What can machine learning do for antimicrobial peptides, and what can antimicrobial peptides do for machine learning?

Interface Focus

Volumn 7, Issue 6, 2017, Pages

  Lee, Ernest Y ^a   Lee, Michelle W ^a   Fulan, Benjamin M ^b   Ferguson, Andrew L ^b,c   Wong, Gerard C L ^a  

^a Engineering IV   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

Amphiphilic peptides; Antimicrobial peptides; Machine learning; Membrane curvature

Indexed keywords

EID: 85032030361     PISSN: 20428898     EISSN: 20428901     Source Type: Journal    
DOI: 10.1098/rsfs.2016.0153     Document Type: Review

References (135)

1. Lee EY, Fulan BM, Wong GCL, Ferguson AL. 2016 Mapping membrane activity in undiscovered peptide sequence space using machine learning. Proc. Natl Acad. Sci. USA 113, 13588-13593. (doi:10.1073/pnas.1609893113)
2. Lee EY, Wong GCL, Ferguson AL. 2017 Machine learning-enabled discovery and design of membrane-active peptides. Bioorg. Med. Chem. (doi:10.1016/j.bmc.2017.07.012)
3. Zasloff M. 2002 Antimicrobial peptides of multicellular organisms. Nature 415, 389-395. (doi:10.1038/415389a)
4. Shai Y. 1999 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, 55-70. (doi:10.1016/S0005-2736(99)00200-X)
5. Brogden KA. 2005 Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250. (doi:10.1038/nrmicro1098)
6. Hancock REW, Lehrer R. 1998 Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16, 82-88. (doi:10.1016/S0167-7799(97)01156-6)
7. Hancock REW, Sahl H-G. 2006 Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557. (doi:10.1038/nbt1267)
8. Yeaman MR, Yount NY. 2003 Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55. (doi:10.1124/pr.55.1.2)
9. Wang Z, Wang G. 2004 APD: the antimicrobial peptide database. Nucleic Acids Res. 32, D590-D592. (doi:10.1093/nar/gkh025)
10. Wang G, Li X, Wang Z. 2009 APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res. 37, D933-D937. (doi:10.1093/nar/gkn823)
11. Wang G, Li X, Wang Z. 2016 APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 44, D1087-D1093. (doi:10.1093/nar/gkv1278)
12. Skarnes RC, Watson DW. 1957 Antimicrobial factors of normal tissues and fluids. Bacteriol. Rev. 21, 273-294.
13. Zasloff M. 1987 Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc. Natl Acad. Sci. USA 84, 5449-5453. (doi:10.1073/pnas.84.15.5449)
14. Oren Z, Shai Y. 1998 Mode of action of linear amphipathic α-helical antimicrobial peptides. Biopolymers 47, 451-463. (doi:10.1002/(SICI)1097-0282(1998)47:6,451::AID-BIP4.3.0.CO;2-F)
15. Ganz T. 2003 Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-720. (doi:10.1038/nri1180)
16. Selsted ME, Novotny MJ, Morris WL, Tang YQ, Smith W, Cullor JS. 1992 Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267, 4292-4295.
17. Agerberth B, Lee JY, Bergman T, Carlquist M, Boman HG, Mutt V, Jörnvall H. 1991 Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur. J. Biochem. 202, 849-854. (doi:10.1111/j.1432-1033.1991.tb16442.x)
18. Wang G. 2008 Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles. J. Biol. Chem. 283, 32637-32643. (doi:10.1074/jbc.M805533200)
19. Gesell J, Zasloff M, Opella SJ. 1997 Two-dimensional 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an α-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J. Biomol. NMR 9, 127-135. (doi:10.1023/A:1018698002314)
20. Terwilliger TC, Eisenberg D. 1982 The structure of melittin. I. Structure determination and partial refinement. J. Biol. Chem. 257, 6010-6015.
