 200
58. K. Lohner The role of membrane lipid composition in cell targeting of antimicrobial peptides Development of Novel Antimicrobial Agents: Emerging Strategies 2001 Horizon Scientific Press Wymondham, Norfolk 149 165
59. S. Morein, A.S. Anderson, L. Rilfors, and G. Lindblom Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures J. Biol. Chem. 271 12 1996 6801 6809
60. L. Rilfors, A. Wieslander, and G. Lindblom Regulation and physicochemical properties of the polar lipids in Acholeplasma laidlawii Subcell. Biochem. 20 1993 109 166
61. R.N. McElhaney Mycoplasmas: Molecular Biology and Pathogenesis 1992 American Society of Microbiology Washington DC 113 155
62. B. de Kruijff Biomembranes. Lipids beyond the bilayer Nature 386 6621 1997 129 130
63. E. Mileykovskaya, and W. Dowhan Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange J. Bacteriol. 182 2000 1172 1175 (Pubitemid 30075045)
64. S. Vanounou, A.H. Parola, and I. Fishov Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids Mol. Microbiol. 49 4 2003 1067 1079 (Pubitemid 36981350)
65. E. Staudegger, E.J. Prenner, M. Kriechbaum, G. Degovics, R.N. Lewis, R.N. McElhaney, and K. Lohner X-ray studies on the interaction of the antimicrobial peptide gramicidin S with microbial lipid extracts: evidence for cubic phase formation Biochim. Biophys. Acta 1468 1-2 2000 213 230
66. A. Roux, D. Cuvelier, P. Nassoy, J. Prost, P. Bassereau, and B. Goud Role of curvature and phase transition in lipid sorting and fission of membrane tubules EMBO J. 24 8 2005 1537 1545 (Pubitemid 40646444)
67. P.F. Devaux, A. Herrmann, N. Ohlwein, and M.M. Kozlov How lipid flippases can modulate membrane structure Biochim. Biophys. Acta 1778 7-8 2008 1591 1600
68. A. Ivankin, B. Apellániz, D. Gidalevitz, and J.L. Nieva Mechanism of membrane perturbation by the HIV-1 gp41 membrane-proximal external region and its modulation by cholesterol Biochim. Biophys. Acta 1818 11 2012 2521 2528
69. P. Laggner, and K. Lohner Lipid Bilayers. Structure and Interactions 2000 Springer Berlin, Heiderlberg, New York 233 259
70. K. Lohner, and E.J. Prenner Differential scanning calorimetry and X-ray diffraction studies of the specificity of the interaction of antimicrobial peptides with membrane-mimetic systems Biochim. Biophys. Acta 1462 1999 141 156
71. K. Lohner Is the high propensity of ethanolamine plasmalogens to form non-lamellar lipid structures manifested in the properties of biomembranes? Chem. Phys. Lipids 81 2 1996 167 184 (Pubitemid 26297539)
72. K. Matsuzaki, K. Sugishita, N. Ishibe, M. Ueha, S. Nakata, K. Miyajima, and R.M. Epand Relationship of membrane curvature to the formation of pores by magainin 2 Biochemistry 37 34 1998 11856 11863 (Pubitemid 28400057)
73. N.W. Schmidt, M. Lis, K. Zhao, G.H. Lai, A.N. Alexandrova, G.N. Tew, and G.C.L. Wong Molecular basis for nanoscopic membrane curvature generation from quantum mechanical models and synthetic transporter sequences J. Am. Chem. Soc. 134 46 2012 19207 19216
74. A.A. Polyansky, P.E. Volynsky, A.S. Arseniev, and R.G. Efremov Adaptation of a membrane-active peptide to heterogeneous environment. I. Structural plasticity of the peptide J. Phys. Chem. B 113 4 2009 1107 1119
