Evidence of pores and thinned lipid bilayers induced in oriented lipid membranes interacting with the antimicrobial peptides, magainin-2 and aurein-3.3

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 7, 2009, Pages 1482-1496

  Kim, Chul ^a   Spano, Justin ^a   Park, Eun Kyung ^a   Wi, Sungsool ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

31P and 2H solid state NMR; Antimicrobial peptide; Aurein 3.3; Elliptic toroidal pore; Lateral diffusion; Lipid bilayer; Magainin 2; Thinned membrane bilayer

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; AUREIN 3.3; MAGAININ 2; PHOSPHOLIPID; PHOSPHORUS 31; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; ANTIMICROBIAL CATIONIC PEPTIDE; AUREIN 3.3 PEPTIDE; CHOLESTEROL; MAGAININ 2 PEPTIDE, XENOPUS; PHOSPHATIDYLCHOLINE; XENOPUS PROTEIN;

ANISOTROPY; ARTICLE; CALCULATION; DIFFUSION COEFFICIENT; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE DAMAGE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; POROSITY;

ANISOTROPY; ANTIMICROBIAL CATIONIC PEPTIDES; CHOLESTEROL; LIPID BILAYERS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLCHOLINES; POROSITY; XENOPUS PROTEINS;

EID: 68149136602     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.04.017     Document Type: Article

References (83)

