Membrane defects enhance the interaction of antimicrobial peptides, aurein 1.2 versus caerin 1.1

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 8, 2013, Pages 1863-1872

  Fernandez, David I ^a   Sani, Marc Antoine ^a   Miles, Andrew J ^b   Wallace, B A ^b   Separovic, Frances ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Antimicrobial peptide; Circular dichroism; Lipid domain; Model membrane; Peptide lipid interaction; Solid state NMR

Indexed keywords

AUREIN; CAERIN; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; PHOSPHORUS 31; POLYPEPTIDE ANTIBIOTIC AGENT; PROTON; UNCLASSIFIED DRUG; WATER;

ALPHA HELIX; ARTICLE; CHEMICAL INTERACTION; CIRCULAR DICHROISM; LIPID BILAYER; MEMBRANE PERMEABILITY; PHASE TRANSITION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSITION TEMPERATURE;

ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CIRCULAR DICHROISM; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE FRAGMENTS; PHASE TRANSITION; SEX ATTRACTANTS;

EID: 84877011622     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.03.010     Document Type: Article

References (59)

1. M.A. Apponyi, T.L. Pukala, C.S. Brinkworth, V.M. Meselli, J.H. Bowie, M.J. Tyler, G.W. Booker, J. Wallace, J.A. Carver, F. Separovic, J. Doyle, and L.E. Llewellyn Host defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance Peptides 25 2004 1035
2. T. Rozek, R.J. Waugh, S.T. Steinborner, J.H. Bowie, M.J. Tyler, and J.C. Wallace The maculatin peptides from the skin glands of the tree frog Litoria genimaculata: a comparison of the structures and antibacterial activities of maculatin 1.1 and caerin 1.1 J. Pept. Sci. 4 1998 111 115 (Pubitemid 128543157)
3. T.K. Rozek, L. Wegener, J.H. Bowie, I.N. Olver, J.A. Carver, J.C. Wallace, and M.J. Tyler The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. The solution structure of aurein 1.2 Eur. J. Biochem. 267 2000 5330 5341
4. D.J.M. Stone, J.H. Bowie, M.J. Tyler, and J.C. Wallace The structure of caerin 1.1, a novel antibiotic peptide from Australian tree frogs J. Chem. Soc. Chem. Commun. 1992 1224 1225
5. H. Wong, J.H. Bowie, and J.A. Carver The solution structure and activity of caerin 1.1, an antimicrobial peptide from the Australian green tree frog, Litoria splendida Eur. J. Biochem. 247 1997 545 557 (Pubitemid 27308633)
6. D.I. Fernandez, J.D. Gehman, and F. Separovic Membrane interactions of antimicrobial peptides from Australian frogs Biochim. Biophys. Acta 1788 2009 1630 1638
7. I. Marcotte, K.L. Wegener, Y.-H. Lam, B.C.S. Chia, M.R.R.d. Planque, J.H. Bowie, M. Auger, and F. Separovic Interaction of antimicrobial peptides from Australian amphibians with lipid membranes Chem. Phys. Lipids 122 2003 107 120 (Pubitemid 36207516)
8. K.L. Wegener, J.A. Carver, and J.H. Bowie The solution structures and activity of caerin 1.1 and caerin 1.4 in aqueous trifluoroethanol and dodecylphosphocholine micelles Biopolymers 69 2003 42 59 (Pubitemid 36547055)
9. S.R. Dennison, F. Harris, and D.A. Phoenix The interactions of aurein 1.2 with cancer cell membranes Biophys. Chem. 127 2007 78 83
10. S.E. VanCompernolle, R.J. Taylor, K.O. Richter, J. Jiang, B.E. Youree, J.H. Bowie, M.J. Tyler, J.M. Conlon, D. Wade, C. Aiken, T.S. Dermody, V.N. KewelRamani, L.A. Rollins-Smith, and D. Unutmaz Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells J. Virol. 79 2005 11598 11606 (Pubitemid 41279278)
11. G. Wang, K.M. Watson, A. Peterkofsky, and R.W. Buckheit Jr. Identification of novel human immunodeficiency virus type 1-inhibitory peptides based on the antimicrobial peptide database Antimicrob. Agents Chemother. 54 2010 1343 1346
12. E.E. Ambroggio, F. Separovic, J.H. Bowie, G.D. Fidelio, and L.A. Bagatolli Direct visualisation of membrane leakage induced by the antibiotic peptides: maculatin, citropin, and aurein Biophys. J. 89 2005 1874 1881 (Pubitemid 41233542)
13. M.S. Balla, J.H. Bowie, and F. Separovic Solid-state NMR study of antimicrobial peptides from Australian frogs in phospholipid membranes Eur. Biophys. J. Biophys. Lett. 33 2004 109 116 (Pubitemid 38987097)
