Recent advances in computational modeling of α-Helical membrane-active peptides

Current Protein and Peptide Science

Volumn 13, Issue 7, 2012, Pages 644-657

  Polyansky, Anton A ^a,b   Chugunov, Anton O ^a   Vassilevski, Alexander A ^a   Grishin, Eugene V ^a   Efremov, Roman G ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b Vienna Biocenter   (Austria)

Author keywords

Antimicrobial peptides; Cell penetrating peptides; Fusion peptides; Molecular dynamics simulations; Molecular hydrophobicity potential; Rational design

Indexed keywords

ALAMETHICIN; ALPHA HELICAL MEMBRANE ACTIVE PEPTIDE; CELL PENETRATING PEPTIDE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; MELITTIN; PENETRATIN; PEPTIDE; UNCLASSIFIED DRUG;

COMPUTER MODEL; DYNAMICS; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; PROTEIN LIPID INTERACTION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; REVIEW; SEQUENCE ANALYSIS; SIMULATION; STATIC ELECTRICITY; THERMODYNAMICS; THREE DIMENSIONAL IMAGING;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE PERMEABILITY; CELL-PENETRATING PEPTIDES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE FUSION; MEMBRANE LIPIDS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84874900581     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312804142147     Document Type: Review

References (136)

1. Baxter, J.D.; Funder, J.W. Hormone receptors. N. Engl. J. Med., 1979, 301, 1149-1161.
2. Vassilevski, A.A.; Kozlov, S.A.; Grishin, E.V. Molecular diversity of spider venom. Biochemistry (Mosc), 2009, 74, 1505-1534.
3. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415, 389-395.
4. Yeaman, M.R.; Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev., 2003, 55, 27-55.
5. Bechinger, B.; Lohner, K. Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim. Biophys. Acta, 2006, 1758, 1529-1539;
6. Mae, M.; Langel, U. Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr. Opin. Pharmacol., 2006, 6, 509-514;
7. Deshayes, S.; Morris, M.C.; Divita, G.; Heitz, F. Cell-penetrating peptides: tools for intracellular delivery of therapeutics. Cell Mol. Life Sci., 2005, 62, 1839-1849.
8. Fischer, R.; Fotin-Mleczek, M.; Hufnagel, H.; Brock, R. Break on through to the other side-biophysics and cell biology shed light on cell-penetrating peptides. Chembiochem, 2005, 6, 2126-2142.
9. Harrison, S.C. Viral membrane fusion. Nat. Struct. Mol. Biol., 2008, 15, 690-698.
10. Tamm, L.K.; Han, X.; Li, Y.; Lai, A.L. Structure and function of membrane fusion peptides. Biopolymers, 2002, 66, 249-260.
11. Martin, I.; Ruysschaert, J.M. Common properties of fusion peptides from diverse systems. Biosci. Rep., 2000, 20, 483-500.
12. McLaughlin, S.; Aderem, A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci., 1995, 20, 272-276.
13. Willey, J.M.; van der Donk, W.A. Lantibiotics: peptides of diverse structure and function. Annu Rev. Microbiol., 2007, 61, 477-501.
14. Henriques, S.T.; Melo, M.N.; Castanho, M.A. Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem J., 2006, 399, 1-7.
15. Raghuraman, H.; Chattopadhyay, A. Melittin: a membrane-active peptide with diverse functions. Biosci Rep., 2007, 27, 189-223.
16. Derossi, D.; Joliot, A.H.; Chassaing, G.; Prochiantz, A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem., 1994, 269, 10444-10450.
17. Wharton, S.A.; Martin, S.R.; Ruigrok, R.W.; Skehel, J.J.; Wiley, D.C. Membrane fusion by peptide analogues of influenza virus haemagglutinin. J. Gen. Virol., 1988, 69, 1847-1857.
18. Boman, H.G. Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med., 2003, 254, 197-215.
19. Brown, K.L.; Hancock, R.E. Cationic host defense (antimicrobial) peptides. Curr. Opin. Immunol., 2006, 18, 24-30.
20. Dathe, M.; Wieprecht, T. Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta, 1999, 1462, 71-87.
21. Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, α-helical antimicrobial peptides. Biopolymers, 2000, 55, 4-30.
