Advertisement

The Mechanisms of Action of Cationic Antimicrobial Peptides Refined by Novel Concepts from Biophysical Investigations

  • Christopher Aisenbrey
  • Arnaud Marquette
  • Burkhard BechingerEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1117)

Abstract

Even 30 years after the discovery of magainins, biophysical and structural investigations on how these peptides interact with membranes can still bear surprises and add new interesting detail to how these peptides exert their antimicrobial action. Early on, using oriented solid-state NMR spectroscopy, it was found that the amphipathic helices formed by magainins are active when being oriented parallel to the membrane surface. More recent investigations indicate that this in-planar alignment is also found when PGLa and magainin in combination exert synergistic pore-forming activities, where studies on the mechanism of synergistic interaction are ongoing. In a related manner, the investigation of dimeric antimicrobial peptide sequences has become an interesting topic of research which bears promise to refine our views how antimicrobial action occurs. The molecular shape concept has been introduced to explain the effects of lipids and peptides on membrane morphology, locally and globally, and in particular of cationic amphipathic helices that partition into the membrane interface. This concept has been extended in this review to include more recent ideas on soft membranes that can adapt to external stimuli including membrane-disruptive molecules. In this manner, the lipids can change their shape in the presence of low peptide concentrations, thereby maintaining the bilayer properties. At higher peptide concentrations, phase transitions occur which lead to the formation of pores and membrane lytic processes. In the context of the molecular shape concept, the properties of lipopeptides, including surfactins, are shortly presented, and comparisons with the hydrophobic alamethicin sequence are made.

Keywords

Magainin PGLa Cecropin LL37 Surfactin Alamethicin Membrane topology Membrane pore Membrane macroscopic phase SMART model Carpet model Toroidal pore model Peptide-lipid interactions Molecular shape concept 

Abbreviations

Aib

α-Aminobutyric acid

AMP

Antimicrobial peptide

ATR FTIR

Attenuated total reflection Fourier transform infrared

CD

Circular dichroism

CL

Cardiolipin

CMC

Critical micelle concentration

DLPC

1,2-Lauroyl-sn-glycero-3-phosphocholine

DMPC

1,2-Dimyristoyl-sn-glycero-3-zhosphocholine

DMPG

1,2-Dimyristoyl-sn-glycero-3-phospho-(1′-rac-glycerol)

DOPC

1,2-Dioleoyl-sn-glycero-3-phosphocholine

DOPG

1,2-Dioleoyl-sn-glycero-3-phospho-(1′-rac-glycerol)

DPC

Dodecylphosphocholine

GUV

Giant unilamellar vesicle

ITC

Isothermal titration calorimetry

LUV

Large unilamellar vesicle

MD

Molecular dynamics

MIC

Minimal inhibitory concentration

NMR

Nuclear magnetic resonance

PC

Phosphatidylcholine

PE

Phosphatidylethanolamine

PG

Phosphatidylglycerol

POPC

1-Palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine

POPE

1-Palmitoyl-2-oleoyl-sn-glycero-3-phosphoethanolamine

POPG

1-Palmitoyl-2-oleoyl-sn-glycero-3-phospho-(1′-rac-glycerol)

POPS

1-Palmitoyl-2-oleoyl-sn-glycero-3-phosphoserine

SMART

Soft Membranes Adapt and Respond, also Transiently

Notes

Acknowledgments

We gratefully acknowledge the discussion with and contributions from many coworkers and colleagues from our own team and from outside. We are grateful to Ekaterina Zaitseva for her feedback on electrophysiology and Roland Stote for much helping to refine the text on molecular dynamics. Over the years, the Agence Nationale de la Recherche (projects TRANSPEP 07-PCV-0018, ProLipIn 10-BLAN-731, membraneDNP 12-BSV5-0012, MemPepSyn 14-CE34-0001-01, InMembrane 15-CE11-0017-01, Biosupramol 17-CE18-0033-3, and the LabEx Chemistry of Complex Systems 10-LABX-0026_CSC), the IRTG Soft Matter Science (Freiburg, Strasbourg), the Marie-Curie Research and Training Network 33439 of the European Commission BIOCONTROL, the University of Strasbourg, the CNRS, the Région Alsace, the RTRA International Center of Frontier Research in Chemistry, and the French Foundation for Medical Research (FRM) have provided financial support. BB thanks the Institut Universitaire de France for providing additional time to be dedicated to research.