75. N.W. Schmidt, K.P. Tai, K. Kamdar, A. Mishra, G.H. Lai, K. Zhao, A.J. Ouellette, and G.C.L. Wong Arginine in α-defensins: differential effects on bactericidal activity correspond to geometry of membrane curvature generation and peptide-lipid phase behavior J. Biol. Chem. 287 26 2012 21866 21872
76. M. Rappolt, A. Hickel, F. Bringezu, and K. Lohner Mechanism of the lamellar/inverse hexagonal phase transition examined by high resolution X-ray diffraction Biophys. J. 84 5 2003 3111 3122 (Pubitemid 36531759)
77. J. Erbes, C. Czeslik, W. Hahn, R. Winter, M. Rappolt, and G. Rapp On the existence of bicontinuous cubic phases in dioleoylphosphatidylethanolamine Ber. Bunsenges. Phys. Chem. 98 1994 8776 8779
78. J.M. Seddon, J. Robins, T. Gulik-Krzywicki, and H. Delacroix Inverse micellar phases of phospholipids and glycolipids Phys. Chem. Chem. Phys. 2 2000 4485 4493
79. P.T.C. So, S.M. Gruner, and S. Erramilli Pressure-induced topological phase transition in membranes Phys. Rev. Lett. 70 1993 3455 3458
80. S. Buchoux, J. Lai-Kee-Him, M. Garnier, P. Tsan, F. Besson, A. Brisson, and E.J. Dufourc Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism Biophys. J. 95 8 2008 3840 3849
81. R.S. Cantor Lateral pressures in cell membranes: a mechanism for modulation of protein function J. Phys. Chem. B 101 10 1997 1723 1725 (Pubitemid 127578327)
82. R.S. Cantor The influence of membrane lateral pressures on simple geometric models of protein conformational equilibria Chem. Phys. Lipids 101 1 1999 45 56 (Pubitemid 29385550)
83. R.S. Cantor Lipid composition and the lateral pressure profile in bilayers Biophys. J. 76 5 May 1999 2625 2639 (Pubitemid 29264622)
84. T. Doherty, A.J. Waring, and M. Hong Peptide-lipid interactions of the beta-hairpin antimicrobial peptide tachyplesin and its linear derivatives from solid-state NMR Biochim. Biophys. Acta 1758 9 2006 1285 1291 (Pubitemid 44462775)
85. 2 + Biophys. J. 85 4 2003 2363 2373 (Pubitemid 37210786)
86. J.J. Buffy, A.J. Waring, R.I. Lehrer, and M. Hong Immobilization and aggregation of the antimicrobial peptide protegrin-1 in lipid bilayers investigated by solid-state NMR Biochemistry 42 46 2003 13725 13734 (Pubitemid 37444922)
87. A. Laederach, A.H. Andreotti, and D.B. Fulton Solution and micelle-bound structures of tachyplesin I and its active aromatic linear derivates Biochemistry 41 2002 12359 12368
88. R. El Jastimi, and M. Lafleur Nisin promotes the formation of non-lamellar inverted phases in unsaturated phosphatidylethanolamines Biochim. Biophys. Acta 1418 1 1999 97 105 (Pubitemid 29182749)
89. H.M. Chen, K.W. Leung, N.N. Thakur, A. Tan, and R.W. Jack Distinguishing between different pathways of bilayer disruption by the related antimicrobial peptides cecropin B, B1 and B3 Eur. J. Biochem. 270 5 2003 911 920 (Pubitemid 36315334)
90. R.F. Epand, N. Umezawa, E.A. Porter, S.H. Gellman, and R.M. Epand Interactions of the antimicrobial beta-peptide beta-17 with phospholipid vesicles differ from membrane interactions of magainins Eur. J. Biochem. 270 6 2003 1240 1248 (Pubitemid 36384456)
91. J.C. Bozelli, E.T. Sasahara, M.R.S. Pinto, C.R. Nakaie, and S. Schreier Effect of head group and curvature on binding of the antimicrobial peptide tritrpticin to lipid membranes Chem. Phys. Lipids 165 4 2012 365 373