22. Sitaram, N.; Nagaraj, R. Host-defense antimicrobial peptides: importance of structure for activity. Curr. Pharm. Des., 2002, 8, 727-742.
23. Eisenberg, D.; Weiss, R.M.; Terwilliger, T.C. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature, 1982, 299, 371-374.
24. Fauchére, J.-L.; Quarendona, P.; Kaetterer, L. Estimating and representing hydrophobicity potential. J. Mol. Graph., 1988, 6, 203-206.
25. Efremov, R.G.; Chugunov, A.O.; Pyrkov, T.V.; Priestle, J.P.; Arseniev, A.S.; Jacoby, E. Molecular lipophilicity in protein modeling and drug design. Curr. Med. Chem., 2007, 14, 393-415.
26. Wiener, M.C.; White, S.H. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys J., 1992, 61, 434-447.
27. Hristova, K.; Dempsey, C.E.; White, S.H. Structure, location, and lipid perturbations of melittin at the membrane interface. Biophys J., 2001, 80, 801-811.
28. Ramamoorthy, A.; Thennarasu, S.; Lee, D.K.; Tan, A.; Maloy, L. 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., 2006, 91, 206-216.
29. Thennarasu, S.; Tan, A.; Penumatchu, R.; Shelburne, C.E.; Heyl, D.L.; Ramamoorthy, A. Antimicrobial and membrane disrupting activities of a peptide derived from the human cathelicidin antimicrobial peptide LL37. Biophys J., 2010, 98, 248-257.
30. Ieronimo, M.; Afonin, S.; Koch, K.; Berditsch M.; Wadhwani, P.; Ulrich, A.S. 19F NMR analysis of the antimicrobial peptide PGLa bound to native cell membranes from bacterial protoplasts and human erythrocytes. J. Am. Chem. Soc., 2010, 132, 8822-8824.
31. Langham, A.; Kaznessis, Y.N. Molecular simulations of antimicrobial peptides. Methods Mol. Biol., 2010, 618, 267-285.
32. Matyus, E.; Kandt, C.; Tieleman D.P. Computer simulation of antimicrobial peptides. Curr. Med. Chem., 2007, 14, 2789-2798.
33. Gordon-Grossman, M.; Gofman, Y.; Zimmermann, H.; Frydman, V.; Shai, Y; Ben-Tal, N.; Goldfarb, D. A combined pulse EPR and Monte Carlo simulation study provides molecular insight on peptide-membrane interactions. J. Phys. Chem. B, 2009, 113, 12687-12695.
34. Shental-Bechor, D.; Haliloglu, T.; Ben-Tal, N. Interactions of cationic-hydrophobic peptides with lipid bilayers: a Monte Carlo simulation method. Biophys. J., 2007, 93, 1858-1871.
35. Ludtke, S.J.; He, K.; Heller, W.T.; Harroun, T.A.; Yang, L.; Huang, H.W. Membrane pores induced by magainin. Biochemistry, 1996, 35, 13723-13728.
36. Yang, L.; Harroun, T.A.; Weiss, T.M.; Ding, L.; Huang, H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J., 2001, 81, 1475-1485.
37. Henzler Wildman, K.A.; Lee, D.K.; Ramamoorthy, A. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry, 2003, 42, 6545-6558.
38. Sobko, A.A.; Kotova, E.A.; Antonenko, Y.N.; Zakharov, S.D.; Cramer, W.A. Lipid dependence of the channel properties of a colicin E1-lipid toroidal pore. J. Biol. Chem., 2006, 281, 14408-14416.
39. Murzyn, K.; Pasenkiewicz-Gierula, M. Construction of a toroidal model for the magainin pore. J. Mol. Model., 2003, 9, 217-224.
40. Frink, L.J.; Frischknecht, A.L. Computational investigations of pore forming peptide assemblies in lipid bilayers. Phys. Rev. Lett., 2006, 97, 208701.