References

  1. Acar JF (2000) Antibiotic synergy and antagonism. Med Clin N Am 84:1391–1406CrossRefPubMedGoogle Scholar
  2. Agerberth B, Gunne H, Odeberg J, Kogner P, Boman HG, Gudmundsson GH (1995) FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proc Natl Acad Sci U S A 92:195–199CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ahn M, Gunasekaran P, Rajasekaran G, Kim EY, Lee SJ, Bang G, Cho K, Hyun JK, Lee HJ, Jeon YH, Kim NH, Ryu EK, Shin SY, Bang JK (2017) Pyrazole derived ultra-short antimicrobial peptidomimetics with potent anti-biofilm activity. Eur J Med Chem 125:551–564CrossRefPubMedGoogle Scholar
  4. Aisenbrey C, Bechinger B (2004) Tilt and rotational pitch angles of membrane-inserted polypeptides from combined 15N and 2H solid-state NMR spectroscopy. Biochemistry 43:10502–10512CrossRefPubMedGoogle Scholar
  5. Aisenbrey C, Bechinger B (2014) Molecular packing of amphipathic peptides on the surface of lipid membranes. Langmuir 30:10374–10383CrossRefPubMedGoogle Scholar
  6. Amos ST, Vermeer LS, Ferguson PM, Kozlowska J, Davy M, Bui TT, Drake AF, Lorenz CD, Mason AJ (2016) Antimicrobial peptide potency is facilitated by greater conformational flexibility when binding to gram-negative bacterial inner membranes. Sci Rep 6:37639CrossRefPubMedPubMedCentralGoogle Scholar
  7. Arnusch CJ, Albada HB, van Vaardegem M, Liskamp RMJ, Sahl HG, Shadkchan Y, Osherov N, Shai Y (2012) Trivalent ultrashort lipopeptides are potent pH dependent antifungal agents. J Med Chem 55:1296–1302CrossRefPubMedGoogle Scholar
  8. Avitabile C, D’Andrea LD, Romanelli A (2014) Circular dichroism studies on the interactions of antimicrobial peptides with bacterial cells. Sci Rep 4:4293CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bak M, Bywater RP, Hohwy M, Thomsen JK, Adelhorst K, Jakobsen HJ, Sorensen OW, Nielsen NC (2001) Conformation of alamethicin in oriented phospholipid bilayers determined by N-15 solid-state nuclear magnetic resonance. Biophys J 81:1684–1698CrossRefPubMedPubMedCentralGoogle Scholar
  10. Barns KJ, Weisshaar JC (2013) Real-time attack of LL-37 on single Bacillus subtilis cells. Biochim Biophys Acta 1828:1511–1520CrossRefPubMedPubMedCentralGoogle Scholar
  11. Barns KJ, Weisshaar JC (2016) Single-cell, time-resolved study of the effects of the antimicrobial peptide alamethicin on Bacillus subtilis. Biochim Biophys Acta 1858:725–732CrossRefPubMedPubMedCentralGoogle Scholar
  12. Batenburg AM, van Esch JH, De Kruijff B (1988) Melittin-induced changes of the macroscopic structure of phosphatidylethanolamines. Biochemistry 27:2324–2331CrossRefPubMedGoogle Scholar
  13. Bechinger B (1996) Towards membrane protein design: pH-sensitive topology of histidine-containing polypeptides. J Mol Biol 263:768–775CrossRefPubMedGoogle Scholar
  14. Bechinger B (1997) Structure and functions of channel-forming polypeptides: magainins, cecropins, melittin and alamethicin. J Membr Biol 156:197–211CrossRefPubMedGoogle Scholar
  15. Bechinger B (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim Biophys Acta 1462:157–183CrossRefPubMedGoogle Scholar
  16. Bechinger B (2004) Membrane-lytic peptides. Crit Rev Plant Sci 23:271–292CrossRefGoogle Scholar
  17. Bechinger B (2005) Detergent-like properties of magainin antibiotic peptides: a 31P solid-state NMR study. Biochim Biophys Acta 1712:101–108CrossRefPubMedGoogle Scholar
  18. Bechinger B (2009) Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape. Cur Opin Colloid Interface Sci Surfactant 14:349–355CrossRefGoogle Scholar
  19. Bechinger B (2011) Insights into the mechanisms of action of host defence peptides from biophysical and structural investigations. J Pept Sci 17:306–314CrossRefPubMedGoogle Scholar
  20. Bechinger B (2015) The SMART model: soft membranes adapt and respond, also transiently, to external stimuli. J Pept Sci 21:346–355CrossRefPubMedGoogle Scholar
  21. Bechinger B, Gorr SU (2017) Antimicrobial peptides: mechanisms of action and resistance. J Dent Res 96:254–260CrossRefPubMedGoogle Scholar
  22. Bechinger B, Lohner K (2006) Detergent-like action of linear cationic membrane-active antibiotic peptides. Biochim Biophys Acta 1758:1529–1539CrossRefPubMedGoogle Scholar
  23. Bechinger B, Salnikov ES (2012) The membrane interactions of antimicrobial peptides revealed by solid-state NMR spectroscopy. Chem Phys Lipids 165:282–301CrossRefPubMedGoogle Scholar
  24. Bechinger B, Sizun C (2003) Alignment and structural analysis of membrane polypeptides by 15N and 31P solid-state NMR spectroscopy. Concepts Magn Reson 18A:130–145CrossRefGoogle Scholar
  25. Bechinger B, Shon K, Eck H, Zasloff M, Opella SJ (1990) NMR studies of magainin peptide antibiotics in membranes. Biol Chem Hoppe Seyler 371:758–758Google Scholar
  26. Bechinger B, Kim Y, Chirlian LE, Gesell J, Neumann JM, Montal M, Tomich J, Zasloff M, Opella SJ (1991a) Orientations of amphipathic helical peptides in membrane bilayers determined by solid- state NMR spectroscopy. J Biomol NMR 1:167–173CrossRefPubMedGoogle Scholar
  27. Bechinger B, Zasloff M, Opella SJ (1991b) Solid state NMR of magainin and PGLa peptide antibiotics in bilayers. J Cell Biochem Suppl 15G:84Google Scholar
  28. Bechinger B, Zasloff M, Opella SJ (1992) Structure and interactions of magainin antibiotic peptides in lipid bilayers: a solid-state NMR investigation. BiophysJ 62:12–14CrossRefGoogle Scholar
  29. Bechinger B, Zasloff M, Opella SJ (1993) Structure and orientation of the antibiotic peptide magainin in membranes by solid-state NMR spectroscopy. Protein Sci 2:2077–2084CrossRefPubMedPubMedCentralGoogle Scholar
  30. Bechinger B, Zasloff M, Opella SJ (1998) Structure and dynamics of the antibiotic peptide PGLa in membranes by multidimensional solution and solid-state NMR spectroscopy. Biophys J 74:981–987CrossRefPubMedPubMedCentralGoogle Scholar
  31. Bechinger B, Ruysschaert JM, Goormaghtigh E (1999) Membrane helix orientation from linear dichroism of infrared attenuated Total reflection spectra. Biophys J 76:552–563CrossRefPubMedPubMedCentralGoogle Scholar
  32. Bechinger B, Resende JM, Aisenbrey C (2011) The structural and topological analysis of membrane-associated polypeptides by oriented solid-state NMR spectroscopy: established concepts and novel developments. Biophys Chem 153:115–125CrossRefPubMedGoogle Scholar
  33. Bolen EJ, Holloway PW (1990) Quenching of tryptophan fluorescence by brominated phospholipid. Biochemistry 29:9638–9643CrossRefPubMedGoogle Scholar
  34. Bolosov IA, Kalashnikov AA, Panteleev PV, Ovchinnikova TV (2017) Analysis of synergistic effects of antimicrobial peptide arenicin-1 and conventional antibiotics. Bull Exp Biol Med 162:765–768CrossRefPubMedGoogle Scholar
  35. Boman HG (1995) Peptide antibiotics and their role in innate immunity. Annu Rev Immunol 13:61–92CrossRefPubMedGoogle Scholar
  36. Bortolus M, Dalzini A, Toniolo C, Hahm KS, Maniero AL (2014) Interaction of hydrophobic and amphipathic antimicrobial peptides with lipid bicelles. J Pept Sci 20:517–525CrossRefPubMedGoogle Scholar
  37. Brown LR (1979) Use of fully deuterated micelles for conformational studies of membrane proteins by high resolution 1H nuclear magnetic resonance. Biochim Biophys Acta 557:135–148CrossRefPubMedGoogle Scholar
  38. Bruch MD, Dhingra MM, Gierasch LM (1991) Side chain-backbone hydrogen bonding contributes to helix stability in peptides derived from an alpha-helical region of carboxypeptidase A. Proteins Struct Funct Genet 10:130–139CrossRefPubMedGoogle Scholar
  39. Cao P, Yang Y, Uche FI, Hart SR, Li WW, Yuan C (2018) Coupling plant-derived cyclotides to metal surfaces: an antibacterial and antibiofilm study. Int J Mol Sci 19:E793CrossRefPubMedGoogle Scholar