92. G. Cevc Rational design of new product candidates: The next generation of highly deformable bilayer vesicles for noninvasive, targeted therapy J. Controlled Release 160 2012 135 146
93. 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 6 2013 L9 L11
94. M.-A. Sani, T.C. Whitwell, and F. Separovic Lipid composition regulates the conformation and insertion of the antimicrobial peptide maculatin 1.1 Biochim. Biophys. Acta 1818 2 2012 205 211
95. S.R. Tabaei, M. Rabe, V.P. Zhdanov, N.-J. Cho, and F. Höök Single vesicle analysis reveals nanoscale membrane curvature selective pore formation in lipid membranes by an antiviral α-helical peptide Nano Lett. 12 11 2012 5719 5725
96. T. Wang, S.D. Cady, and M. Hong NMR determination of protein partitioning into membrane domains with different curvatures and application to the influenza M2 peptide Biophys. J. 102 4 2012 787 794
97. K. Iwamoto, T. Hayakawa, M. Murate, A. Makino, K. Ito, T. Fujisawa, and T. Kobayashi Curvature-dependent recognition of ethanolamine phospholipids by duramycin and cinnamycin Biophys. J. 93 5 2007 1608 1619 (Pubitemid 47403302)
98. C. Galanth, F. Abbassi, O. Lequin, J. Ayala-Sanmartin, A. Ladram, P. Nicolas, and M. Amiche Mechanism of antibacterial action of dermaseptin B2: interplay between helix-hinge-helix structure and membrane curvature strain Biochemistry 48 2 2009 313 327
99. H. Hong, and L.K. Tamm Elastic coupling of integral membrane protein stability to lipid bilayer forces Proc. Natl. Acad. Sci. U. S. A. 101 12 2004 4065 4070 (Pubitemid 38405884)
100. D. Marsh, B. Shanmugavadivu, and J.H. Kleinschmidt Membrane elastic fluctuations and the insertion and tilt of beta-barrel proteins Biophys. J. 91 1 2006 227 232 (Pubitemid 44015322)
101. G.E. Schulz The structure of bacterial outer membrane proteins Biochim. Biophys. Acta 1565 2 2002 308 317 (Pubitemid 35284483)
102. J.R. Lewis, and D.S. Cafiso Correlation between the free energy of a channel-forming voltage-gated peptide and the spontaneous curvature of bilayer lipids Biochemistry 38 18 1999 5932 5938
103. K. He, S.J. Ludtke, W.T. Heller, and H.W. Huang Mechanism of alamethicin insertion into lipid bilayers Biophys. J. 71 5 1996 2669 2679 (Pubitemid 26367729)
104. R.S. Cantor Size distribution of barrel-stave aggregates of membrane peptides: influence of the bilayer lateral pressure profile Biophys. J. 82 5 2002 2520 2525 (Pubitemid 34441291)
105. D. Marsh, M. Jost, C. Peggion, and C. Toniolo Lipid chain-length dependence for incorporation of alamethicin in membranes: electron paramagnetic resonance studies on TOAC-spin labeled analogs Biophys. J. 92 11 2007 4002 4011 (Pubitemid 46910586)
106. G.S. Attard, R.H. Templer, W.S. Smith, A.N. Hunt, and S. Jackowski Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress Proc. Natl. Acad. Sci. U. S. A. 97 16 2000 9032 9036 (Pubitemid 30626668)
107. S.M. Davies, R.M. Epand, R. Kraayenhof, and R.B. Cornell Regulation of CTP: phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: an important role for stored curvature strain energy Biochemistry 40 35 2001 10522 10531 (Pubitemid 32816663)
108. 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 8 2009 1667 1679
109. P. Tremouilhac, E. Strandberg, P. Wadhwani, and A.S. Ulrich Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin J. Biol. Chem. 281 43 2006 32089 32094 (Pubitemid 46036763)