41. Rzepiela, A.J.; Sengupta, D.; Goga, N.; Marrink, S.J. Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions. Faraday Discuss., 2010, 144, 431-443.
42. Wimley, W.C.; Hristova, K. Antimicrobial peptides: successes, challenges and unanswered questions. J. Membr. Biol., 2011, 239, 27-34.
43. Mihajlovic, M.; Lazaridis, T. Antimicrobial peptides in toroidal and cylindrical pores. Biochim. Biophys. Acta, 2010, 1798, 1485-1493.
44. La Rocca, P.; Biggin, P.C.; Tieleman, D.P.; Sansom, M.S.P. Simulation studies of the interaction of antimicrobial peptides and lipid bilayers. Biochim. Biophys. Acta, 1999, 1462, 185-200.
45. Ash, W.L.; Zlomislic, M.R.; Oloo, E.O.; Tieleman, D.P. Computer simulations of membrane proteins. Biochim. Biophys. Acta, 2004, 1666, 158-189.
46. Shepherd, C.M.; Vogel, H.J.; Tieleman, D.P. Interactions of the designed antimicrobial peptide MB21 and truncated dermaseptin S3 with lipid bilayers: molecular-dynamics simulations. Biochem. J., 2003, 370, 233-243.
47. Huang, Q.; Chen, Ch.-L.; Herrmann A. Bilayer conformation of fusion peptide of influenza virus hamgglutinin: a molecular dynamics study. Biophys. J., 2004, 87, 14-22.
48. Kandasamy, S.K.; Larson, R.G. Binding and insertion of α-helical anti-microbial peptides in POPC bilayers studied by molecular dynamics simulations. Chem. Phys. Lipids, 2004, 132, 113-132.
49. Khandelia, H.; Kaznessis Y.N. Molecular dynamics simulations of helical antimicrobial peptides in SDS micelles: what do point mutations achieve? Peptides, 2005, 26, 2037-2049.
50. Khandelia, H.; Kaznessis, Y.N. Molecular dynamics simulations of the helical antimicrobial peptideovispirin-1 in a zwitterionic dodecylphosphocholine micelle: insights into host-cell toxicity. J. Phys. Chem. B, 2005, 109, 12990-2996.
51. Vaccaro, L.; Cross, K.J.; Kleinjung, J.; Straus, S.K.; Thomas, D.J.; Wharton, S.A.; Skehel, J.J.; Fraternali, F. Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers. Biophys. J., 2005, 88, 25-36.
52. Polyansky, A.A.; Ramaswamy, R.; Volynsky, P.E.; Sbalzarini, I.F.; Marrink, S.J.; Efremov, R.G. Antimicrobial peptides induce growth of phosphatidylglycerol domains in a model bacterial membrane. J. Phys. Chem. Lett., 2010, 1, 3108-3111.
53. Leontiadou, H.; Mark, A.E.; Marrink, S.J. Antimicrobial peptides in action. J. Am. Chem. Soc., 2006, 128, 12156-12161.
54. Thøgersen, L; Schiøtt, B; Vosegaard, T; Nielsen, N.C.; Tajkhorshid E. Peptide aggregation and pore formation in a lipid bilayer: a combined coarse-grained and all atom molecular dynamics study. Biophys. J., 2008, 95, 4337-4347.
55. Langham, A.; Kaznessis, Y.N. Molecular simulations of antimicrobial peptides. Methods Mol. Biol., 2010, 618, 267-285.
56. Soliman, W.; Bhattacharjee, S.; Kaur, K. Adsorption of an antimicrobial peptide on self-assembled monolayers by molecular dynamics simulation. J. Phys. Chem. B, 2010, 114, 11292-11302.
57. Dorosz, J.; Gofman, Y.; Kolusheva, S.; Otzen, D.; Ben-Tal, N.; Nielsen, N.C.; Jelinek, R. Membrane interactions of novicidin, a novel antimicrobial peptide: phosphatidylglycerol promotes bilayer insertion. J. Phys. Chem. B, 2010, 14, 11053-11060.