  40. Caputo GA, London E (2003) Using a novel dual fluorescence quenching assay for measurement of tryptophan depth within lipid bilayers to determine hydrophobic alpha-helix locations within membranes. Biochemistry 42:3265–3274CrossRefPubMedGoogle Scholar
  41. Cardoso MH, de Almeida KC, Candido ES, Murad AM, Dias SC, Franco OL (2017) Comparative NanoUPLC-MS(E) analysis between magainin I-susceptible and -resistant Escherichia coli strains. Sci Rep 7:4197CrossRefPubMedPubMedCentralGoogle Scholar
  42. Carrillo C, Teruel JA, Aranda FJ, Ortiz A (2003) Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim Biophys Acta 1611:91–97CrossRefPubMedGoogle Scholar
  43. Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Downes FP, Shah S, Rudrik JT, Pupp GR, Brown WJ, Cardo D, Fridkin SK, Staphylococcus V-R (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 348:1342–1347CrossRefPubMedGoogle Scholar
  44. Chen FY, Lee MT, Huang HW (2003) Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys J 84:3751–3758CrossRefPubMedPubMedCentralGoogle Scholar
  45. Cheng JTJ, Hale JD, Elliot M, Hancock REW, Straus SK (2009) Effect of membrane composition on antimicrobial peptides aurein 2.2 and 2.3 from Australian Southern Bell Frogs. Biophys J 96:552–565CrossRefPubMedPubMedCentralGoogle Scholar
  46. Cheng JTJ, Hale JD, Elliott M, Hancock REW, Straus SK (2011) The importance of bacterial membrane composition in the structure and function of aurein 2.2 and selected variants. Biochim Biophys Acta 1808:622–633CrossRefPubMedGoogle Scholar
  47. Choi H, Rangarajan N, Weisshaar JC (2016) Lights, camera, action! Antimicrobial peptide mechanisms imaged in space and time. Trends Microbiol 24:111–122CrossRefPubMedGoogle Scholar
  48. Choi H, Yang Z, Weisshaar JC (2017) Oxidative stress induced in E. coli by the human antimicrobial peptide LL-37. PLoS Pathog 13:e1006481CrossRefPubMedPubMedCentralGoogle Scholar
  49. Chou S, Shao C, Wang J, Shan A, Xu L, Dong N, Li Z (2016) Short, multiple-stranded beta-hairpin peptides have antimicrobial potency with high selectivity and salt resistance. Acta Biomater 30:78–93CrossRefPubMedGoogle Scholar
  50. Christensen B, Fink J, Merrifield RB, Mauzerall D (1988) Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc Natl Acad Sci USA 85:5072–5076CrossRefPubMedGoogle Scholar
  51. Clark KS, Svetlovics J, McKeown AN, Huskins L, Almeida PF (2011) What determines the activity of antimicrobial and cytolytic peptides in model membranes. Biochemistry 50:7919–7932CrossRefPubMedPubMedCentralGoogle Scholar
  52. Cruciani RA, Barker JL, Zasloff M, Chen HC, Colamonici O (1991) Antibiotic magainins exert cytolytic activity transformed cell lines through channel formation. Proc Natl Acad Sci U S A 88:3792–3796CrossRefPubMedPubMedCentralGoogle Scholar
  53. Cruzeiro-Hansson L, Mouritsen OG (1988) Passive ion permeability of lipid membranes modelled via lipid-domain interfacial area. Biochim Biophys Acta 944:63–72CrossRefPubMedGoogle Scholar
  54. Cuervo JH, Rodriguez B, Houghten RA (1988) The magainins: sequence factors relevant to increased antimicrobial activity and decreased hemolytic activity. Pept Res 1:81–86PubMedGoogle Scholar
  55. Dalla Serra M, Cirioni O, Vitale RM, Renzone G, Coraiola M, Giacometti A, Potrich C, Baroni E, Guella G, Sanseverino M, De LS, Scalise G, Amodeo P, Scaloni A (2008) Structural features of distinctin affecting peptide biological and biochemical properties. Biochemistry 47:7888–7899CrossRefPubMedGoogle Scholar
  56. Das N, Dai J, Hung I, Rajagopalan MR, Zhou HX, Cross TA (2015) Structure of CrgA, a cell division structural and regulatory protein from Mycobacterium tuberculosis, in lipid bilayers. Proc Natl Acad Sci U S A 112:E119–E126CrossRefPubMedGoogle Scholar
  57. del Rio Martinez JM, Zaitseva E, Petersen S, Baaken G, Behrends JC (2015) Automated formation of lipid membrane microarrays for ionic single-molecule sensing with protein nanopores. Small 11:119–125CrossRefPubMedGoogle Scholar
  58. Dempsey CE, Ueno S, Avison MB (2003) Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue. Biochemistry 42:402–409CrossRefPubMedGoogle Scholar
  59. Diamond G, Beckloff N, Weinberg A, Kisich KO (2009) The roles of antimicrobial peptides in innate host defense. Curr Pharm Des 15:2377–2392CrossRefPubMedPubMedCentralGoogle Scholar
  60. Duclohier H, Molle G, Spach G (1989) Antimicrobial peptide magainin I from xenopus skin forms anion-permeable channels in planar lipid bilayers. Biophys J 56:1017–1021CrossRefPubMedPubMedCentralGoogle Scholar
  61. Eddy MT, Su Y, Silvers R, Andreas L, Clark L, Wagner G, Pintacuda G, Emsley L, Griffin RG (2015) Lipid bilayer-bound conformation of an integral membrane beta barrel protein by multidimensional MAS NMR. J Biomol NMR 61:299–310CrossRefPubMedPubMedCentralGoogle Scholar
  62. Farrotti A, Bocchinfuso G, Palleschi A, Rosato N, Salnikov ES, Voievoda N, Bechinger B, Stella L (2015) Molecular dynamics methods to predict peptide location in membranes: LAH4 as a stringent test case. Biochim Biophys Acta 1848:581–592CrossRefPubMedGoogle Scholar
  63. Gallaher J, Wodzinska K, Heimburg T, Bier M (2010) Ion-channel-like behavior in lipid bilayer membranes at the melting transition. Phys Rev E Stat Nonlinear Soft Matter Phys 81:061925CrossRefGoogle Scholar
  64. Gazit E, Miller IR, Biggin PC, Sansom MSP, Shai Y (1996) Structure and orientation of the mammalian antibacterial peptide cecropin P1 within phospholipid membranes. J Mol Biol 258:860–870CrossRefPubMedGoogle Scholar
  65. Georgescu J, Munhoz VHO, Bechinger B (2010) NMR structures of the histidine-rich peptide LAH4 in micellar environments: membrane insertion, pH-dependent mode of antimicrobial action and DNA transfection. Biophys J 99:2507–2515CrossRefPubMedPubMedCentralGoogle Scholar
  66. Ghosh C, Haldar J (2015) Membrane-active small molecules: designs inspired by antimicrobial peptides. ChemMedChem 10:1606–1624CrossRefPubMedGoogle Scholar
  67. Ghosh C, Manjunath GB, Akkapeddi P, Yarlagadda V, Hoque J, Uppu DSSM, Konai MM, Haldar J (2014) Small molecular antibacterial peptoid mimics: the simpler the better! J Med Chem 57:1428–1436CrossRefPubMedGoogle Scholar
  68. Ghosh C, Harmouche N, Bechinger B, Haldar J (2018) Aryl-alkyl-lysines interact with anionic lipid components of bacterial cell envelope eliciting anti-inflammatory and anti-biofilm properties. ACS Omega 3:9182–9190CrossRefGoogle Scholar
  69. Giovannini MG, Poulter L, Gibson BW, Williams DH (1987) Biosynthesis and degradation of peptides derived from Xenopus laevis prohormones. Biochem J 243:113–120CrossRefPubMedPubMedCentralGoogle Scholar
  70. Glattard E, Salnikov ES, Aisenbrey C, Bechinger B (2016) Investigations of the synergistic enhancement of antimicrobial activity in mixtures of magainin 2 and PGLa. Biophys Chem 210:35–44CrossRefPubMedGoogle Scholar
  71. Gogonea V (2015) Structural insights into high density lipoprotein: old models and new facts. Front Pharmacol 6:318PubMedGoogle Scholar
  72. Gopinath T, Veglia G (2015) Multiple acquisition of magic angle spinning solid-state NMR experiments using one receiver: application to microcrystalline and membrane protein preparations. J Magn Reson 253:143–153CrossRefPubMedPubMedCentralGoogle Scholar
  73. Gopinath T, Mote KR, Veglia G (2015) Simultaneous acquisition of 2D and 3D solid-state NMR experiments for sequential assignment of oriented membrane protein samples. J Biomol NMR 62:53–61CrossRefPubMedPubMedCentralGoogle Scholar
  74. Grage SL, Afonin S, Kara S, Buth G, Ulrich AS (2016) Membrane thinning and thickening induced by membrane-active amphipathic peptides. Front Cell Dev Biol 4:65CrossRefPubMedPubMedCentralGoogle Scholar