1. Papagianni M. Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol. Adv. 21 (2003) 465-499
2. Bachere E. Anti-infectious immune effectors in marine invertebrates: potential tools for disease control in larviculture. Aquaculture 227 (2003) 427-438
3. Thomma B.P., Cammue B.P., and Thevissen K. Mode of action of plant defensins suggests therapeutic potential. Curr. Drug Target Infect. Disord. 3 (2003) 1-8
4. Hancock R.E., and Lehrer R. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16 (1998) 82-88
5. Rozek T., Bowie J.H., Wallace J.C., and Tyler M.J. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. Part 2. Sequence determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 14 (2000) 2002-2011
6. Cole A.M. Antimicrobial peptide microbicides targeting HIV. Protein and Peptide Lett. 12 (2005) 41-47
7. Conlon J.M. The therapeutic potential of antimicrobial peptides from frog skin. Rev. in Medical Microbiol. 15 (2004) 17-25
8. Yount N.Y., and Yeaman M.R. Immunocontinuum: perspectives in antimicrobial peptide mechanisms of action and resistance. Protein and Peptide Lett. 12 (2005) 49-67
9. Rozek T., Wegener K.L., Bowie J.H., Olver N., Carver J.A., Wallace J.C., and Tyler M.J. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. Eur. J. Biochem. 267 (2000) 5330-5341
10. Hoskin D.W., and Ramamoorthy A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 1778 (2008) 357-375
11. Saberwal G., and Nagaraj R. Cell-lytic and antibacterial peptides that act by perturbing the barrier function of membranes: facets of their conformational features, structure-function correlations and membrane perturbing abilities. Biochim. Biophys. Acta 1197 (1994) 109-131
12. Hancock R.E.W., Falla T., and Brown M.H. Cationic bactericidal peptides. Adv. Microb. Physiol. 37 (1995) 135-175
13. Nicolas P., and Mor A. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 49 (1995) 277-304
14. Nissen-Meyer J., and Nes I.F. Ribosomally synthesized antimicrobial peptides: their function, structure, biogenesis, and mechanism of action. Arch. Microbiol., Arch. Microbiol. 167 (1997) 67-77
15. Edgerton M., Koshlukova S.E., Lo T.E., Chrzan B.G., Straubinger R.M., and Raj P.A. Candidacidal activity of salivary histatins. Identification of a histatin 5-binding protein on Candida albicans. J. Biol. Chem. 273 (1998) 20438-20447
16. Teuber M., and Bader J. Action of polymyxin B on bacterial membranes. Binding capacities for polymyxin B of inner and outer membranes isolated from Salmonella typhimurium G30. Arch. Microbiol. 109 (1976) 51-58
17. Hwang P.M., and Vogel H.J. Structure-function relationships of antimicrobial peptides. Biochem. Cell Biol. 76 (1998) 235-246
18. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1376 (1998) 391-400
19. Matsuzaki K., Sugishita K., Ishibe N., Ueha M., Nakata S., Miyajima K., and Epand R.M. Relationship of membrane curvature to the formation of pores by magainin-2. Biochemistry 37 (1998) 11856-11863
20. Chen F., Lee M., and Huang H.W. Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys. J. 84 (2003) 3751-3758
21. Bechinger B. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462 (1999) 157-183
22. Pouny Y., Rapaport D., Mor A., Nicolas P., and Shai Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31 (1992) 12416-12423
23. Mazzuca C., Stella L., Venanzi M., Formaggio F., Toniolo C., and Pispisa B. Mechanism of membrane activity of the antibiotic trichogin GA IV: a two-state transition controlled by peptide concentration. Biophys. J. 88 (2005) 3411-3421
24. Heller W.T., Waring A.J., Lehrer R.I., and Huang H.W. Multiple states of b-sheet peptide protegrin in lipid bilayers. Biochemistry 37 (1998) 17331-17338
25. He K., Ludtke S.J., and Huang H.W. Antimicrobial peptide pores in membranes detected by neutron in-plane scattering. Biochemistry 34 (1995) 15614-15618
26. Wu Y., He K., Ludtke S.J., and Huang H.W. X-ray diffraction study of lipid bilayer membranes interacting with amphiphilic helical peptides: diphytanoyl phosphatidylcholine with alamethicin at low concentrations. Biophys. J. 68 (1995) 2361-2369
27. Glaser, C. R.W.S., Durr U.H.N., Wadhwani P., Afonin S., Strandberg E., and Ulrich A.S. Concentration-dependent realignment of the antimicrobial peptide PGLa in lipid membranes observed by solid-state 19F-NMR. Biophys. J. 88 (2005) 3392-3397
28. Afonin S., Grage S.L., Ieronimo M., Wadhwani P., and Ulrich A.S. Temperature-dependent transmembrane insertion of the amphiphilic peptide PGLa in lipid bilayers observed by solid state 19F NMR spectroscopy. J. Am. Chem. Soc. 130 (2008) 16512-16514