58. Soliman, W.; Bhattacharjee, S.; Kaur, K. Interaction of an antimicrobial peptide with a model lipid bilayer using molecular dynamics simulation. Langmuir, 2009, 25, 6591-6595.
59. Volynsky, P.E.; Polyansky, A.A.; Simakov, N.A.; Arseniev, A.S.; Efremov, R.G. Effect of lipid composition on the "membrane response" induced by a fusion peptide. Biochemistry, 2005, 44, 14626-14637.
60. Nikolaus, J.; Scolari, S.; Bayraktarov, E.; Jungnick, N.; Engel, S.; PiaPlazzo, A.; Stöckl, M.; Volkmer, R.; Veit, M.; Herrmann, A. Hemagglutinin of influenza virus partitions into the nonraft domain of model membranes. Biophys J., 2010, 99, 489-498.
61. Polyansky, A.A.; Volynsky, P.E.; Efremov R.G. Computer simulations of membrane-lytic peptides: perspectives in drug design. J. Bioinform. Comput. Biol., 2007, 5, 611-626.
62. Xu, G., Wu, M., Wang, L., Zhang, X., Cao, S., Liu, M., Cui, Y. Conformational and dynamics simulation study of antimicrobial peptide hedistin-heterogeneity of its helix-turn-helix motif. Biochim Biophys Acta, 2009, 1788, 2497-2508.
63. Chen, R.; Mark, A. E. The effect of membrane curvature on the conformation of antimicrobial peptides: implications for binding and the mechanism of action. Eur. Biophys. J., 2011, 40, 545-553.
64. Polyansky, A.A.; Volynsky, P.E.; Arseniev, A.S.; Efremov, R.G. Adaptation of a membrane active peptide to heterogeneous environment. I. Structural plasticity of the peptide. J. Phys. Chem. B, 2009, 113, 1107-1119.
65. Fleming, E.; Maharaj, N.P.; Chen, J.L.; Nelson, R.B.; Elmore, D.E. Effect of lipid composition on buforin II structure and membrane entry. Proteins, 2008, 73, 480-491.
66. Pimthon, J.; Willumeit, R.; Lendlein, A.; Hofmann D. Membrane association and selectivity of the antimicrobial peptide NK-2: a molecular dynamics simulation study. J. Pept. Sci., 2009, 15, 654-667.
67. Sengupta, D.; Leontiadou, H.; Mark, A.E.; Marrink, S.J. Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim. Biophys. Acta, 2008, 1778, 2308-2317.
68. Herce, H.D.; Garcia, A.E. Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc. Natl. Acad. Sci. U.S.A., 2007, 104, 20805-290810.
69. Yesylevskyy, S.; Marrink, S.J.; Mark, A.E. Alternative mechanisms for the interaction of the cell-penetrating peptides penetratin and the TAT peptide with lipid bilayers. Biophys J., 2009, 97, 40-49.
70. Marrink, S.J.; de Vries, A.H.; Tieleman, D.P. Lipids on the move: simulations of membrane pores, domains, stalks and curves. Biochim. Biophys. Acta, 2009, 1788, 149-168.
71. Illya, G.; Deserno, M. Coarse-grained simulation studies of peptide-induced pore formation. Biophys J., 2008, 95, 4163-4173.
72. Marrink, S.J.; Risselada, H.J.; Yefimov, S.; Tieleman, D.P.; de Vries, A.H. The MARTINI ForceField: coarse grained model for biomolecular simulations. J. Phys. Chem. B, 2007, 111, 7812-7824.
73. Monticelli, L.; Kandasamy, S.K.; Periole, X., Larson, R.G.; Tieleman, D.P.; Marrink, S.J. The MARTINI coarse-grained force field: extension to proteins. J. Chem. Theory Comput., 2008, 4, 819-834.
74. Bond, P.J.; Parton, D.L.; Clark, J.F.; Sansom, M.S. Coarse-grained simulations of the membrane-active antimicrobial peptide maculatin 1.1. Biophys. J., 2008, 95, 3802-3815.