  75. Grau A, Gomez Fernandez JC, Peypoux F, Ortiz A (1999) A study on the interactions of surfactin with phospholipid vesicles. Biochim Biophys Acta 1418:307–319CrossRefPubMedGoogle Scholar
  76. Gregory SM, Cavenaugh A, Journigan V, Pokorny A, Almeida PFF (2008) A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide cecropin A. Biophys J 94:1667–1680CrossRefPubMedPubMedCentralGoogle Scholar
  77. Hadley EB, Hancock RE (2010) Strategies for the discovery and advancement of novel cationic antimicrobial peptides. Curr Top Med Chem 10:1872–1881CrossRefPubMedGoogle Scholar
  78. Hall K, Lee TH, Mechler AI, Swann MJ, Aguilar MI (2014) Real-time measurement of membrane conformational states induced by antimicrobial peptides: balance between recovery and lysis. Sci Rep 4:5479CrossRefPubMedPubMedCentralGoogle Scholar
  79. Hallock KJ, Lee DK, Omnaas J, Mosberg HI, Ramamoorthy A (2002) Membrane composition determines pardaxin’s mechanism of lipid bilayer disruption. Biophys J 83:1004–1013CrossRefPubMedPubMedCentralGoogle Scholar
  80. Hara T, Kodama H, Kondo M, Wakamatsu K, Takeda A, Tachi T, Matsuzaki K (2001) Effects of peptide dimerization on pore formation: antiparallel disulfide-dimerized magainin 2 analogue. Biopolymers 58:437–446CrossRefPubMedGoogle Scholar
  81. Harmouche N, Bechinger B (2018) Lipid-mediated interactions between the amphipathic antimicrobial peptides magainin 2 and PGLa in phospholipid bilayers. Biophys J 115:1033-1044Google Scholar
  82. Harpole TJ, Delemotte L (2018) Conformational landscapes of membrane proteins delineated by enhanced sampling molecular dynamics simulations. Biochim Biophys Acta 1860:909–926CrossRefGoogle Scholar
  83. Harzer U, Bechinger B (2000) The alignment of lysine-anchored membrane peptides under conditions of hydrophobic mismatch: a CD, 15 N and 31 P solid-state NMR spectroscopy investigation. Biochemistry 39:13106–13114CrossRefPubMedGoogle Scholar
  84. Hasan M, Karal MAS, Levadnyy V, Yamazaki M (2018) Mechanism of initial stage of pore formation induced by antimicrobial peptide magainin 2. Langmuir 34:3349–3362CrossRefPubMedGoogle Scholar
  85. Hayden RM, Goldberg GK, Ferguson BM, Schoeneck MW, Libardo MD, Mayeux SE, Shrestha A, Bogardus KA, Hammer J, Pryshchep S, Lehman HK, McCormick ML, Blazyk J, Angeles-Boza AM, Fu R, Cotten ML (2015) Complementary effects of host defense peptides piscidin 1 and piscidin 3 on DNA and lipid membranes: biophysical insights into contrasting biological activities. J Phys Chem B 119:15235–15246CrossRefPubMedGoogle Scholar
  86. He K, Ludtke SJ, Heller WT, Huang HW (1996) Mechanism of alamethicin insertion into lipid bilayers. Biophys J 71:2669–2679CrossRefPubMedPubMedCentralGoogle Scholar
  87. Heerklotz H, Seelig J (2001) Detergent-like action of the antibiotic peptide surfactin on lipid membranes. Biophys J 81:1547–1554CrossRefPubMedPubMedCentralGoogle Scholar
  88. Heerklotz H, Seelig J (2007) Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur Biophys J 36:305–314CrossRefPubMedGoogle Scholar
  89. Heerklotz H, Wieprecht T, Seelig J (2004) Membrane perturbation by the lipopeptide surfactin and detergents as studied by deuterium. J Phys Chem B 108:4909–4915CrossRefGoogle Scholar
  90. Heimburg T (2012) The capacitance and electromechanical coupling of lipid membranes close to transitions: the effect of electrostriction. Biophys J 103:918–929CrossRefPubMedPubMedCentralGoogle Scholar
  91. Henderson JM, Waring AJ, Separovic F, Lee KYC (2016) Antimicrobial peptides share a common interaction driven by membrane line tension reduction. Biophys J 111:2176–2189CrossRefPubMedPubMedCentralGoogle Scholar
  92. Holzl MA, Hofer J, Steinberger P, Pfistershammer K, Zlabinger GJ (2008) Host antimicrobial proteins as endogenous immunomodulators. Immunol Lett 119:4–11CrossRefPubMedGoogle Scholar
  93. Hong M, Su Y (2011) Structure and dynamics of cationic membrane peptides and proteins: insights from solid-state NMR. Protein Sci 20:641–655CrossRefPubMedPubMedCentralGoogle Scholar
  94. Imura Y, Choda N, Matsuzaki K (2008) Magainin 2 in action: distinct modes of membrane permeabilization in living bacterial and mammalian cells. Biophys J 95:5757–5765CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ines M, Dhouha G (2015) Lipopeptide surfactants: production, recovery and pore forming capacity. Peptides 71:100–112CrossRefPubMedGoogle Scholar
  96. Islam MZ, Alam JM, Tamba Y, Karal MAS, Yamazaki M (2014) The single GUV method for revealing the functions of antimicrobial, pore-forming toxin, and cell-penetrating peptides or proteins. Phys Chem Chem Phys 16:15752–15767CrossRefPubMedGoogle Scholar
  97. Israelachvili JN, Marcelja S, Horn RG (1980) Physical principles of membrane organization. Q Rev Biophys 13:121–200CrossRefPubMedGoogle Scholar
  98. Itkin A, Salnikov ES, Aisenbrey C, Raya J, Raussens V, Ruysschaert JM, Bechinger B (2017) Evidence for heterogeneous conformations of the gamma cleavage site within the amyloid precursor proteins transmembrane domain. ACS Omega 2:6525–6534CrossRefGoogle Scholar
  99. Jaipuria G, Leonov A, Giller K, Vasa SK, Jaremko L, Jaremko M, Linser R, Becker S, Zweckstetter M (2017) Cholesterol-mediated allosteric regulation of the mitochondrial translocator protein structure. Nat Commun 8:14893CrossRefPubMedPubMedCentralGoogle Scholar
  100. Jean-Francois F, Castano S, Desbat B, Odaert B, Roux M, Metz-Boutigue MH, Dufourc EJ (2008) Aggregation of cateslytin beta-sheets on negatively charged lipids promotes rigid membrane domains. A new mode of action for antimicrobial peptides? Biochemistry 47:6394–6402CrossRefPubMedGoogle Scholar
  101. Jenssen H, Hamill P, Hancock RE (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19:491–511CrossRefPubMedPubMedCentralGoogle Scholar
  102. Kandaswamy K, Liew TH, Wang CY, Huston-Warren E, Meyer-Hoffert U, Hultenby K, Schroder JM, Caparon MG, Normark S, Henriques-Normark B, Hultgren SJ, Kline KA (2013) Focal targeting by human beta-defensin 2 disrupts localized virulence factor assembly sites in Enterococcus faecalis. Proc Natl Acad Sci U S A 110:20230–20235CrossRefPubMedPubMedCentralGoogle Scholar
  103. Karal MA, Alam JM, Takahashi T, Levadny V, Yamazaki M (2015) Stretch-activated pore of the antimicrobial peptide, magainin 2. Langmuir 31:3391–3401CrossRefPubMedGoogle Scholar
  104. Killian JA, de Planque MRR, van der Wel PCA, Salemink I, De Kruijff B, Greathouse DV, Koeppe RE (1998) Modulation of membrane structure and function by hydrophobic mismatch between proteins and lipids. Pure Appl Chem 70:75–82CrossRefGoogle Scholar
  105. Kim C, Spano J, Park EK, Wi S (2009) Evidence of pores and thinned lipid bilayers induced in oriented lipid membranes interacting with the antimicrobial peptides, magainin-2 and aurein-3.3. Biochim Biophys Acta 1788:1482–1496CrossRefPubMedGoogle Scholar
  106. Kim EY, Rajasekaran G, Shin SY (2017) LL-37-derived short antimicrobial peptide KR-12-a5 and its d-amino acid substituted analogs with cell selectivity, anti-biofilm activity, synergistic effect with conventional antibiotics, and anti-inflammatory activity. Eur J Med Chem 136:428–441CrossRefPubMedGoogle Scholar
  107. Kindrachuk J, Napper S (2010) Structure-activity relationships of multifunctional host defence peptides. Mini-Rev Med Chem 10:596–614CrossRefPubMedGoogle Scholar
  108. Kiss G, Michl H (1962) Über das Giftsekret der Gelbbauchunke Bombina variegata L. Toxicon (Oxford) 1:33–39CrossRefGoogle Scholar
  109. Klocek G, Seelig J (2008) Melittin interaction with sulfated cell surface sugars. Biochemistry 47:2841–2849CrossRefPubMedGoogle Scholar