21. Huang HW, Chen F-Y, Lee M-T. 2004 Molecular mechanism of peptide-induced pores in membranes. Phys. Rev. Lett. 92, 198304. (doi:10.1103/PhysRevLett.92.198304)
22. Hancock RE. W, Rozek A. 2002 Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206, 143-149. (doi:10.1111/j.1574-6968.2002.tb11000.x)
23. Yang L, Harroun TA, Weiss TM, Ding L, Huang HW. 2001 Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81, 1475-1485. (doi:10.1016/S0006-3495(01)75802-X)
24. Ehrenstein G, Lecar H. 1977 Electrically gated ionic channels in lipid bilayers. Q. Rev. Biophys. 10, 1-34. (doi:10.1017/S0033583500000123)
25. Lee M-T, Chen F-Y, Huang HW. 2004 Energetics of pore formation induced by membrane active peptides. Biochemistry 43, 3590-3599. (doi:10.1021/bi036153r)
26. Spaar A, Münster C, Salditt T. 2004 Conformation of peptides in lipid membranes studied by X-ray grazing incidence scattering. Biophys J. 87, 396-407. (doi:10.1529/biophysj.104.040667)
27. He K, Ludtke SJ, Worcester DL, Huang HW. 1996 Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys J. 70, 2659-2666. (doi:10.1016/S0006-3495(96)79835-1)
28. 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. (doi:10.1007/BF01877228)
29. Pouny Y, Rapaport D, Mor A, Nicolas P, Shai Y. 1992 Interaction of antimicrobial dermaseptin and its fluorescently labeled analogs with phospholipid membranes. Biochemistry 31, 12416-12423. (doi:10.1021/bi00164a017)
30. 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. (doi:10.1016/S0006-3495(01)75868-7)
31. Bechinger B. 1999 The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462, 157-183. (doi:10.1016/S0005-2736(99)00205-9)
32. Ladokhin AS, White SH. 2001 ‘Detergent-like’ permeabilization of anionic lipid vesicles by melittin. Biochim. Biophys. Acta 1514, 253-260. (doi:10.1016/S0005-2736(01)00382-0)
33. Matsuzaki K, Murase O, Fujii N, Miyajima K. 1996 An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35, 11361-11368. (doi:10.1021/bi960016v)
34. Hallock KJ, Lee D-K, 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. (doi:10.1016/S0006-3495(03)70031-9)
35. 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. (doi:10.1021/bi0257991)
36. Epand RM, Epand RF. 2011 Bacterial membrane lipids in the action of antimicrobial agents. J. Pept. Sci. 17, 298-305. (doi:10.1002/psc.1319)
37. Zachowski A. 1993 Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294, 1-14. (doi:10.1042/bj2940001)
38. van Meer G, Voelker DR, Feigenson GW. 2008 Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124. (doi:10.1038/nrm2330)
39. Zimmerberg J, Kozlov MM. 2006 How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19. (doi:10.1038/nrm1784)
40. Epand RF, Savage PB, Epand RM. 2007 Bacterial lipid composition and the antimicrobial efficacy of cationic steroid compounds (ceragenins). Biochim. Biophys. Acta 1768, 2500-2509. (doi:10.1016/j.bbamem.2007.05.023)
41. Siegel DP, Kozlov MM. 2004 The Gaussian curvature elastic modulus of N-monomethylated dioleoylphosphatidylethanolamine: relevance to membrane fusion and lipid phase behavior. Biophys J. 87, 366-374. (doi:10.1529/biophysj.104.040782)
42. Som A, Yang L, Wong GCL, Tew GN. 2009 Divalent metal ion triggered activity of a synthetic antimicrobial in cardiolipin membranes. J. Am. Chem. Soc. 131, 15102-15103. (doi:10.1021/ja9067063)
43. Yang L., et al. 2008 Mechanism of a prototypical synthetic membrane-active antimicrobial: efficient hole-punching via interaction with negative intrinsic curvature lipids. Proc. Natl. Acad. Sci. USA 105, 20595-20600. (doi:10.1073/pnas.0806456105)
44. Yang L, Gordon VD, Mishra A, Som A, Purdy KR, Davis MA, Tew GN, Wong GC. L. 2007 Synthetic antimicrobial oligomers induce a composition-dependent topological transition in membranes. J. Am. Chem. Soc. 129, 12141-12147. (doi:10.1021/ja072310o)
45. Hastie T, Tibshirani R, Friedman J. 2009 The elements of statistical learning. New York, NY: Springer Science & Business Media.
