Membrane selectivity and biophysical studies of the antimicrobial peptide GL13K

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 9, 2013, Pages 2193-2203

  Balhara, Vinod ^a   Schmidt, Rolf ^a   Gorr, Sven Ulrik ^b   Dewolf, Christine ^a  

^a Gina Cody School of Engineering and Computer Science   (Canada)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Antimicrobial peptide; Dual polarization interferometry; Isothermal titration calorimetry; Membrane disruption; Model membrane; Supported lipid bilayer: atomic force microscopy

Indexed keywords

DIOLEOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLGLYCEROL; GL13K; LIPOSOME; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; 1,2 DIOLEOYL SN GLYCERO 3 PHOSPHOGLYCEROL; 1,2 OLEOYLPHOSPHATIDYLCHOLINE; 1,2-DIOLEOYL-SN-GLYCERO-3-PHOSPHOGLYCEROL; 1,2-OLEOYLPHOSPHATIDYLCHOLINE; ANTIMICROBIAL CATIONIC PEPTIDE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL MEMBRANE; BETA SHEET; BINDING AFFINITY; BIOPHYSICS; CALORIMETRY; CHEMICAL INTERACTION; CIRCULAR DICHROISM; DRUG STRUCTURE; ENTHALPY; ENTROPY; INTERFEROMETRY; LIGHT SCATTERING; LIPID BILAYER; MATHEMATICAL ANALYSIS; MEMBRANE BINDING; MICELLIZATION; PRIORITY JOURNAL; AMPS; ANTIMICROBIAL PEPTIDES; ARTIFICIAL MEMBRANE; CHEMISTRY; DPI; DUAL POLARIZATION INTERFEROMETRY; H-PSP; HUMAN PAROTID SECRETORY PROTEIN; ISOTHERMAL TITRATION CALORIMETRY; MEMBRANE DAMAGE; P/L; PEPTIDE/LIPID RATIO; PROTEIN SECONDARY STRUCTURE; SUPPORTED LIPID BILAYER: ATOMIC FORCE MICROSCOPY; TE; TM; TRANSVERSE ELECTRIC PHASE; TRANSVERSE MAGNETIC PHASE;

BACTERIA (MICROORGANISMS);

AMPS; ANTIMICROBIAL PEPTIDE; ANTIMICROBIAL PEPTIDES; DPI; DUAL POLARIZATION INTERFEROMETRY; H-PSP; HUMAN PAROTID SECRETORY PROTEIN; ISOTHERMAL TITRATION CALORIMETRY; MEMBRANE DISRUPTION; MODEL MEMBRANE; P/L; PEPTIDE/LIPID RATIO; SUPPORTED LIPID BILAYER: ATOMIC FORCE MICROSCOPY; TE; TM; TRANSVERSE ELECTRIC PHASE; TRANSVERSE MAGNETIC PHASE;

ANTIMICROBIAL CATIONIC PEPTIDES; CIRCULAR DICHROISM; LIPID BILAYERS; LIPOSOMES; MICROSCOPY, ATOMIC FORCE; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PROTEIN STRUCTURE, SECONDARY;

EID: 84879473115     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.05.027     Document Type: Article

References (78)