  110. Kmiecik S, Gront D, Kolinski M, Wieteska L, Dawid AE, Kolinski A (2016) Coarse-grained protein models and their applications. Chem Rev 116:7898–7936CrossRefPubMedGoogle Scholar
  111. Kobayashi S, Hirakura Y, Matsuzaki K (2001) Bacteria-selective synergism between the antimicrobial peptides alpha-helical magainin 2 and cyclic beta-sheet tachyplesin I: toward cocktail therapy. Biochemistry 40:14330–14335CrossRefPubMedGoogle Scholar
  112. Kollmitzer B, Heftberger P, Rappolt M, Pabst G (2013) Monolayer spontaneous curvature of raft-forming membrane lipids. Soft Matter 9:10877–10884CrossRefPubMedPubMedCentralGoogle Scholar
  113. Kozlowska J, Vermeer LS, Rogers GB, Rehnnuma N, Amos SB, Koller G, McArthur M, Bruce KD, Mason AJ (2014) Combined systems approaches reveal highly plastic responses to antimicrobial peptide challenge in Escherichia coli. PLoS Pathog 10:e1004104CrossRefPubMedPubMedCentralGoogle Scholar
  114. Kuroda K, DeGrado WF (2005) Amphiphilic polymethacrylate derivatives as antimicrobial agents. J Am Chem Soc 127:4128–4129CrossRefPubMedGoogle Scholar
  115. Ladokhin AS, Wimley WC, White SH (1995) Leakage of membrane vesicle contents – determination of mechanisms using fluorescence requenching. Biophys J 69:1964–1971CrossRefPubMedPubMedCentralGoogle Scholar
  116. Laub KR, Witschas K, Blicher A, Madsen SB, Luckhoff A, Heimburg T (2012) Comparing ion conductance recordings of synthetic lipid bilayers with cell membranes containing TRP channels. Biochim Biophys Acta 1818:1123–1134CrossRefPubMedGoogle Scholar
  117. Laurencin M, Simon M, Fleury Y, Baudy-Floc’h M, Bondon A, Legrand B (2018) Selectivity modulation and structure of alpha/aza-beta(3) cyclic antimicrobial peptides. Chemistry 24:6191–6201CrossRefPubMedGoogle Scholar
  118. Lear JD, Wasserman ZR, DeGrado WF (1988) Synthetic amphiphilic peptide models for protein ion channels. Science 240:1177–1181CrossRefPubMedGoogle Scholar
  119. Leber R, Pachler M, Kabelka I, Svoboda I, Enkoller D, Vácha R, Lohner K, Pabst G (2018) Synergism of antimicrobial frog peptides couples to membrane intrinsic curvature strain. Biophys J 114:1945–1954CrossRefPubMedGoogle Scholar
  120. Leitgeb B, Szekeres A, Manczinger L, Vagvolgyi C, Kredics L (2007) The history of alamethicin: a review of the most extensively studied peptaibol. Chem Biodivers 4:1027–1051CrossRefPubMedGoogle Scholar
  121. Liu SP, Zhou L, Lakshminarayanan R, Beuerman RW (2010) Multivalent antimicrobial peptides as therapeutics: design principles and structural diversities. Int J Pept Res Ther 16:199–213CrossRefPubMedPubMedCentralGoogle Scholar
  122. Lohner K (2009) New strategies for novel antibiotics: peptides targeting bacterial cell membranes. Gen Physiol Biophys 28:105–116CrossRefPubMedGoogle Scholar
  123. Lorenzon EN, Santos-Filho NA, Ramos MA, Bauab TM, Camargo IL, Cilli EM (2016) C-terminal lysine-linked magainin 2 with increased activity against multidrug-resistant bacteria. Protein Pept Lett 23:738–747CrossRefPubMedGoogle Scholar
  124. Loudet C, Khemtemourian L, Aussenac F, Gineste S, Achard MF, Dufourc EJ (2005) Bicelle membranes and their use for hydrophobic peptide studies by circular dichroism and solid state NMR. Biochim Biophys Acta 1724:315–323CrossRefPubMedGoogle Scholar
  125. Ludtke SJ, He K, Wu Y, Huang HW (1994) Cooperative membrane insertion of magainin correlated with its cytolytic activity. Biochim Biophys Acta 1190:181–184CrossRefPubMedGoogle Scholar
  126. Ludtke S, He K, Huang H (1995) Membrane thinning caused by magainin 2. Biochemistry 34:16764–16769CrossRefPubMedGoogle Scholar
  127. Ludtke SJ, He K, Heller WT, Harroun TA, Yang L, Huang HW (1996) Membrane pores induced by magainin. Biochemistry 35:13723–13728CrossRefPubMedGoogle Scholar
  128. Maget-Dana R, Peypoux F (1994) Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87:151–174CrossRefPubMedGoogle Scholar
  129. Maget-Dana R, Ptak M (1995) Interactions of surfactin with membrane models. Biophys J 68:1937–1943CrossRefPubMedPubMedCentralGoogle Scholar
  130. Makovitzki A, Baram J, Shai Y (2008) Antimicrobial lipopolypeptides composed of palmitoyl Di- and tricationic peptides: in vitro and in vivo activities, self-assembly to nanostructures, and a plausible mode of action. Biochemistry 47:10630–10636CrossRefPubMedGoogle Scholar
  131. Mangoni ML, Shai Y (2011) Short native antimicrobial peptides and engineered ultrashort lipopeptides: similarities and differences in cell specificities and modes of action. Cell Mol Life Sci 68:2267–2280CrossRefPubMedGoogle Scholar
  132. Marquette A, Bechinger B (2018) Biophysical investigations elucidating the mechanisms of action of antimicrobial peptides and their synergism. Biomol Ther 8:E18Google Scholar
  133. Marquette A, Mason AJ, Bechinger B (2008) Aggregation and membrane permeabilizing properties of designed histidine-containing cationic linear peptide antibiotics. J Pept Sci 14:488–495CrossRefPubMedGoogle Scholar
  134. Marquette A, Lorber B, Bechinger B (2010) Reversible liposome association induced by LAH4: a peptide with potent antimicrobial and nucleic acid transfection activities. Biophys J 98:2544–2553CrossRefPubMedPubMedCentralGoogle Scholar
  135. Marquette A, Salnikov E, Glattard E, Aisenbrey C, Bechinger B (2015) Magainin 2-PGLa interactions in membranes – two peptides that exhibit synergistic enhancement of antimicrobial activity. Curr Top Med Chem 16:65–75CrossRefGoogle Scholar
  136. Mason AJ, Martinez A, Glaubitz C, Danos O, Kichler A, Bechinger B (2006) The antibiotic and DNA-transfecting peptide LAH4 selectively associates with, and disorders, anionic lipids in mixed membranes. FASEB J 20:320–322CrossRefPubMedGoogle Scholar
  137. Mason AJ, Moussaoui W, Abdelrhaman T, Boukhari A, Bertani P, Marquette A, Shooshtarizaheh P, Moulay G, Boehm N, Guerold B, Sawers RJH, Kichler A, Metz-Boutigue MH, Candolfi E, Prevost G, Bechinger B (2009) Structural determinants of antimicrobial and antiplasmodial activity and selectivity in histidine rich amphipathic cationic peptides. J Biol Chem 284:119–133CrossRefPubMedGoogle Scholar
  138. Matos PM, Franquelim HG, Castanho MA, Santos NC (2010) Quantitative assessment of peptide-lipid interactions. Ubiquitous fluorescence methodologies. Biochim Biophys Acta 1798:1999–2012CrossRefPubMedGoogle Scholar
  139. Matsuzaki K (1998) Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim Biophys Acta 1376:391–400CrossRefPubMedGoogle Scholar
  140. Matsuzaki K, Harada M, Funakoshi S, Fujii N, Miyajima K (1991) Physicochemical determinants for the interactions of magainins 1 and 2 with acidic lipid bilayers. Biochim Biophys Acta 1063:162–170CrossRefPubMedGoogle Scholar
  141. Matsuzaki K, Murase O, Tokuda H, Funakoshi S, Fujii N, Miyajima K (1994) Orientational and aggregational states of magainin 2 in phospholipid bilayers. Biochemistry 33:3342–3349CrossRefPubMedGoogle Scholar
  142. Matsuzaki K, Murase O, Fujii N, Miyajima K (1995a) Translocation of a channel-forming antimicrobial peptide, magainin2, across lipid bilayers by forming a pore. Biochemistry 34:6521–6526CrossRefPubMedGoogle Scholar
  143. Matsuzaki K, Murase O, Miyajima K (1995b) Kinetics of pore formation by an antimicrobial peptide, magainin 2, in phospholipid bilayers. Biochemistry 34:12553–12559CrossRefPubMedGoogle Scholar
  144. Matsuzaki K, Murase O, Fujii N, Miyajima K (1996) An antimicrobial peptide, magainin 2, induced flip-flop of phospholipid coupled with pore formation and peptide translocation. Biochemistry 35:11361–11368CrossRefPubMedGoogle Scholar