110. B. Bechinger, M. Zasloff, and S.J. Opella Structure and dynamics of the antibiotic peptide PGLa in membranes by solution and solid-state nuclear magnetic resonance spectroscopy Biophys. J. 74 2 Pt 1 1998 981 987 (Pubitemid 28345291)
111. E.S. Salnikov, and B. Bechinger Lipid-controlled peptide topology and interactions in bilayers: structural insights into the synergistic enhancement of the antimicrobial activities of PGLa and magainin 2 Biophys. J. 100 6 2011 1473 1480
112. B. Bechinger, L.M. Gierasch, M. Montal, M. Zasloff, and S.J. Opella Orientations of helical peptides in membrane bilayers by solid state NMR spectroscopy Solid State Nucl. Magn. Reson. 7 3 1996 185 191 (Pubitemid 126412370)
113. D. Marsh Pivotal surfaces in inverse hexagonal and cubic phases of phospholipids and glycolipids Chem. Phys. Lipids 164 3 2011 177 183
114. R. Koynova, and M. Caffrey Phases and phase transitions of the phosphatidylcholines Biochim. Biophys. Acta 1376 1 1998 91 145 (Pubitemid 28321526)
115. M.M. Sperotto, and O.G. Mouritsen Monte Carlo simulation studies of lipid order parameter profiles near integral membrane proteins Biophys. J. 59 2 1991 261 270
116. M. de Planque, and J. Killian Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring Mol. Membr. Biol. 20 4 2003 271 284 (Pubitemid 37406619)
117. R. Rand, N. Fuller, S. Gruner, and V. Parsegian Membrane curvature, lipid segregation, and structural transitions for phospholipids under dual-solvent stress Biochemistry 29 1 1990 76 87 (Pubitemid 20033709)
118. M.K. Dymond, and G.S. Attard Cationic type I amphiphiles as modulators of membrane curvature elastic stress in vivo Langmuir 24 20 2008 11743 11751
119. M. Bogdanov, and W. Dowhan Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli J. Biol. Chem. 270 2 1995 732 739
120. A.G. Rietveld, M.C. Koorengevel, and B. de Kruijff Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli EMBO J. 14 22 1995 5506 5513
121. D. Zweytick, B. Japelj, E. Mileykovskaya, M. Zorko, W. Dowhan, S. Blondelle, S. Riedl, R. Jerala, and K. Lohner N-acylated peptides derived from human lactoferricin perturb organization of cardiolipin and phosphatidylethanolamine in cell membranes and induce defects in Escherichia coli cell division PLoS One 9 3 2014 e90228
122. H. Jerabek, G. Pabst, M. Rappolt, and T. Stockner Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine J. Am. Chem. Soc. 132 23 2010 7990 7997
123. Y.A. Domanov, and P.K.J. Kinnunen Antimicrobial peptides temporins B and L induce formation of tubular lipid protrusions from supported phospholipid bilayers Biophys. J. 91 12 2006 4427 4439 (Pubitemid 44904229)
124. L.C. Salay, M. Ferreira, O.N. Oliveira, C.R. Nakaie, and S. Schreier Headgroup specificity for the interaction of the antimicrobial peptide tritrpticin with phospholipid Langmuir monolayers Colloids Surf. B: Biointerfaces 100 2012 95 102
125. D. Zweytick, S. Tumer, S.E. Blondelle, and K. Lohner Membrane curvature stress and antibacterial activity of lactoferricin derivatives Biochem. Biophys. Res. Commun. 369 2 2008 395 400
126. D. Zweytick, G. Deutsch, J. Andrä, S.E. Blondelle, E. Vollmer, R. Jerala, and K. Lohner Studies on lactoferricin-derived Escherichia coli membrane-active peptides reveal differences in the mechanism of N-acylated versus nonacylated peptides J. Biol. Chem. 286 24 2011 21266 21276