75. Epand, R.F.; Maloy, W.L.; Ramamoorthy, A.; Epand, R.M. Probing the "charge cluster mechanism" in amphipathic helical cationic antimicrobial peptides. Biochemistry, 2010, 49, 4076-4084.
76. Pag, U.; Oedenkoven, M.; Sass, V.; Shai, Y.; Shamova, O.; Antcheva, N.; Tossi, A.; Sahl, H. G.Analysis of In vitro activities and modes of action of synthetic antimicrobial peptides derived from an alpha-helical "sequence template". J. Antimicrob. Chemother., 2008, 61, 341-352.
77. Fuhrmans, M.; Knecht, V.; Marrink, S.J. A single bicontinuous cubic phase induced by fusion peptides. J. Am. Chem. Soc., 2009, 131, 9166-9167.
78. Zemel, A.; Fattal, D. R.; Ben-Shaul, A. Energetics and selfassembly of amphipathic peptide pores in lipid membranes. Biophys. J., 2003, 84, 2242-2255.
79. Zemel, A.; Ben-Shaul, A.; May, S. Perturbation of a lipid membrane by amphipathic peptides and its role in pore formation. Eur. Biophys. J., 2005, 34, 230-242.
80. Vivcharuk, V.; Kaznessis, Y. Free energy profile of the interaction between a monomer or a dimer of protegrin-1 in a specific binding orientation and a model lipid bilayer. J. Phys. Chem. B, 2010, 114, 2790-2797.
81. Rui, H.; Im, W. Protegrin-1 orientation and physicochemical properties in membrane bilayers studied by potential of mean force calculations. J. Comp. Chem., 2010, 31, 2859-2867.
82. Tolokh, I.; Vivcharuk, V.; Tomberli, B.; Gray, C. Binding free energy and counterion release for adsorption of the antimicrobial peptide lactoferricin B on a POPG membrane. Phys. Rev. E, 2009, 80, 1-12.
83. Vivcharuk, V.; Tolokh, I. S.; Gray, C. G. Prediction of binding free energy for adsorption of antimicrobial peptide lactoferricin B on a POPC membrane. Phys. Rev. E, 2008, 77, 1-11.
84. Aliste, M.P.; MacCallum, J.L.; Tieleman, D.P. Molecular dynamics simulations of pentapeptides at interfaces: salt bridge and cation-pi interactions. Biochemistry, 2003, 42, 8976-8987.
85. Lensink, M. F.; Christiaens, B.; Vandekerckhove, J.; Prochiantz, A; Rosseneu, M. Penetratin-membrane association: W48/R52/W56 shield the peptide from the aqueous phase. Biophys. J. 2005, 88, 939-952.
86. Wang, Q.; Hong, G.; Johnson, G.R.; Pachter, R.; Cheung, M.S. Biophysical properties of membrane-active peptides based on micelle modeling: a case study of cell-penetrating and antimicrobial peptides. J. Phys. Chem. B. 2010, 114, 13726-13735.
87. Palm-Apergi, C.; Lorents, A.; Padari, K.; Pooga, M.; Hällbrink, M. The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake. FASEB J., 2009, 23, 214-223.
88. Babakhani, A.; Gorfe, A.A.; Kim, J.E.; McCammon, J.A. Thermodynamics of peptide insertion and aggregation in a lipid bilayer. J. Phys. Chem. B, 2008, 112, 10528-10534.
89. Dennison, S.R.; Wallace, J.; Harris, F.; Phoenix, D.A. Amphiphilic α-helical antimicrobial peptides and their structure/function relationships. Protein Pept. Lett., 2005, 12, 31-39.
90. White, S.H.; Wimley, W.C. Membrane protein folding and stability: physical principles. Annu Rev. Biophys. Biomol. Struct., 1999, 28, 319-365.
91. Cornette, J.L.; Cease, K.B.; Margalit, H.; Spouge, J.L.; Berzofsky, J.A.; DeLisi, C. Hydrophobicity scales and computational techniques for detecting amphipathic structures in proteins. J. Mol. Biol., 1987, 195, 659-685.