  145. Matsuzaki K, Mitani Y, Akada K, Murase O, Yoneyama S, Zasloff M, Miyajima K (1998) Mechanism of synergism between antimicrobial peptides magainin 2 and PGLa. Biochemistry 37:15144–15153CrossRefPubMedGoogle Scholar
  146. McCafferty DG, Cudic P, Yu MK, Behenna DC, Kruger R (1999) Synergy and duality in peptide antibiotic mechanisms. Curr Opin Chem Biol 3:672–680CrossRefPubMedGoogle Scholar
  147. Mecke A, Lee DK, Ramamoorthy A, Orr BG, Banaszak Holl MM (2005) Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of MSI-78 in lipid bilayers. Biophys J 89:4043–4050CrossRefPubMedPubMedCentralGoogle Scholar
  148. Medintz IL, Hildebrandt N (2013) Förster resonance energy transfer: from theory to applications. Wiley-VCH, WeinheimCrossRefGoogle Scholar
  149. Michalek M, Aisenbrey C, Bechinger B (2014) Investigation of membrane penetration depth and interactions of the amino-terminal domain of huntingtin: refined analysis by tryptophan fluorescence measurement. Eur Biophys J 43:347–360CrossRefPubMedGoogle Scholar
  150. Miles AJ, Wallace BA (2006) Synchrotron radiation circular dichroism spectroscopy of proteins and applications in structural and functional genomics. Chem Soc Rev 35:39–51CrossRefPubMedGoogle Scholar
  151. Miles AJ, Wallace BA (2016) Circular dichroism spectroscopy of membrane proteins. Chem Soc Rev 45:4859–4872CrossRefPubMedGoogle Scholar
  152. Milov AD, Samoilova RI, Tsvetkov YD, De Zotti M, Formaggio F, Toniolo C, Handgraaf JW, Raap J (2009) Structure of self-aggregated alamethicin in ePC membranes detected by pulsed electron-electron double resonance and electron spin Echo envelope modulation spectroscopies. Biophys J 96:3197–3209CrossRefPubMedPubMedCentralGoogle Scholar
  153. Montal M, Mueller P (1972) Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci U S A 69:3561–3566CrossRefPubMedPubMedCentralGoogle Scholar
  154. Mor A, Hani K, Nicolas P (1994) The vertebrate peptide antibiotics dermaseptins have overlapping structural features but target specific microorganisms. J Biol Chem 269:31635–31641PubMedGoogle Scholar
  155. Naito A, Matsumori N, Ramamoorthy A (2018) Dynamic membrane interactions of antibacterial and antifungal biomolecules, and amyloid peptides, revealed by solid-state NMR spectroscopy. Biochim Biophys Acta 1862:307–323CrossRefGoogle Scholar
  156. Nishida M, Imura Y, Yamamoto M, Kobayashi S, Yano Y, Matsuzaki K (2007) Interaction of a magainin-PGLa hybrid peptide with membranes: insight into the mechanism of synergism. Biochemistry 46:14284–14290CrossRefPubMedGoogle Scholar
  157. North CL, Barranger-Mathys M, Cafiso DS (1995) Membrane orientation of the N-terminal segment of alamethicin determined by solid-state 15 N NMR. Biophys J 69:2392–2397CrossRefPubMedPubMedCentralGoogle Scholar
  158. Otzen DE (2017) Biosurfactants and surfactants interacting with membranes and proteins: same but different? Biochim Biophys Acta 1859:639–649CrossRefGoogle Scholar
  159. Oyston PC, Fox MA, Richards SJ, Clark GC (2009) Novel peptide therapeutics for treatment of infections. J Med Microbiol 58:977–987CrossRefPubMedGoogle Scholar
  160. Palermo EF, Kuroda K (2010) Structural determinants of antimicrobial activity in polymers which mimic host defense peptides. Appl Microbiol Biotechnol 87:1605–1615CrossRefPubMedGoogle Scholar
  161. Patch JA, Barron AE (2003) Helical peptoid mimics of magainin-2 amide. J Am Chem Soc 125:12092–12093CrossRefPubMedGoogle Scholar
  162. Patel H, Tscheka C, Edwards K, Karlsson G, Heerklotz H (2011) All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. Biochim Biophys Acta 1808:2000–2008CrossRefPubMedGoogle Scholar
  163. Patel H, Huynh Q, Barlehner D, Heerklotz H (2014) Additive and synergistic membrane permeabilization by antimicrobial (lipo)peptides and detergents. Biophys J 106:2115–2125CrossRefPubMedPubMedCentralGoogle Scholar
  164. Paterson DJ, Tassieri M, Reboud J, Wilson R, Cooper JM (2017) Lipid topology and electrostatic interactions underpin lytic activity of linear cationic antimicrobial peptides in membranes. Proc Natl Acad Sci U S A 114:E8324–E8332CrossRefPubMedPubMedCentralGoogle Scholar
  165. Payne JE, Dubois AV, Ingram RJ, Weldon S, Taggart CC, Elborn JS, Tunney MM (2017) Activity of innate antimicrobial peptides and ivacaftor against clinical cystic fibrosis respiratory pathogens. Int J Antimicrob Agents 50:427–435CrossRefPubMedGoogle Scholar
  166. Perrone B, Miles AJ, Salnikov ES, Wallace B, Bechinger B (2014) Lipid- interactions of the LAH4, a peptide with antimicrobial and nucleic transfection activities. Eur Biophys J 43:499–507CrossRefPubMedGoogle Scholar
  167. Pino-Angeles A, Leveritt JM 3rd, Lazaridis T (2016) Pore structure and synergy in antimicrobial peptides of the magainin family. PLoS Comput Biol 12:e1004570CrossRefPubMedPubMedCentralGoogle Scholar
  168. Pirtskhalava M, Gabrielian A, Cruz P, Griggs HL, Squires RB, Hurt DE, Grigolava M, Chubinidze M, Gogoladze G, Vishnepolsky B, Alekseyev V, Rosenthal A, Tartakovsky M (2016) DBAASP v.2: an enhanced database of structure and antimicrobial/cytotoxic activity of natural and synthetic peptides. Nucleic Acids Res 44:D1104–D1112CrossRefPubMedGoogle Scholar
  169. Porter EA, Weisblum B, Gellman SH (2002) Mimicry of host-defense peptides by unnatural oligomers: antimicrobial beta-peptides. J Am Chem Soc 124:7324–7330CrossRefPubMedGoogle Scholar
  170. Pouny Y, Rapaport D, Mor A, Nicolas P, Shai Y (1992) Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31:12416–12423CrossRefPubMedGoogle Scholar
  171. Raimondo D, Andreotti G, Saint N, Amodeo P, Renzone G, Sanseverino M, Zocchi I, Molle G, Motta A, Scaloni A (2005) A folding-dependent mechanism of antimicrobial peptide resistance to degradation unveiled by solution structure of distinctin. Proc Natl Acad Sci U S A 102:6309–6314CrossRefPubMedPubMedCentralGoogle Scholar
  172. Ramamoorthy A, Thennarasu S, Lee DK, Tan A, Maloy L (2006) 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 91:206–216CrossRefPubMedPubMedCentralGoogle Scholar
  173. Rangarajan N, Bakshi S, Weisshaar JC (2013) Localized permeabilization of E. coli membranes by the antimicrobial peptide cecropin A. Biochemistry 52:6584–6594CrossRefPubMedGoogle Scholar
  174. Rank LA, Walsh NM, Liu R, Lim FY, Bok JW, Huang M, Keller NP, Gellman SH, Hull CM (2017) A cationic polymer that shows high antifungal activity against diverse human pathogens. Antimicrob Agents Chemother 61:e00204–e00217CrossRefPubMedPubMedCentralGoogle Scholar
  175. Rautenbach M, Troskie AM, Vosloo JA (2016a) Antifungal peptides: to be or not to be membrane active. Biochimie 130:132–145CrossRefPubMedGoogle Scholar
  176. Rautenbach M, Troskie AM, Vosloo JA, Dathe ME (2016b) Antifungal membranolytic activity of the tyrocidines against filamentous plant fungi. Biochimie 130:122–131CrossRefPubMedGoogle Scholar
  177. Reijmar K, Edwards K, Andersson K, Agmo Hernandez V (2016) Characterizing and controlling the loading and release of cationic amphiphilic peptides onto and from PEG-stabilized lipodisks. Langmuir 32:12091–12099CrossRefPubMedGoogle Scholar
  178. Resende JM, Moraes CM, Munhoz VHDO, Aisenbrey C, Verly RM, Bertani P, Cesar A, Pilo-Veloso D, Bechinger B (2009) Membrane structure and conformational changes of the antibiotic heterodimeric peptide distinctin by solid-state NMR spectroscopy. Proc Natl Acad Sci U S A 106:16639–16644CrossRefPubMedPubMedCentralGoogle Scholar
  179. Resende JM, Verly RM, Aisenbrey C, Amary C, Bertani P, Pilo-Veloso D, Bechinger B (2014) Membrane interactions of phylloseptin-1, −2, and −3 peptides by oriented solid-state NMR spectroscopy. Biophys J 107:901–911CrossRefPubMedPubMedCentralGoogle Scholar