127. P. a B. Marasinghe, J.J. Buffy, K. Schmidt-Rohr, and M. Hong Membrane curvature change induced by an antimicrobial peptide detected by 31P exchange NMR J. Phys. Chem. B 109 46 Nov. 2005 22036 22044 (Pubitemid 41784841)
128. S. Thennarasu, R. Huang, D.-K. Lee, P. Yang, L. Maloy, Z. Chen, and A. Ramamoorthy Limiting an antimicrobial peptide to the lipid-water interface enhances its bacterial membrane selectivity: a case study of MSI-367 Biochemistry 49 50 2010 10595 10605
129. S. Thennarasu, D.-K. Lee, A. Tan, U. Prasad Kari, and A. Ramamoorthy Antimicrobial activity and membrane selective interactions of a synthetic lipopeptide MSI-843 Biochim. Biophys. Acta 1711 1 2005 49 58 (Pubitemid 40726400)
130. A. Ramamoorthy, S. Thennarasu, D.-K. Lee, A. Tan, and L. Maloy Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin Biophys. J. 91 1 2006 206 216 (Pubitemid 44015320)
131. I.D. Alves, N. Goasdoué, I. Correia, S. Aubry, C. Galanth, S. Sagan, S. Lavielle, and G. Chassaing Membrane interaction and perturbation mechanisms induced by two cationic cell penetrating peptides with distinct charge distribution Biochim. Biophys. Acta 1780 7-8 2008 948 959
132. K. Nomura, and G. Corzo The effect of binding of spider-derived antimicrobial peptides, oxyopinins, on lipid membranes Biochim. Biophys. Acta 1758 9 2006 1475 1482 (Pubitemid 44436083)
133. A. Hickel, S. Danner-Pongratz, H. Amenitsch, G. Degovics, M. Rappolt, K. Lohner, and G. Pabst Influence of antimicrobial peptides on the formation of nonlamellar lipid mesophases Biochim. Biophys. Acta 1778 10 2008 2325 2333
134. L. Yang, V.D. Gordon, A. Mishra, A. Som, K.R. Purdy, M.A. Davis, G.N. Tew, and G.C.L. Wong Synthetic antimicrobial oligomers induce a composition-dependent topological transition in membranes J. Am. Chem. Soc. 129 40 2007 12141 12147 (Pubitemid 47556850)
135. O. Domenech, G. Francius, P.M. Tulkens, F. Van Bambeke, Y. Dufrêne, and M.-P. Mingeot-Leclercq Interactions of oritavancin, a new lipoglycopeptide derived from vancomycin, with phospholipid bilayers: effect on membrane permeability and nanoscale lipid membrane organization Biochim. Biophys. Acta 1788 9 2009 1832 1840
136. J.-P.S. Powers, A. Tan, A. Ramamoorthy, and R.E.W. Hancock Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes Biochemistry 44 47 2005 15504 15513 (Pubitemid 41706134)
137. R. Willumeit, M. Kumpugdee, S.S. Funari, K. Lohner, B.P. Navas, K. Brandenburg, S. Linser, and J. Andrä Structural rearrangement of model membranes by the peptide antibiotic NK-2 Biochim. Biophys. Acta 1669 2 2005 125 134 (Pubitemid 40704730)
138. K. Hu, N.W. Schmidt, R. Zhu, Y. Jiang, G.H. Lai, G. Wei, E.F. Palermo, K. Kuroda, G.C.L. Wong, and L. Yang A critical evaluation of random copolymer mimesis of homogeneous antimicrobial peptides Macromolecules 46 5 2013 1908 1915
139. L. Keller, M. Gruner, and K. Gawrisch Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures Biochim. Biophys. Acta 1278 1996 241 246 (Pubitemid 26062579)
140. Y. Wu, K. He, S.J. Ludtke, and H.W. Huang X-ray diffraction study of lipid bilayer membranes interacting with amphiphilic helical peptides: diphytanoyl phosphatidylcholine with alamethicin at low concentrations Biophys. J. 68 6 1995 2361 2369