92. Schiffer, M. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys. J, 1967, 7, 121-135.
93. Segrest, J.P.; De Loof, H.; Dohlman, J.G.; Brouillette, C.G.; Anantharamaiah, G.M. Amphipathic helix motif: classes and properties. Proteins, 1990, 8, 103-117.
94. Wallace, J.; Daman, O.A.; Harris, F.; Phoenix, D.A. Investigation of hydrophobic moment and hydrophobicity properties for transmembrane α-helices. Theor. Biol. Med. Model., 2004, 1, 5.
95. Finer-Moore, J.; Stroud, R.M. Amphipathic analysis and possible formation of the ion channel in an acetylcholine receptor. Proc. Natl. Acad. Sci. U.S.A., 1984, 81, 155-159.
96. Donnelly, D.; Overington, J.P.; Ruffle, S.V.; Nugent, J.H.; Blundell, T.L. Modeling α-helical transmembrane domains: the calculation and use of substitution tables for lipid-facing residues. Protein Sci, 1993, 2, 55-70.
97. Ghose, A.K.; Viswanadhan, V.N.; Wendoloski, J.J. Prediction of hydrophobic (lipophilic) properties of small organic molecules using fragmental methods: an analysis of ALOGP and CLOGP methods. J. Phys. Chem. A, 1998, 102, 3762-3772.
98. Dubovskii, P.V.; Volynsky, P.E.; Polyansky, A.A.; Chupin, V.V.; Efremov, R.G.; Arseniev, A.S. Spatial structure and activity mechanism of a novel spider antimicrobial peptide. Biochemistry, 2006, 45, 10759-10767.
99. Dubovskii, P.V.; Volynsky, P.E.; Polyansky, A.A.; Karpunin, D.V.; Chupin, V.V.; Efremov, R.G.; Arseniev, A.S. Threedimensional structure/hydrophobicity of latarcins specifies their mode of membrane activity. Biochemistry, 2008, 47, 3525-3533.
100. Brasseur, R.; Pillot, T.; Lins, L.; Vandekerckhove, J.; Rosseneu, M. Peptides in membranes: tipping the balance of membrane stability. Trends Biochem. Sci., 1997, 22, 167-171.
101. Efremov, R.G.; Nolde, D.E.; Volynsky, P.E.; Chernyavsky, A.A.; Dubovskii, P.V.; Arseniev, A.S. Factors important for fusogenic activity of peptides: molecular modeling study of analogs of fusion peptide of influenza virus hemagglutinin. FEBS letters, 1999, 462, 205-210.
102. Lins, L.; Brasseur, R. Tilted peptides: a structural motif involved in protein membrane insertion? J. Pept. Sci., 2008, 14, 416-422.
103. Charloteaux, B.; Lorin, A.; Brasseur, R.; Lins, L. The "Tilted Peptide Theory" links membrane insertion properties and fusogenicity of viral fusion peptides. Prot. Pept. Lett., 2009, 16, 718-725.
104. Polyansky, A.A.; Volynsky, P.E.; Arseniev, A.S.; Efremov, R.G. Adaptation of a membrane-active peptide to heterogeneous environment. II. The role of mosaic nature of the membrane surface. J. Phys. Chem. B, 2009, 113, 1120-1126.
105. The PyMOL Molecular Graphics System, Version 1.3, Schrödinger, LLC.
106. Pyrkov, T.V.; Chugunov, A.O.; Krylov, N.A.; Nolde, D.E.; Efremov, R.G. PLATINUM: a web tool for analysis of hydrophobic/ hydrophilic organization of biomolecular complexes. Bioinformatics, 2009, 25, 1201-1202.
107. Han, X.; Steinhauer, D.A.; Wharton, S.A; Tamm, L.K. Interaction of mutant influenza virus hemagglutinin fusion peptides with lipid bilayers: probing the role of hydrophobic residue size in the central region of the fusion peptide. Biochemistry, 1999, 38, 15052-15059.