  180. Rollins-Smith LA, Doersam JK, Longcore JE, Taylor SK, Shamblin JC, Carey C, Zasloff MA (2002) Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev Comp Immunol 26:63–72CrossRefPubMedGoogle Scholar
  181. Rotem S, Mor A (2009) Antimicrobial peptide mimics for improved therapeutic properties. Biochim Biophys Acta 1788:1582–1592CrossRefPubMedGoogle Scholar
  182. Roversi D, Luca V, Aureli S, Park Y, Mangoni ML, Stella L (2014) How many AMP molecules kill a bacterium? Spectroscopic determination of PMAP-23 binding to E. Coli. ACS Chem Biol 9:2003–2007CrossRefPubMedGoogle Scholar
  183. Russ WP, Engelman DM (2000) The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 296:911–919CrossRefPubMedGoogle Scholar
  184. Sakoulas G, Kumaraswamy M, Kousha A, Nizet V (2017) Interaction of antibiotics with innate host defense factors against Salmonella enterica serotype Newport. mSphere 2:e00410–e00417CrossRefPubMedPubMedCentralGoogle Scholar
  185. Salnikov E, Bechinger B (2011) 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 100:1473–1480CrossRefPubMedPubMedCentralGoogle Scholar
  186. Salnikov ES, Friedrich H, Li X, Bertani P, Reissmann S, Hertweck C, O’Neil JD, Raap J, Bechinger B (2009a) Structure and alignment of the membrane-associated peptaibols ampullosporin A and alamethicin by oriented 15 N and 31 P solid-state NMR spectroscopy. Biophys J 96:86–100CrossRefPubMedGoogle Scholar
  187. Salnikov ES, Mason AJ, Bechinger B (2009b) Membrane order perturbation in the presence of antimicrobial peptides by 2H solid-state NMR spectroscopy. Biochimie 91:734–743CrossRefPubMedGoogle Scholar
  188. Salnikov E, Aisenbrey C, Vidovic V, Bechinger B (2010) Solid-state NMR approaches to measure topological equilibria and dynamics of membrane polypeptides. Biochim Biophys Acta 1798:258–265CrossRefPubMedGoogle Scholar
  189. Salnikov E, Aisenbrey C, Balandin SV, Zhmak MN, Ovchinnikova AY, Bechinger B (2011) Structure and alignment of the membrane-associated antimicrobial peptide arenicin by oriented solid-state NMR spectroscopy. Biochemistry 50:3784–3795CrossRefPubMedGoogle Scholar
  190. Salnikov ES, Aisenbrey C, Aussenac F, Ouari O, Sarrouj H, Reiter C, Tordo P, Engelke F, Bechinger B (2016a) Membrane topologies of the PGLa antimicrobial peptide and a transmembrane anchor sequence by Dynamic Nuclear Polarization/solid-state NMR spectroscopy. Sci Rep 6:20895CrossRefPubMedPubMedCentralGoogle Scholar
  191. Salnikov ES, Raya J, De Zotti M, Zaitseva E, Peggion C, Ballano G, Toniolo C, Raap J, Bechinger B (2016b) Alamethicin supramolecular organization in lipid membranes from 19F solid- state NMR. Biophys J 111:2450–2459CrossRefPubMedPubMedCentralGoogle Scholar
  192. Salnikov ES, Anantharamaiah GM, Bechinger B (2018) Supramolecular organization of apolipoprotein A-I – derived peptides within disc-like arrangements. Biophys J 115:467–477 in pressCrossRefPubMedPubMedCentralGoogle Scholar
  193. Sani MA, Separovic F (2018) Antimicrobial peptide structures: from model membranes to live cells. Chemistry 24:286–291CrossRefPubMedGoogle Scholar
  194. Sansom MSP (1991) The biophysics of peptide models of ion channels. Prog Biophysmol Biol 55:139–235CrossRefGoogle Scholar
  195. Sansom MS (1993) Alamethicin and related peptaibols – model ion channels. Eur Biophys J 22:105–124CrossRefPubMedGoogle Scholar
  196. Scherer PG, Seelig J (1989) Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles. Biochemistry 28:7720–7727CrossRefPubMedGoogle Scholar
  197. Schweizer F (2009) Cationic amphiphilic peptides with cancer-selective toxicity. Eur J Pharmacol 625:190–194CrossRefPubMedGoogle Scholar
  198. Scott RW, DeGrado WF, Tew GN (2008) De novo designed synthetic mimics of antimicrobial peptides. Curr Opin Biotechnol 19:620–627CrossRefPubMedPubMedCentralGoogle Scholar
  199. Seelig J (2004) Thermodynamics of lipid-peptide interactions. Biochim Biophys Acta 1666:40–50CrossRefPubMedGoogle Scholar
  200. Shai Y (1999) Mechanism of the binding, insertion, and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective lytic peptides. Biochim Biophys Acta 1462:55–70CrossRefPubMedGoogle Scholar
  201. Smart M, Rajagopal A, Liu WK, Ha BY (2017) Opposing effects of cationic antimicrobial peptides and divalent cations on bacterial lipopolysaccharides. Phys Rev E 96:042405CrossRefPubMedGoogle Scholar
  202. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252–260CrossRefPubMedGoogle Scholar
  203. Steinstraesser L, Kraneburg U, Jacobsen F, Al-Benna S (2010) Host defense peptides and their antimicrobial-immunomodulatory duality. Immunobiology 216:322–333CrossRefPubMedGoogle Scholar
  204. Strandberg E, Tiltak D, Ehni S, Wadhwani P, Ulrich AS (2012) Lipid shape is a key factor for membrane interactions of amphipathic helical peptides. Biochim Biophys Acta 1818:1764–1776CrossRefPubMedGoogle Scholar
  205. Strandberg E, Zerweck J, Wadhwani P, Ulrich AS (2013) Synergistic insertion of antimicrobial magainin-family peptides in membranes depends on the lipid spontaneous curvature. Biophys J 104:L09–L11Google Scholar
  206. Sychev SV, Sukhanov SV, Panteleev PV, Shenkarev ZO, Ovchinnikova TV (2018) Marine antimicrobial peptide arenicin adopts a monomeric twisted beta-hairpin structure and forms low conductivity pores in zwitterionic lipid bilayers. Pept Science 110:e23093CrossRefGoogle Scholar
  207. Tamba Y, Yamazaki M (2005) Single giant unilamellar vesicle method reveals effect of antimicrobial peptide magainin 2 on membrane permeability. Biochemistry 44:15823–15833CrossRefPubMedGoogle Scholar
  208. Tamba Y, Yamazaki M (2009) Magainin 2-induced pore formation in the lipid membranes depends on its concentration in the membrane interface. J Phys Chem B 113:4846–4852CrossRefPubMedGoogle Scholar
  209. Tamba Y, Ariyama H, Levadny V, Yamazaki M (2010) Kinetic pathway of antimicrobial peptide magainin 2-induced pore formation in lipid membranes. J Phys Chem B 114:12018–12026CrossRefPubMedGoogle Scholar
  210. Tieleman DP, Hess B, Sansom MS (2002) Analysis and evaluation of channel models: simulations of alamethicin. Biophys J 83:2393–2407CrossRefPubMedPubMedCentralGoogle Scholar
  211. Tremouilhac P, Strandberg E, Wadhwani P, Ulrich AS (2006a) Conditions affecting the re-alignment of the antimicrobial peptide PGLa in membranes as monitored by solid state 2H-NMR. Biochim Biophys Acta 1758:1330–1342CrossRefPubMedGoogle Scholar
  212. Tremouilhac P, Strandberg E, Wadhwani P, Ulrich AS (2006b) Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin. J Biol Chem 281:32089–32094CrossRefPubMedGoogle Scholar
  213. Tsutsumi LS, Elmore JM, Dang UT, Wallace MJ, Marreddy R, Lee RB, Tan GT, Hurdle JG, Lee RE, Sun D (2018) Solid-phase synthesis and antibacterial activity of cyclohexapeptide wollamide B analogs. ACS Comb Sci 20:172–185CrossRefPubMedGoogle Scholar
  214. Ulmschneider JP, Smith JC, Ulmschneider MB, Ulrich AS, Strandberg E (2012) Reorientation and dimerization of the membrane-bound antimicrobial peptide PGLa from microsecond all-atom MD simulations. Biophys J 103:472–482CrossRefPubMedPubMedCentralGoogle Scholar
  215. Usachev KS, Kolosova OA, Klochkova EA, Yulmetov AR, Aganov AV, Klochkov VV (2017) Oligomerization of the antimicrobial peptide protegrin-5 in a membrane-mimicking environment. Structural studies by high-resolution NMR spectroscopy. Eur Biophys J 46:293–300CrossRefPubMedGoogle Scholar
  216. Vacha R, Frenkel D (2014) Simulations suggest possible novel membrane pore structure. Langmuir 30:1304–1310CrossRefPubMedGoogle Scholar
  217. Vaz Gomes A, de Waal A, Berden JA, Westerhoff HV (1993) Electric potentiation, cooperativity, and synergism of magainin peptides in protein-free liposomes. Biochemistry 32:5365–5372CrossRefPubMedGoogle Scholar