46. Turing AM. 1950 Computing machinery and intelligence. Mind 49, 433-460. (doi:10.1093/mind/LIX.236.433)
47. Graves A, Liwicki M, Fernández S, Bertolami R, Bunke H, Schmidhuber J. 2009 A novel connectionist system for unconstrained handwriting recognition. IEEE Trans. Pattern Anal. Mach. Intell. 31, 855-868. (doi:10.1109/TPAMI.2008.137)
48. Ganesan N, Venkatesh K, Rama MA. 2010 Application of neural networks in diagnosing cancer disease using demographic data. Inter. J. Comput. Theory Eng. 1, 81-97. (doi:10.5120/476-783)
49. Betechuoh BL, Marwala T, Tettey T. 2006 Autoencoder networks for HIV classification. Curr. Sci. 91, 1467-1473.
50. Agarwal M, Jain N, Kumar MM. 2010 Face recognition using eigen faces and artificial neural network. Inter. J. Comput. Theory Eng. 2, 624-629. (doi:10.7763/IJCTE.2010.V2.213)
51. Rothwell AC, Jagger LD, Dennis WR, Clarke DR. 2004 Intelligent spam detection system using an updateable neural analysis engine. Patent no. WO/ 2003/010680.
52. Balabin RM, Lomakina EI. 2009 Neural network approach to quantum-chemistry data: accurate prediction of density functional theory energies. J. Chem. Phys. 131, 074104. (doi:10.1063/1.3206326)
53. Silver D., et al. 2016 Mastering the game of Go with deep neural networks and tree search. Nature 529, 484-489. (doi:10.1038/nature16961)
54. Fjell CD, Jenssen H, Hilpert K, Cheung WA, Panté N, Hancock REW, Cherkasov A. 2009 Identification of novel antibacterial peptides by chemoinformatics and machine learning. J. Med. Chem. 52, 2006-2015. (doi:10.1021/jm8015365)
55. Mitchell JBO. 2014 Machine learning methods in chemoinformatics. Wiley Interdiscip. Rev. Comput. Mol. Sci. 4, 468-481. (doi:10.1002/wcms.1183)
56. Hilpert K, Fjell CD, Cherkasov A. 2008 Short linear cationic antimicrobial peptides: screening, optimizing, and prediction. Methods Mol. Biol. 494, 127-159. (doi:10.1007/978-1-59745-419-3_8)
57. Lata S, Sharma BK, Raghava G. 2007 Analysis and prediction of antibacterial peptides. BMC Bioinformatics 8, 1. (doi:10.1186/1471-2105-8-263)
58. Cherkasov A, Hilpert K, Jenssen H, Fjell CD, Waldbrook M, Mullaly SC, Volkmer R, Hancock REW. 2008 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, 65-74. (doi:10.1021/cb800240j)
59. Fjell CD, Jenssen H, Fries P, Aich P, Griebel P, Hilpert K, Hancock RE. W, Cherkasov A. 2008 Identification of novel host defense peptides and the absence of α-defensins in the bovine genome. Proteins Struct. Funct. Bioinform. 73, 420-430. (doi:10.1002/prot.22059)
60. Wang P., et al. 2011 Prediction of antimicrobial peptides based on sequence alignment and feature selection methods. PLoS ONE 6, e18476. (doi:10.1371/journal.pone.0018476)
61. Torrent M, Andreu D, Nogués VM, Boix E. 2011 Connecting peptide physicochemical and antimicrobial properties by a rational prediction model. PLoS ONE 6, e16968. (doi:10.1371/journal.pone.0016968)
62. Maccari G, Di Luca M, Nifosí R, Cardarelli F, Signore G, Boccardi C, Bifone A. 2013 Antimicrobial peptides design by evolutionary multiobjective optimization. PLoS Comput. Biol. 9, e1003212. (doi:10.1371/journal.pcbi.1003212)
63. Xiao X, Wang P, Lin W-Z, Jia J-H, Chou K-C. 2013 iAMP-2 L: a two-level multi-label classifier for identifying antimicrobial peptides and their functional types. Anal. Biochem. 436, 168-177. (doi:10.1016/j.ab.2013.01.019)
64. Giguère S, Laviolette F, Marchand M, Tremblay D, Moineau S, Liang X, Biron É, Corbeil J. 2015 Machine learning assisted design of highly active peptides for drug discovery. PLoS Comput. Biol. 11, e1004074. (doi:10.1371/journal.pcbi.1004074)
65. Schneider P, Müller AT, Gabernet G, Button AL, Posselt G, Wessler S, Hiss JA, Schneider G. 2017 Hybrid network model for ‘deep learning’ of chemical data: application to antimicrobial peptides. Mol. Inform. 36, 1600011. (doi:10.1002/minf.201600011)
66. Kozma D, Simon I, Tusnády GE. 2012 PDBTM: protein data bank of transmembrane proteins after 8 years. Nucleic Acids Res. 41, 1169. (doi:10.1093/nar/gks1169)
67. Porto WF, Pires ÁS, Franco OL. 2012 CS-AMPPred: an updated SVM model for antimicrobial activity prediction in cysteine-stabilized peptides. PLoS ONE 7, e51444. (doi:10.1371/journal.pone.0051444)