14. M. Boland, and F. Separovic Membrane interactions of antimicrobial peptides from Australian tree frogs Biochim. Biophys. Acta 1758 2006 1178 1183 (Pubitemid 44436071)
15. G.W.J. Seto, S. Marwaha, D.M. Kobewka, R.N.A.H. Lewis, F. Separovic, and R.N. McElhaney Interactions of the Australian tree frog antimicrobial peptides aurein 1.2, citropin 1.1 and maculatin 1.1 with lipid model membranes: diferential scanning calorimetric and Fourier transform infrared spectroscopic studies Biochim. Biophys. Acta 1768 2007 2787 2800 (Pubitemid 350060869)
16. Z. Oren, and Y. Shai Mode of action of linear amphipathic α-helical antimicrobial peptides Biopolymers (Pept. Sci.) 47 1999 451 463
17. Y. Shai Mechanism of the binding, insertion and destabilisation of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane lytic peptides Biochim. Biophys. Acta 1462 1999 55 70
18. Y. Shai, and Z. Oren From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides Peptides 22 2001 1629 1641 (Pubitemid 32918242)
19. L. Yang, T.A. Harroun, T.M. Weiss, L. Ding, and H.W. Huang Barrel-stave model or toroidal model? A case study on melittin pores Biophys. J. 81 2001 1475 1485 (Pubitemid 32783588)
20. Y. Shai Mode of action of membrane active antimicrobial peptides Biopolymers 66 2002 236 248 (Pubitemid 36098316)
21. D.I. Fernandez, A.P.L. Brun, T.C. Whitwell, M.-A. Sani, M. James, and F. Separovic The antimicrobial peptide aurein 1.2 disrupts model membranes via the carpet mechanism Phys. Chem. Chem. Phys. 14 2012 15739 15751
22. K.N. Hall, H. Mozsolits, and M.-I. Aguilar Surface plasmon resonance analysis of antimicrobial peptide-membrane interactions: affinity & mechanism of action Lett. Pept. Sci. 10 2003 475 485 (Pubitemid 40379038)
23. A.I.P.M. de Kroot Metabolism of phosphatidylcholine and its implications for lipid acyl chain composition in Saccharomyces cerevisiae Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1771 2007 343 352
24. F.D. Gunstone, and J.L. Harwood Occurrence and characterisation of oils and fats F.D. Gunstone, J.L. Harwood, A.J. Dijkstra, The Lipids Handbook 2007 CRC Press, Taylor and Francis Group 37 141
25. D.E. Warschawski, A.A. Arnold, M. Beaugrand, A. Gravel, É. Chartrand, and I. Marcotte Choosing membrane mimetics for NMR structural studies of transmembrane proteins Biochim. Biophys. Acta 1808 2011 1957 1974
26. D.I. Fernandez, T.-H. Lee, M.-A. Sani, M.-I. Aguilar, and F. Separovic Proline facilitates the membrane insertion of the antimicrobial peptide maculatin 1.1 via surface indentation and subsequent lipid disordering Biophys. J. 2013 10.1016/j.bpj.2013.01.059 (in press)
27. 31P solid-state NMR spectroscopy study Biochim. Biophys. Acta 1712 2005 101 108 (Pubitemid 40799285)
28. B. Bechinger, and K. Lohner Detergent-like actions of linear amphipathic cationic antimicrobial peptides Biochim. Biophys. Acta 1758 2006 1529 1539 (Pubitemid 44436087)
29. T. Pott, J. Dufourcq, and E.J. Dufourcq Fluid or gel phase lipid bilayers to study peptide-membrane interactions? Eur. Biophys. J. 25 1996 55 59 (Pubitemid 26345003)
30. F. Dupuy, and R. Morero Microcin J25 membrane interaction: selectivity towards gel phase Biochim. Biophys. Acta 1808 2011 1764 1771
31. C.E. Dempsey, and B. Sternberg Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14] melittin Biochim. Biophys. Acta 1061 1991 175 184
32. E.J. Dufourc, I.C.P. Smith, and J. Dufourcq Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR Biochemistry 25 1986 6448 6455 (Pubitemid 17217892)
33. 31P-NMR study Biophys. J. 68 1995 965 977
34. M. Kranenburg, and B. Smit Phase behavior of model lipid bilayers J. Phys. Chem. B 109 2005 6553 6563 (Pubitemid 40538422)
35. D. Ruppel, H.-G. Kapitza, H.J. Galla, F. Sixl, and E. Sackmann On the microstructure and phase diagram of dimyristoylphosphatidylcholine-glycophorin bilayers Biochim. Biophys. Acta 692 1982 1 17
36. A. Mechler, S. Praporski, K. Atmuri, M. Boland, F. Separovic, and L.L. Martin Specific and selective peptide-membrane interactions revealed using quartz crystal microbalance Biophys. J. 93 2007 3907 3916 (Pubitemid 350223808)