108. Shai, Y.; Oren, Z. From carpet mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides, 2001, 22, 1629-1641.
109. Conlon, J.M.; Ahmed, E.; Condamine, E. Antimicrobial properties of brevinin-2-related peptide and its analogs: Efficacy against multidrug-resistant Acinetobacter baumannii. Chem. Biol. Drug Des., 2009, 74, 488-493.
110. Ghosh, J.K.; Shai, Y. Direct evidence that the N-terminal heptad repeat of Sendai virus fusion protein participates in membrane fusion. J. Mol. Biol., 1999, 292, 531-546.
111. Yadav, S.P.; Kundu, B.; Ghosh, J.K. Identification and characterization of an amphipathic leucine zipper-like motif in Escherichia coli toxin hemolysin E. Plausible role in the assembly and membrane destabilization. J. Biol. Chem., 2003, 278, 51023-51034.
112. Asthana, N.; Yadav, S.P.; Ghosh, J.K. Dissection of antibacterial and toxic activity of melittin: a leucine zipper motif plays a crucial role in determining its hemolytic activity but not antibacterial activity. J. Biol. Chem, 2004, 279, 55042-55050.
113. Ahmad, A.; Azmi, S.; Srivastava, R.M.; Srivastava, S.; Pandey, B.K.; Saxena, R.; Bajpai, V.K.; Ghosh, J.K. Design of nontoxic analogues of cathelicidin-derived bovine antimicrobial peptide BMAP-27: the role of leucine as well as phenylalanine zipper sequences in determining its toxicity. Biochemistry, 2009, 48, 10905-10917.
114. Chen, Y.; Mant, C.T.; Farmer, S.W.; Hancock, R.E.; Vasil, M.L.; Hodges, R.S. Rational design of alpha-helical antimicrobial peptides with enhanced activities and specificity/therapeutic index. J. Biol. Chem., 2005, 280, 12316-12329.
115. Jiang, Z; Kullberg, B.J.; van der Lee, H.; Vasil, A.I.; Hale, J.D; Mant, C.T.; Hancock, R.E.; Vasil, M.L.; Netea, M.G.; Hodges, R.S. Effects of hydrophobicity on the antifungal activity of alphahelical antimicrobial peptides. Chem. Biol. Drug. Des., 2008, 72, 483-495.
116. Jiang, Z.; Vasil, A.I.; Hale, J.D.; Hancock, R.E.; Vasil, M.L.; Hodges, R.S. Effects of net charge and the number of positively charged residues on the biological activity of amphipathic alphahelical cationic antimicrobial peptides. Biopolymers, 2008, 90, 369-383.
117. Dathe, M.; Meyer, J.; Beyermann, M.; Maul, B.; Hoischen, C.; Bienert. General aspects of peptide selectivity towards lipid bilayers and cell membranes studied by variation of the structural parameters of amphipathic helical model peptides. Biochim. Biophys. Acta, 2002, 1558, 171-186.
118. Zelezetsky, I.; Tossi, A. Alpha-helical antimicrobial peptides--using a sequence template to guide structure-activity relationship studies. Biochim. Biophys. Acta, 2006, 1758, 1436-1449.
119. Jenssen, H.; Fjell, C.D.; Cherkasov, A.; Hancock, R.E. QSAR modeling and computer-aided design of antimicrobial peptides. J. Pept. Sci., 2008, 14, 110-114.
120. Taboureau, O. Methods for building quantitative structure-activity relationship (QSAR) descriptors and predictive models for computer-aided design of antimicrobial peptides. Methods Mol. Biol., 2010, 618, 77-86.
121. Taboureau, O.; Olsen, O.H.; Nielsen, J.D.; Raventos, D.; Mygind, P.H.; Kristensen, H.H. Design of novispirin antimicrobial peptides by quantitative structure-activity relationship. Chem. Biol. Drug. Des., 2006, 68, 48-57.
122. Rathinakumar, R.; Wimley, W.C. Biomolecular engineering by combinatorial design and high-throughput screening: small, soluble peptides that permeabilize membranes. J. Am. Chem. Soc., 2008, 130, 9849-9858.