68. Gelbart WM, Ben-Shaul A, Roux DD. 1994 Micelles, membranes, microemulsions, and monolayers. New York, NY: Springer.
69. Schmidt NW, Wong GCL. 2013 Antimicrobial peptides and induced membrane curvature: geometry, coordination chemistry, and molecular engineering. Curr. Opin. Solid State Mat. Sci. 17, 151-163. (doi:10.1016/j.cossms.2013.09.004)
70. Schmidt NW., et al. 2011 Criterion for amino acid composition of defensins and antimicrobial peptides based on geometry of membrane destabilization. J. Am. Chem. Soc. 133, 6720-6727. (doi:10.1021/ja200079a)
71. Schmidt NW, Mishra A, Lai GH, Wong GCL. 2010 Arginine-rich cell-penetrating peptides. FEBS Lett. 584, 1806-1813. (doi:10.1016/j.febslet.2009.11.046)
72. Schmidt NW, Mishra A, Wang J, DeGrado WF, Wong GC. L. 2013 Influenza virus A M2 protein generates negative gaussian membrane curvature necessary for budding and scission. J. Am. Chem. Soc. 135, 13710-13719. (doi:10.1021/ja400146z)
73. Braun AR, Sevcsik E, Chin P, Rhoades E, Tristram-Nagle S, Sachs JN. 2012 α-Synuclein induces both positive mean curvature and negative Gaussian curvature in membranes. J. Am. Chem. Soc. 134, 2613-2620. (doi:10.1021/ja208316h)
74. Cao D-S, Xu Q.-S, Liang Y-Z. 2013 propy: A tool to generate various modes of Chou’s PseAAC. Bioinformatics 29, 960-962. (doi:10.1093/bioinformatics/btt072)
75. Pedregosa F., et al. 2011 Scikit-learn: machine learning in python. J. Mach. Learn. Res. 12, 2825-2830.
76. Mauri A, Ballabio D, Consonni V, Manganaro A, Todeschini R. 2008 Peptides multivariate characterisation using a molecular descriptor based approach. Match Commun. Math. Comput. Chem. 60, 671-690.
77. Li ZR, Lin HH, Han LY, Jiang L, Chen X, Chen YZ. 2006 PROFEAT: a web server for computing structural and physicochemical features of proteins and peptides from amino acid sequence. Nucleic Acids Res. 34, W32-W37. (doi:10.1093/nar/gkl305)
78. Bi J, Bennett K, Embrechts M, Breneman C, Song M. 2003 Dimensionality reduction via sparse support vector machines. J. Mach. Learn. Res. 3, 1229-1243.