37. T.-H. Lee, C. Heng, M.J. Swann, J.D. Gehman, F. Separovic, and M.-I. Aguilar Real-time quantitative analysis of lipid disordering by aurein 1.2 during membrane adsorption, destabilisation and lysis Biochim. Biophys. Acta 1798 2010 1977 1986
38. J.D. Gehman, F. Luc, K. Hall, T.-H. Lee, M.P. Boland, T.L. Pukala, J.H. Bowie, M.I. Aguilar, and F. Separovic Effect of antimicrobial peptides from Australian tree frogs on anionic phospholipid membranes Biochemistry 47 2008 8557 8565
39. M.-A. Sani, C. Loudet, G. Grobner, and E.J. Dufourc Pro-apoptotic Bax-α 1 synthesis and evidence for β-sheet to α-helix conformational change as triggered by negatively charged lipid membranes J. Pept. Sci. 13 2007 100 106 (Pubitemid 46290946)
40. M.H. Levitt Composite pulses Prog. Nucl. Magn. Reson. Spectrosc. 18 1986 61 122
41. J.H. Davis, M. Bloom, K.W. Butler, and I.C. Smith The temperature dependence of molecular order and the influence of cholesterol in Acholeplasma laidlawii membranes Biochim. Biophys. Acta 597 1980 477 491 (Pubitemid 10054146)
42. M. Rance, and R.A. Byrd Obtaining high-fidelity spin 1/2 powder spectra in anisotropic media: phase-cycled Hahn echo spectroscopy J. Magn. Reson. 52 1983 221 240
43. D.I. Fernandez, M.-A. Sani, and F. Separovic Interactions of the antimicrobial peptide maculatin 1.1 and analogues with phospholipid bilayers Aust. J. Chem. 64 2011 798 805
44. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
45. A. Abdul-Gader, A.J. Miles, and B.A. Wallace A reference dataset for the analyses of membrane protein secondary structures and transmembrane residues using circular dichroism spectroscopy Bioinformatics 27 2011 1630 1636
46. N. Sreerama, and R.W. Woody Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287 2000 252 260 (Pubitemid 32006234)
47. A.J. Miles, L. Whitmore, and B.A. Wallace Spectral magnitude effects on the analyses of secondary structure from circular dichroism spectroscopic data Protein Sci. 14 2005 368 374 (Pubitemid 40194588)
48. J.R. Silvius Thermotropic phase transitions of pure lipids in model membranes and their modifications by membrane proteins Lipid-Protein Interactions 1982 John Wiley & Sons New York
49. J. Seelig, and W. Niederberger Deuterium-labelled lipids as structural probes in liquid crystalline bilayers. A deuterium magnetic resonance study J. Am. Chem. Soc. 96 1974 2069 2072
50. P.R. Cullis, and B.d. Kruijff Lipid polymorphism and the functional roles of lipids in biological membranes Biochim. Biophys. Acta 559 1979 399 420
51. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes Biochim. Biophys. Acta 515 1978 105 140 (Pubitemid 8398025)
52. P.J. Sherman, R.J. Jackway, J.D. Gehman, S. Praporski, G.A. McCubbin, A. Mechler, L.L. Martin, F. Separovic, and J.H. Bowie The solution structure and membrane interations of the antimicrobial peptide fallaxidin 4.2: an NMR and QCM study Biochemistry 48 2009 11892 11901
53. D.I. Fernandez, M.-A. Sani, J.D. Gehman, K.-S. Hahm, and F. Separovic Interactions of a synthetic Leu-Lys-rich antimicrobial peptide with phospholipid bilayers Eur. Biophys. J. Biophys. Lett. 40 2011 471 480
54. J.F. Nagle, and S. Tristram-Nagle Structure of lipid bilayers Biochim. Biophys. Acta Rev. Biomembr. 1469 2000 159 195
55. M.-A. Sani, T.C. Whitwell, and F. Separovic Lipid composition regulates the conformation and insertion of the antimicrobial peptide maculatin 1.1 Biochim. Biophys. Acta Biomembr. 1818 2012 205 211
56. 2H-NMR studies Biophys. J. 71 1996 3320 3329 (Pubitemid 26422373)
57. 2H nuclear magnetic resonance and differential scanning calorimetry Biochemistry 29 1990 451 464 (Pubitemid 20037653)
58. P.G. Scherer, and J. Seelig Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles Biochemistry 28 1989 7720 7728
59. K.A. Henzler-Wildman, G.V. Martinez, M.F. Brown, and A. Ramamoorthy Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37 Biochemistry 43 2004 8459 8469 (Pubitemid 38902524)