29. Strandberg E., Kanithasen N., Tiltak D., Burck J., Wadhwani P., Zwernemann O., and Ulrich A.S. Solid-state NMR analysis comparing the designer-made antibiotic MSI-103 with its parent peptide PGLa in lipid bilayers. Biochemistry 47 (2008) 2601-2616
30. Tremouilhac P., Strandberg E., Wadhwani P., and Ulrich A.S. Conditions affecting the re-alignment of the antimicrobial peptide PGLa in membranes as monitored by solid state 2H-NMR. Biochim. Biophys. Acta, Biomembr. 1758 (2006) 1330-1342
31. Wadhwani P., Burck J., Strandberg E., Mink C., Afonin S., and Ulrich A.S. Using a sterically restrictive amino acid as a 19F NMR label to monitor and to control peptide aggregation in membranes. J. Am. Chem. Soc. 130 (2008) 16515-16517
32. He K., Ludtke S.J., Heller W.T., and Huang H.W. Mechanism of alamethicin insertion into lipid bilayers. Biophys. J. 71 (1996) 2669-2679
33. Ramamoorthy A., Thennarasu S., Lee D.-K., Tan A., and Maloy L. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophysical Journal 91 (2006) 206-216
34. Thennarasu S., Lee D.-K., Tan A., Prasad Kari U., and Ramamoorthy A. Antimicrobial activity and membrane selective interactions of a synthetic lipopeptide MSI-843. Biochimica et Biophysica Acta, Biomembranes 1711 (2005) 49-58
35. Porcelli F., Buck B., Lee D.-K., Hallock K.J., Ramamoorthy A., and Veglia G. Structure and orientation of pardaxin determined by NMR experiments in model membranes. J. Biol. Chem. 279 (2004) 45815-45823
36. Zasloff M. 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 (1987) 5449-5453
37. Apponyi M.A., Pukala T.L., Brinkworth C.S., Maselli M., Bowie J.H., Tyler M.J., Booker G.W., Wallace J.C., Carver J.A., Separovic F., Doyle J., and Llewellyn L.E. Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25 (2004) 1035-1054
38. Pan Y.-L., Cheng J.T.-J., Hale J., Pan J., Hancock R.E., and Strauss S.K. Characterization of the structure and membrane interaction of the antimicrobial peptides aurein 2.2 and 2.3 from Australian Southern Bell Frogs. Biophys. J. 92 (2007) 2854-2864
39. Marcotte I., Wegener K.L., Lam Y.-H., Chia B.C.S., de Planque M.R.R., Bowie J.H., Auger M., and Separovic F. Interaction of antimicrobial peptides from Australian amphibians with lipid membranes. Chem. Phys. Lipids 122 (2003) 107-120
40. Hirsh D.J., Hammer J., Maloy L., Blazyk J., and Schaefer J. Secondary structure and location of a magainin analogue in synthetic phospholipid bilayers. Biochemistry 35 (1996) 12733-12741
41. Bechinger B., Zasloff M., and Opella S.J. Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear-magnetic-resonance spectroscopy. Protein Sci. 2 (1993) 2077-2084
42. Bechinger B., Gierasch L.M., Montal M., Zasloff M., and Opella S.J. Orientations of Helical Peptides in Membrane Bilayers by Solid State NMR Spectroscopy Solid State Nucl. Magn. Reson. 7 (1996) 185-191
43. 2H solid-state NMR study. J. Phys. Chem. B 112 (2008) 11402-11414
44. Cornell B.A., Separovic F., Baldassi A.J., and Smith R. Conformation and orientation of gramicidin A in oriented phospholipid bilayers measured by solid state carbon-13 NMR. Biophys. J. 53 (1988) 67-76
45. Hallock K.J.L. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys. J. 84 (2003) 3052-3060
46. Yamaguchi S., Hong T., Waring A., Lehrer R.I., and Hong M. Solid-State NMR investigations of peptide-lipid interaction and orientation of a b-sheet antimicrobial peptide, protegrin. Biochemistry 41 (2002) 9852-9862
47. Buffy J.J., McCormick M.J., Wi S., Waring A., Lehrer R.I., and Hong M. Solid-state NMR investigation of the selective perturbation of lipid bilayers by the cyclic antimicrobial peptide RTD-1. Biochemistry 43 (2004) 9800-9812
48. Yamaguchi S., Huster D., Waring A., Lehrer R.I., Kearney W., Tack B.F., and Hong M. Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR spectroscopy. Biophys. J. 81 (2001) 2203-2214
49. Yang L., Weiss T.M., Lehrer R.I., and Huang H.W. Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys. J. 79 (2000) 2002-2009
50. Butterworth J. Spin echoes in solids. Proc. Phys. Soc. 86 (1965) 297-304
51. Fenske D.B., and Jarrell H.C. Phosphorus-31 two-dimensional solid-state exchange NMR. Biophys. J. 59 (1991) 55-69
52. Auger M., Smith I.C., and Jarrell H.C. Slow motions in lipid bilayers. Direct detection by two-dimensional solid-state deuterium nuclear magnetic resonance. Biophys. J. 59 (1991) 31-38
53. Macquaire F., and Bloom M. Membrane curvature studied using two-dimensional NMR in fluid lipid bilayers. Phys. Rev. E 51 (1995) 4735-4742
54. Dolainsky C., Unger M., Bloom M., and Bayerl T.M. Two-dimensional exchange 2H NMR experiments of phospholipid bilayers on a spherical solid support. Phys. Rev. E 51 (1995)