123. Rathinakumar, R.; Walkenhorst, W.F.; Wimley, W.C. Broadspectrum antimicrobial peptides by rational combinatorial design and high-throughput screening: the importance of interfacial activity. J. Am. Chem. Soc., 2009, 131, 7609-7617.
124. Hilpert, K.; Fjell, C.D.; Cherkasov, A. Short linear cationic antimicrobial peptides: screening, optimizing, and prediction. Methods Mol. Biol., 2008, 494, 127-159.
125. Hilpert, K.; Volkmer-Engert, R.; Walter, T.; Hancock, R.E. Highthroughput generation of small antibacterial peptides with improved activity. Nat. Biotechnol., 2005, 23, 1008-1012.
126. Hilpert, K.; Elliott M.R.; Volkmer-Engert, R.; Henklein, P.; Donini, O.; Zhou, Q.; Winkler, D.F; Hancock, R.E. Sequence requirements and an optimization strategy for short antimicrobial peptides. Chem. Biol., 2006, 13, 1101-1117.
127. Fjell, C.D.; Jenssen, H.; Hilpert, K.; Cheung, W.A.; Panté, N.; Hancock, R.E.; Cherkasov, A. Identification of novel antibacterial peptides by chemoinformatics and machine learning. J. Med. Chem., 2009, 52, 2006-2015.
128. Cherkasov, A.; Hilpert, K.; Jenssen, H.; Fjell, C.D.; Waldbrook, M.; Mullaly, S.C.; Volkmer, R.; Hancock, R.E. Use of artificial intelligence in the design of small peptide antibiotics effective against a broad spectrum of highly antibiotic-resistant superbugs. ACS Chem. Biol., 2009, 4, 65-74.
129. Polyansky, A.A.; Vassilevski, A.A.; Volynsky, P.E.; Vorontsova, O.V.; Samsonova, O.V.; Egorova, N.S.; Krylov, N.A.; Feofanov, A.V.; Arseniev, A.S.; Grishin, E.V.; Efremov, R.G. N-terminal amphipathic helix as a trigger of hemolytic activity in antimicrobial peptides: a case study in latarcins. FEBS Lett., 2009, 583, 2425-2428.
130. Bhonsle, J.B.; Venugopal, D.; Huddler, D.P.; Magill, A.J.; Hicks, R.P. Application of 3D-QSAR for identification of descriptors defining bioactivity of antimicrobial peptides. J. Med. Chem., 2007, 50, 6545-6553.
131. Langham, A.A.; Khandelia, H.; Schuster, B.; Waring, A.J.; Lehrer, R.I.; Kaznessis, Y.N. Correlation between simulated physicochemical properties and hemolycity of protegrin-like antimicrobial peptides: predicting experimental toxicity. Peptides, 2008, 29, 1085-1093.
132. Mikut, R. Computer-based analysis, visualization, and interpretation of antimicrobial peptide activities. Methods Mol. Biol., 2010, 618, 287-299.
133. Tsai, C.W.; Hsu, N.Y.; Wang, C.H.; Lu C.Y.; Chang, Y.; Tsai, H.H.; Ruaan, R.C. Coupling molecular dynamics simulations with experiments for the rational design of indolicidin-analogous antimicrobial peptides. J. Mol. Biol., 2009, 392, 837-854.
134. Soman, S.S.; Sivakumar, K.C.; Sreekumar, E. Molecular dynamics simulation studies and in vitro site directed mutagenesis of avian beta-defensin Apl_AvBD2. BMC Bioinformatics, 2010, 11 Suppl 1: S7.
135. Frecer, V.; Ho B.; Ding J.L. De novo design of potent antimicrobial peptides. Antimicrob. Agents Chemother., 2004, 48, 3349-3357.
136. Tew, G.N.; Scott, R.W.; Klein, M.L.; Degrado, W.F. De novo design of antimicrobial polymers, foldamers, and small molecules: from discovery to practical applications. Acc. Chem. Res., 2010, 43, 30-39