  218. Verardi R, Traaseth NJ, Shi L, Porcelli F, Monfregola L, De Luca S, Amodeo P, Veglia G, Scaloni A (2011) Probing membrane topology of the antimicrobial peptide distinctin by solid-state NMR spectroscopy in zwitterionic and charged lipid bilayers. Biochim Biophys Acta 1808:34–40CrossRefPubMedGoogle Scholar
  219. Verly RM, Resende JM, Junior EFC, de Magalhães MTC, Guimarães CFCR, Munhoz VHO, Bemquerer MP, Almeida FCL, Santoro MM, Piló-Veloso D, Bechinger B (2017) Structure and membrane interactions of the homodimeric antibiotic peptide homotarsinin. Sci Rep 7:40854CrossRefPubMedPubMedCentralGoogle Scholar
  220. Vermeer LS, Marquette A, Schoup M, Fenard D, Galy A, Bechinger B (2016) Simultaneous analysis of secondary structure and light scattering from circular dichroism titrations: application to vectofusin-1. Sci Rep 6:39450CrossRefPubMedPubMedCentralGoogle Scholar
  221. Violette A, Fournel S, Lamour K, Chaloin O, Frisch B, Briand JP, Monteil H, Guichard G (2006) Mimicking helical antibacterial peptides with nonpeptidic folding oligomers. Chem Biol 13:531–538CrossRefPubMedGoogle Scholar
  222. Visscher KM, Medeiros-Silva J, Mance D, Rodrigues J, Daniels M, Bonvin A, Baldus M, Weingarth M (2017) Supramolecular organization and functional implications of K+ channel clusters in membranes. Angew Chem Int Ed Eng 56:13222–13227CrossRefGoogle Scholar
  223. Vogt TCB, Bechinger B (1999) The interactions of histidine-containing amphipathic helical peptide antibiotics with lipid bilayers: the effects of charges and pH. J Biol Chem 274:29115–29121CrossRefPubMedGoogle Scholar
  224. Voievoda N (2014) Biophysical investigations of the membrane and nucleic acids interactions of the transfection peptide LAH4-L1. PhD thesis, University of Strasbourg PhDGoogle Scholar
  225. Voievoda N, Schulthess T, Bechinger B, Seelig J (2015) Thermodynamic and biophysical analysis of the membrane-association of a histidine-rich peptide with efficient antimicrobial and transfection activities. J Phys Chem B 119:9678–9687CrossRefPubMedGoogle Scholar
  226. Wakamatsu K, Takeda A, Tachi T, Matsuzaki K (2002) Dimer structure of magainin 2 bound to phospholipid vesicles. Biopolymers 64:314–327CrossRefPubMedGoogle Scholar
  227. Wallace BA, Moa B (1984) Circular dichroism analyses of membrane proteins: an examination of differential light scattering and absorption flattening effects in large membrane vesicles and membrane sheets. Anal Biochem 142:317–328CrossRefPubMedGoogle Scholar
  228. Wang G, Li X, Wang Z (2016) APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res 44:D1087–D1093CrossRefPubMedGoogle Scholar
  229. Watanabe H, Kawano R (2016) Channel current analysis for pore-forming properties of an antimicrobial peptide, magainin 1, using the droplet contact method. Anal Sci 32:57–60CrossRefPubMedGoogle Scholar
  230. Wenk M, Seelig J (1998) Magainin 2 amide interaction with lipid membranes: calorimetric detection of peptide binding and pore formation. Biochemistry 37:3909–3916CrossRefPubMedGoogle Scholar
  231. Wenzel M, Chiriac AI, Otto A, Zweytick D, May C, Schumacher C, Gust R, Albada HB, Penkova M, Kramer U, Erdmann R, Metzler-Nolte N, Straus SK, Bremer E, Becher D, Brotz-Oesterhelt H, Sahl HG, Bandow JE (2014) Small cationic antimicrobial peptides delocalize peripheral membrane proteins. Proc Natl Acad Sci USA 111:E1409–E1418CrossRefPubMedGoogle Scholar
  232. Westerhoff HV, Zasloff M, Rosner JL, Hendler RW, de Waal A, Vaz G, Jongsma PM, Riethorst A, Juretic D (1995) Functional synergism of the magainins PGLa and magainin-2 in Escherichia coli, tumor cells and liposomes. Eur J Biochem 228:257–264CrossRefPubMedGoogle Scholar
  233. Wheaten SA, Ablan FD, Spaller BL, Trieu JM, Almeida PF (2013) Translocation of cationic amphipathic peptides across the membranes of pure phospholipid giant vesicles. J Am Chem Soc 135:16517–16525CrossRefPubMedPubMedCentralGoogle Scholar
  234. Wieprecht T, Apostolov O, Beyermann M, Seelig J (1999a) Thermodynamics of the alpha-helix-coil transition of amphipathic peptides in a membrane environment: implications for the peptide-membrane binding equilibrium. J Mol Biol 294:785–794CrossRefPubMedGoogle Scholar
  235. Wieprecht T, Beyermann M, Seelig J (1999b) Binding of antibacterial magainin peptides to electrically neutral membranes: thermodynamics and structure. Biochemistry 38:10377–10378CrossRefPubMedGoogle Scholar
  236. Wieprecht T, Apostolov O, Beyermann M, Seelig J (2000a) Membrane binding and pore formation of the antibacterial peptide PGLa: thermodynamic and mechanistic aspects. Biochemistry 39:442–452CrossRefPubMedGoogle Scholar
  237. Wieprecht T, Apostolov O, Seelig J (2000b) Binding of the antibacterial peptide magainin 2 amide to small and large unilamellar vesicles. Biophys Chem 85:187–198CrossRefPubMedGoogle Scholar
  238. Wieprecht T, Beyermann M, Seelig J (2002) Thermodynamics of the coil-alpha-helix transition of amphipathic peptides in a membrane environment: the role of vesicle curvature. Biophys Chem 96:191–201CrossRefPubMedGoogle Scholar
  239. Wolf J, Aisenbrey C, Harmouche N, Raya J, Bertani P, Voievoda N, Süss R, Bechinger B (2017) pH-dependent membrane interactions of the histidine-rich cell penetrating peptide LAH4-L1. Biophys J 113:1290–1300CrossRefPubMedPubMedCentralGoogle Scholar
  240. Wu Y, Huang HW, Olah GA (1990) Method of oriented circular dichroism. Biophys J 57:797–806CrossRefPubMedPubMedCentralGoogle Scholar
  241. Wu YS, Ngai SC, Goh BH, Chan KG, Lee LH, Chuah LH (2017) Anticancer activities of surfactin and potential application of nanotechnology assisted surfactin delivery. Front Pharmacol 8:761CrossRefPubMedPubMedCentralGoogle Scholar
  242. Yang D, Zou R, Zhu Y, Liu B, Yao D, Jiang J, Wu J, Tian H (2014) Magainin II modified polydiacetylene micelles for cancer therapy. Nanoscale 6:14772–14783CrossRefPubMedGoogle Scholar
  243. Yang Z, Choi H, Weisshaar JC (2018) Melittin-induced permeabilization, re-sealing, and re-permeabilization of E. coli membranes. Biophys J 114:368–379CrossRefPubMedPubMedCentralGoogle Scholar
  244. Yuksel E, Karakecili A (2014) Antibacterial activity on electrospun poly(lactide-co-glycolide) based membranes via magainin II grafting. Mater Sci Eng C Mater Biol Appl 45:510–518CrossRefPubMedGoogle Scholar
  245. Zanin LM, Dos Santos Alvares D, Juliano MA, Pazin WM, Ito AS, Ruggiero Neto J (2013) Interaction of a synthetic antimicrobial peptide with model membrane by fluorescence spectroscopy. Eur Biophys J 42:819–831CrossRefPubMedGoogle Scholar
  246. 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 U S A 84:5449–5453CrossRefPubMedPubMedCentralGoogle Scholar
  247. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395CrossRefPubMedGoogle Scholar
  248. Zerweck J, Strandberg E, Kukharenko O, Reichert J, Burck J, Wadhwani P, Ulrich AS (2017) Molecular mechanism of synergy between the antimicrobial peptides PGLa and magainin 2. Sci Rep 7:13153CrossRefPubMedPubMedCentralGoogle Scholar
  249. Zhao H, Shao D, Jiang C, Shi J, Li Q, Huang Q, Rajoka MSR, Yang H, Jin M (2017) Biological activity of lipopeptides from Bacillus. Appl Microbiol Biotechnol 101:5951–5960CrossRefPubMedGoogle Scholar
  250. Zhao P, Xue Y, Gao W, Li J, Zu X, Fu D, Bai X, Zuo Y, Hu Z, Zhang F (2018) Bacillaceae-derived peptide antibiotics since 2000. Peptides 101:10–16CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Christopher Aisenbrey
    • 1
  • Arnaud Marquette
    • 1
  • Burkhard Bechinger
    • 1
    • 2
    Email author
  1. 1.Université de Strasbourg/CNRS, UMR7177, Institut de ChimieStrasbourgFrance
  2. 2.Faculté de chimieInstitut le BelStrasbourgFrance

Personalised recommendations