79. Chou K-C. 2009 Pseudo amino acid composition and its applications in bioinformatics, proteomics and system biology. Curr. Proteomics 6, 262-274. (doi:10.2174/157016409789973707)
80. Grantham R. 1974 Amino acid difference formula to help explain protein evolution. Science 185, 862-864. (doi:10.1126/science.185.4154.862)
81. Gilks WR. 2005 Markov chain Monte Carlo. Chichester, UK: John Wiley & Sons, Ltd.
82. Gilks WR, Richardson S, Spiegelhalter D. 1995 Markov chain Monte Carlo in practice. Boca Raton, FL: CRC Press.
83. Geyer CJ. 1992 Practical Markov chain Monte Carlo. Stat. Sci. 7, 473-483. (doi:10.2307/2246094)
84. Arora JS. 2011 Introduction to optimum design. New York, NY: Academic Press.
85. Shoval O, Sheftel H, Shinar G, Hart Y, Ramote O, Mayo A, Dekel E, Kavanagh K, Alon U. 2012 Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. Science 336, 1157-1160. (doi:10.1126/science.1217405)
86. Park CB, Kim HS, Kim SC. 1998 Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244, 253-257. (doi:10.1006/bbrc.1998.8159)
87. Subbalakshmi C, Sitaram N. 1998 Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett. 160, 91-96. (doi:10.1111/j.1574-6968.1998.tb12896.x)
88. Patrzykat A, Friedrich CL, Zhang L, Mendoza V, Hancock REW. 2002 Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob. Agents Chemother. 46, 605-614. (doi:10.1128/AAC.46.3.605-614.2002)
89. Brötz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG. 1998 The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents Chemother. 42, 154-160.
90. Lande R., et al. 2007 Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449, 564-569. (doi:10.1038/nature06116)
91. Zhang L.-J, Gallo RL. 2016 Antimicrobial peptides. Curr. Biol. 26, R14-R19. (doi:10.1016/j.cub.2015.11.017)
92. Kreyszig E. 1991 Differential geometry. New York, NY: Dover Publications.
93. Koller D, Lohner K. 2014 The role of spontaneous lipid curvature in the interaction of interfacially active peptides with membranes. Biochim. Biophys. Acta 1838, 2250-2259. (doi:10.1016/j.bbamem.2014.05.013)
94. Deserno M. 2015 Fluid lipid membranes: from differential geometry to curvature stresses. Chem. Phys. Lipids 185, 11-45. (doi:10.1016/j.chemphyslip.2014.05.001)
95. Bechinger B. 2009 Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape. Curr. Opin. Colloid Interface Sci. 14, 349-355. (doi:10.1016/j.cocis.2009.02.004)
96. Baumgart T, Capraro BR, Zhu C, Das SL. 2011 Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 62, 483-506. (doi:10.1146/annurev.physchem.012809.103450)
97. Antonny B. 2011 Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80, 101-123. (doi:10.1146/annurev-biochem-052809-155121)
98. Stachowiak JC, Hayden CC, Sasaki DY. 2010 Steric confinement of proteins on lipid membranes can drive curvature and tubulation. Proc. Natl Acad. Sci. USA 107, 7781-7786. (doi:10.1073/pnas.0913306107)
99. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, Sherman MB, Geissler PL, Fletcher DA, Hayden CC. 2012 Membrane bending by protein-protein crowding. Nat. Cell Biol. 14, 944-949. (doi:10.1038/ncb2561)
100. Koltover I, Salditt T, Rädler JO, Safinya CR. 1998 An inverted hexagonal phase of cationic liposome-DNA complexes related to DNA release and delivery. Science 281, 78-81. (doi:10.1126/science.281.5373.78)
101. Raviv U, Needleman DJ, Li Y, Miller HP, Wilson L, Safinya CR. 2005 Cationic liposome-microtubule complexes: pathways to the formation of two-state lipid - protein nanotubes with open or closed ends. Proc. Natl Acad. Sci. USA 102, 11167-11172. (doi:10.1073/pnas.0502183102)
102. Tytler EM, Segrest JP, Epand RM, Nie SQ, Epand RF, Mishra VK, Venkatachalapathi YV, Anantharamaiah GM. 1993 Reciprocal effects of apolipoprotein and lytic peptide analogs on membranes. Cross-sectional molecular shapes of amphipathic alpha helixes control membrane stability. J. Biol. Chem. 268, 22112-22118.