55. 31P exchange NMR. J. Phys. Chem. B 109 (2005) 22036-22044
56. D.G. Gorenstein. Academic Press, Orlando, FL 1984.
57. Pouny Y., Rapaport D., Mor A., Nicolas P., and Shai Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogs with phospholipid membranes. Biochemistry 31 (1992) 12416-12423
58. Mecke A., Lee D.-K., Ramamoorthy A., Orr B.G., and Holl M.M.B. Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of MSI-78 in lipid bilayers. Biophys. J. 89 (2005) 4043-4050
59. Janshoff A., Bong D.A., Steinem C., Johnson J.E., and Ghadiri M.R. An animal virus-derived peptide switches membrane morphology: possible relevance to nodaviral transfection processes. Biochemistry 38 (1999) 5328-5336
60. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochimica et Biophysica Acta, Reviews on Biomembranes 1376 (1998) 391-400
61. Dolainsky C., Karakatsanis P., and Bayerl T.M. Lipid domains as obstacles for lateral diffusion in supported bilayers probed at different time and length scales by two-dimensional exchange and field gradient solid state NMR. Phys. Rev. E 55 (1997) 4512-4521
62. Kaplan J.I., and Fraenkel G. NMR of Chemically Exchanging Systems (1980), Academic Press, New York
63. L.M. Jackman and F.A. Cotton. Academic Press, New York 1975.
64. Yang L., Harroun T.A., Weiss T.M., Ding L., and Huang H.W. Barrel-stave model or toroidal model? A case study on mellitin pores. Biophys. J. 81 (2001) 1475-1485
65. Matsuzaki K., Sugishita K., Harada M., Fujii N., and Miyajima K. Interactions of an antimicrobial peptide, magainin 2, with outer and innner membranes of Gram-negative bacteria. Biochim. Biophys. Acta 1327 (1997) 119-130
66. Matsuzaki K., Sugishita K.-i., Ishibe N., Ueha M., Nakata S., Miyajima K., and Epand R.M. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37 (1998) 11856-11863
67. Moll F.I., and Cross T.A. Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D. Biophys. J. 57 (1990) 351-362
68. Yamaguchi S., Hong T., Waring A., Lehrer R.I., and Hong M. Solid-state NMR investigations of peptide-lipid interaction and orientation of a beta-sheet. Antimicrobial Peptide, Protegrin., Biochemistry 41 (2002) 9852-9862
69. Yamaguchi S., Huster D., Waring A., Lehrer R.I., Tack B.F., Kearney W., and Hong M. Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR. Biophys. J. 81 (2001) 2203-2214
70. Sternin E., Fine B., Bloom M., Tilcock C.P., Wong K.F., and Cullis P.R. Acyl chain orientational order in the hexagonal HII phase of phospholipid-water dispersions. Biophys. J. 54 (1988) 689-694
71. Christensen B., Fink J., Merrifield R.B., and Mauzerall D. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 5072-5076
72. Nagle J.F. Area/lipid of bilayers from NMR. Biophys. J. 64 (1993) 1476-1481
73. Yeagle P.L., Albert A.D., Boesze-Battaglia K., Young J., and Frye J. Cholesterol dynamics in membranes. Biophys. J. 57 (1990) 413-424
74. Kessel A., Ben-Tal N., and May S. Interactions of cholesterol with lipid bilayers: the preferred configuration and fluctuations. Biophys. J. 81 (2001) 643-658
75. Mateo C.R., Acuna A.U., and Brochon J.-C. Liquid-crystalline phases of cholesterol/lipid bilayers as revealed by the fluorescence of trans-parinaric acid. Biophys. J. 68 (1995) 978-987
76. Segrest J.P., De Loof H., Dohlman J.G., Brouillette C.G., and Anantharamaiah G.M. Amphipathic helix motif: classes and properties. Proteins: Struct., Funct., and Genet. 8 (1990) 103-117
77. Matsuzaki K., Nakamura A., Murase O., Sugishita K.-i., Fujii N., and Miyajima K. Modulation of Magainin 2-Lipid Bilayer Interactions by Peptide Charge. Biochemistry 36 (1997) 2104-2111
78. D.I. Fernandez, J.D. Gehman, F. Separovic, Membrane interactions of antimicrobial peptides from Australian frogs, Biochim. Biophys. Acta, Biomembr. (2008) in press, doi:10.1016/j.bbamem.2008.10.007.
79. Gennis R.B. Biomembranes: Molecular Structure and Function (1989), Springer, New York
80. De Angelis A.A., Nevzorov A.A., Park S.H., Howell S.C., Mrse A.A., and Opella S.J. High-resolution NMR spectroscopy of membrane proteins in aligned bicelles. J. Am. Chem. Soc. 126 (2004) 15340-15341
81. Saxton M.J. Lateral diffusion in an archipelago. The effect of mobile obstacles. Biophys. J. 52 (1987) 989-997
82. Eisinger J., Flores J., and Petersen W.P. A milling crowd model for local and long-range obstructed lateral diffusion. Mobility of excimeric probes in the membrane of intact erythrocytes 49 (1986) 987-1001
83. Lindblom G., Orädd G., Rilfors L., and Morein S. Regulation of lipid composition in Acholeplasma laidlawii and Escherichia coli membranes: NMR studies of lipid lateral diffusion at different growth temperatures. Biochemistry 41 (2002) 11512-11515