103. Epand RM, Shai Y, Segrest JP, Anantharamiah GM. 1995 Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Pept. Sci. 37, 319-338. (doi:10.1002/bip.360370504)
104. Segrest JP, De Loof H, Dohlman JG, Brouillette CG, Anantharamaiah GM. 1990 Amphipathic helix motif: classes and properties. Proteins Struct. Funct. Bioinform. 8, 103-117. (doi:10.1002/prot.340080202)
105. Zemel A, Ben-Shaul A, May S. 2008 Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides. J. Phys. Chem. B 112, 6988-6996. (doi:10.1021/jp711107y)
106. Wieprecht T, Dathe M, Epand RM, Beyermann M, Krause E, Maloy WL, MacDonald DL, Bienert M. 1997 Influence of the angle subtended by the positively charged helix face on the membrane activity of amphipathic, antibacterial peptides. Biochemistry 36, 12869-12880. (doi:10.1021/bi971398n)
107. Drin G, Antonny B. 2009 Amphipathic helices and membrane curvature. FEBS Lett. 584, 1840-1847. (doi:10.1016/j.febslet.2009.10.022)
108. Chen F-Y, Lee M-T, Huang HW. 2003 Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys J. 84, 3751-3758. (doi:10.1016/S0006-3495(03)75103-0)
109. Tristram-Nagle S, Chan R, Kooijman E, Uppamoochikkal P, Qiang W, Weliky DP, Nagle JF. 2010 HIV fusion peptide penetrates, disorders, and softens T-cell membrane mimics. J. Mol. Biol. 402, 139-153. (doi:10.1016/j.jmb.2010.07.026)
110. Szleifer I, Kramer D, Ben-Shaul A, Roux D, Gelbart WM. 1988 Curvature elasticity of pure and mixed surfactant films. Phys. Rev. Lett. 60, 1966-1969. (doi:10.1103/PhysRevLett.60.1966)
111. Dathe M, Wieprecht T. 1999 Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta 1462, 71-87. (doi:10.1016/S0005-2736(99)00201-1)
112. Yang L, Weiss TM, Lehrer RI, Huang HW. 2000 Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys J. 79, 2002-2009. (doi:10.1016/S0006-3495(00)76448-4)
113. Ludtke SJ, He K, Heller WT, Harroun TA, Yang L, Huang HW. 1996 Membrane pores induced by magainin. Biochemistry 35, 13723-13728. (doi:10.1021/bi9620621)
114. Saiman L, Tabibi S, Starner TD, San Gabriel P, Winokur PL, Jia HP, McCray PB, Tack BF. 2001 Cathelicidin peptides inhibit multiply antibiotic-resistant pathogens from patients with cystic fibrosis. Antimicrob. Agents Chemother. 45, 2838-2844. (doi:10.1128/AAC.45.10.2838-2844.2001)
115. Kalfa VC, Jia HP, Kunkle RA, McCray PB, Tack BF, Brogden KA. 2001 Congeners of SMAP29 kill ovine pathogens and induce ultrastructural damage in bacterial cells. Antimicrob. Agents Chemother. 45, 3256-3261. (doi:10.1128/AAC.45.11.3256-3261.2001)
116. Yu Y, Vroman JA, Bae SC, Granick S. 2010 Vesicle budding induced by a pore-forming peptide. J. Am. Chem. Soc. 132, 195-201. (doi:10.1021/ja9059014)
117. Falagas ME, Kasiakou SK. 2005 Colistin: the revival of polymyxins for the management of multidrug-resistant Gram-negative bacterial infections. Clin. Infect. Dis. 40, 1333-1341. (doi:10.1086/429323)
118. Gidalevitz D, Ishitsuka Y, Muresan AS, Konovalov O, Waring AJ, Lehrer RI, Lee KYC. 2003 Interaction of antimicrobial peptide protegrin with biomembranes. Proc. Natl. Acad. Sci. USA 100, 6302-6307. (doi:10.1073/pnas.0934731100)
119. Schmidt NW, Tai KP, Kamdar K, Mishra A, Lai GH, Zhao K, Ouellette AJ, Wong GCL. 2012 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, 21866-21872. (doi:10.1074/jbc.M112.358721)
120. Lee MW, Chakraborty S, Schmidt NW, Murgai R, Gellman SH, Wong GCL. 2014 Two interdependent mechanisms of antimicrobial activity allow for efficient killing in nylon-3-based polymeric mimics of innate immunity peptides. Biochim. Biophys. Acta 1838, 2269-2279. (doi:10.1016/j.bbamem.2014.04.007)
121. Xiong M., et al. 2015 Helical antimicrobial polypeptides with radial amphiphilicity. Proc. Natl Acad. Sci. USA 112, 13155-13160. (doi:10.1073/pnas.1507893112)
122. Yao H, Lee MW, Waring AJ, Wong GC. L, Hong M. 2015 Viral fusion protein transmembrane domain adopts β-strand structure to facilitate membrane topological changes for virus - cell fusion. Proc. Natl. Acad. Sci. USA 112, 10926-10931. (doi:10.1073/pnas.1501430112)
123. Epand RM. 1993 The amphipathic helix. Boca Raton, FL: CRC Press.
124. Eisenberg D, Weiss RM, Terwilliger TC, Wilcox W. 1982 Hydrophobic moments and protein structure. Faraday Symp. Chem. Soc. 17, 109. (doi:10.1039/fs9821700109)
125. Dathe M, Wieprecht T, Nikolenko H, Handel L, Maloy WL, MacDonald DL, Beyermann M, Bienert M. 1997 Hydrophobicity, hydrophobic moment and angle subtended by charged residues modulate antibacterial and haemolytic activity of amphipathic helical peptides. FEBS Lett. 403, 208-212. (doi:10.1016/S0014-5793(97)00055-0)
126. Hu K., et al. 2013 A critical evaluation of random copolymer mimesis of homogeneous antimicrobial peptides. Macromolecules 46, 1908-1915. (doi:10.1021/ma302577e)
127. Pérez-Payá E, Houghten RA, Blondelle SE. 1995 The role of amphipathicity in the folding, self-association and biological activity of multiple subunit small proteins. J. Biol. Chem. 270, 1048-1056. (doi:10.1074/jbc.270.3.1048)
128. Subbalakshmi C, Nagaraj R, Sitaram N. 1999 Biological activities of C-terminal 15-residue synthetic fragment of melittin: design of an analog with improved antibacterial activity. FEBS Lett. 448, 62-66. (doi:10.1016/S0014-5793(99)00328-2)
129. Wieprecht T, Dathe M, Krause E, Beyermann M, Maloy WL, MacDonald DL, Bienert M. 1997 Modulation of membrane activity of amphipathic, antibacterial peptides by slight modifications of the hydrophobic moment. FEBS Lett. 417, 135-140. (doi:10.1016/S0014-5793(97)01266-0)
130. Dathe M, Schümann M, Wieprecht T, Winkler A, Beyermann M, Krause E, Matsuzaki K, Murase O, Bienert M. 1996 Peptide helicity and membrane surface charge modulate the balance of electrostatic and hydrophobic interactions with lipid bilayers and biological membranes. Biochemistry 35, 12612-12622. (doi:10.1021/bi960835f)
131. Wieprecht T, Dathe M, Beyermann M, Krause E, Maloy WL, MacDonald DL, Bienert M. 1997 Peptide hydrophobicity controls the activity and selectivity of magainin 2 amide in interaction with membranes. Biochemistry 36, 6124-6132. (doi:10.1021/bi9619987)
132. Schmidt NW, Lis M, Zhao K, Lai GH, Alexandrova AN, Tew GN, Wong GCL. 2012 Molecular basis for nanoscopic membrane curvature generation from quantum mechanical models and synthetic transporter sequences. J. Am. Chem. Soc. 134, 19207-19216. (doi:10.1021/ja308459j)
133. Wu Z, Cui Q, Yethiraj A. 2013 Why do arginine and lysine organize lipids differently? Insights from coarse-grained and atomistic simulations. J. Phys. Chem. B 117, 12145-12156. (doi:10.1021/jp4068729)
134. Cui Q, Zhang L, Wu Z, Yethiraj A. 2013 Generation and sensing of membrane curvature: where materials science and biophysics meet. Curr. Opin. Solid State Mat. Sci. 17, 164-174. (doi:10.1016/j.cossms.2013.06.002)
135. Mishra A, Gordon VD, Yang L, Coridan R, Wong GCL. 2008 HIV TAT forms pores in membranes by inducing saddle-splay curvature: potential role of bidentate hydrogen bonding. Angew. Chem. Int. Ed. Engl. 47, 2986-2989. (doi:10.1002/anie.200704444)