1. T. Abraham, R.N.A.H. Lewis, R.S. Hodges, and R.N. McElhaney Isothermal titration calorimetry studies of the binding of the antimicrobial peptide gramicidin S to phospholipid bilayer membranes Biochemistry 44 2005 11279 11285 (Pubitemid 41209063)
2. V.V. Andrushchenko, H.J. Vogel, and E.J. Prenner Solvent-dependent structure of two tryptophan-rich antimicrobial peptides and their analogs studied by FTIR and CD spectroscopy Biochimica et. Biophysica. Acta Biomembr. 1758 2006 1596 1608 (Pubitemid 44466707)
3. G. Cornaglia Fighting infections due to multidrug-resistant Gram-positive pathogens Clin. Microbiol. Infect. 15 2009 209 211
4. M.-P. Kieny The Evolving Threat of Antimicrobial Resistance: Options for Action 2012 World Health Organization Geneva, Switzerland 125
5. J.L. Fox The business of developing antibacterials Nat. Biotechnol. 24 2006 1521 1528 (Pubitemid 44967475)
6. G.P. Page Malcolm, and J. Heim Prospects for the next anti-Pseudomonas drug Curr. Opin. Pharmacol. 9 2009 558 565
7. D. Davies Understanding biofilm resistance to antibacterial agents Nat. Rev. Drug Discov. 2 2003 114 122 (Pubitemid 37361643)
8. N. Hoeiby, T. Bjarnsholt, M. Givskov, S. Molin, and O. Ciofu Antibiotic resistance of bacterial biofilms Int. J. Antimicrob. Agents 35 2010 322 332
9. T.-F.C. Mah, and G.A. O'Toole Mechanisms of biofilm resistance to antimicrobial agents Trends Microbiol. 9 2001 34 39
10. A. Giuliani, G. Pirri, A. Bozzi, A. Giulio, M. Aschi, and A.C. Rinaldi Antimicrobial peptides: natural templates for synthetic membrane-active compounds Cell. Mol. Life Sci. 65 2008 2450 2460
11. S.-U. Gorr Antimicrobial peptides of the oral cavity Periodontol. 2000 51 2009 152 180
12. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (London, U. K.) (Pubitemid 34100944)
13. H.W. Huang Action of antimicrobial peptides: two-state model Biochemistry 39 2000 8347 8352 (Pubitemid 30489931)
14. V.N. Lazarev, and V.M. Govorun Antimicrobial peptides and their use in medicine Appl. Biochem. Microbiol. 46 2010 803 814
15. L.T. Nguyen, E.F. Haney, and H.J. Vogel The expanding scope of antimicrobial peptide structures and their modes of action Trends Biotechnol. 29 2011 464 472
16. H. Sato, and J.B. Feix Peptide-membrane interactions and mechanisms of membrane destruction by amphipathic alpha-helical antimicrobial peptides Biochimica et. Biophysica. Acta Biomembr. 1758 2006 1245 1256 (Pubitemid 44444829)
17. L. Zhang, A. Rozek, and R.E.W. Hancock Interaction of cationic antimicrobial peptides with model membranes J. Biol. Chem. 276 2001 35714 35722
18. D. Allende, S.A. Simon, and T.J. McIntosh Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores Biophys. J. 88 2005 1828 1837 (Pubitemid 40976196)
19. T.J. Cheng John, D. Hale John, M. Elliot, E.W. Hancock Robert, and K. Straus Suzana Effect of membrane composition on antimicrobial peptides aurein 2.2 and 2.3 from Australian southern bell frogs Biophys. J. 96 2009 552 565
20. A.S. Ladokhin, and S.H. White 'Detergent-like' permeabilization of anionic lipid vesicles by melittin Biochim. Biophys. Acta Biomembr. 1514 2001 253 260 (Pubitemid 32831013)
21. G. Wiedman, K. Herman, P. Searson, W.C. Wimley, and K. Hristova The electrical response of bilayers to the bee venom toxin melittin: evidence for transient bilayer permeabilization Biochim. Biophys. Acta Biomembr. 1828 2013 1357 1364
22. W.C. Wimley, and K. Hristova Antimicrobial peptides: successes, challenges and unanswered questions J. Membr. Biol. 239 2011 27 34
23. S.-U. Gorr, M. Abdolhosseini, A. Shelar, and J. Sotsky Dual host-defence functions of SPLUNC2/PSP and synthetic peptides derived from the protein Biochem. Soc. Trans. 39 2011 1028 1032
24. C.D. Bingle, and S.U. Gorr Host defense in oral and airway epithelia: chromosome 20 contributes a new protein family Int. J. Biochem. Cell Biol. 36 2004 2144 2152 (Pubitemid 39094438)
25. S.-U. Gorr, J.B. Sotsky, A.P. Shelar, and D.R. Demuth Design of bacteria-agglutinating peptides derived from parotid secretory protein, a member of the bactericidal/permeability increasing-like protein family Peptides 29 2008 2118 2127 (Amsterdam, Netherlands) (Pubitemid 50326971)
26. M. Abdolhosseini, S.R. Nandula, J. Song, H. Hirt, and S.-U. Gorr Lysine substitutions convert a bacterial-agglutinating peptide into a bactericidal peptide that retains anti-lipopolysaccharide activity and low hemolytic activity Peptides 35 2012 231 238 (N. Y., NY, U.S.)
27. M. Abdolhosseini, J.B. Sotsky, A.P. Shelar, P.B.M. Joyce, and S.-U. Gorr Human parotid secretory protein is a lipopolysaccharide-binding protein: identification of an anti-inflammatory peptide domain Mol. Cell. Biochem. 359 2012 1 8
28. Innovagen, Peptide property calculator, in, vol. 2012, Innovagen, 2012.
29. M.L. Hutchison, and J.R.W. Govan Pathogenicity of microbes associated with cystic fibrosis Microbes Infect. 1 1999 1005 1014
30. D. Gidalevitz, Y. Ishitsuka, A.S. Muresan, O. Konovalov, A.J. Waring, R.I. Lehrer, and K.Y.C. Lee Interaction of antimicrobial peptide protegrin with biomembranes Proc. Natl. Acad. Sci. U.S.A. 100 2003 6302 6307 (Pubitemid 36666576)
31. M.L. Mangoni, and Y. Shai Short native antimicrobial peptides and engineered ultrashort lipopeptides: similarities and differences in cell specificities and modes of action Cell. Mol. Life Sci. 68 2011 2267 2280
32. K. Matsuzaki Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes Biochimica et. Biophysica. Acta Biomembr. 1462 1999 1 10
33. L.D. Mayer, M.J. Hope, and P.R. Cullis Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858 1986 161 168
34. H. Ostolaza, B. Bartolome, I.O.d. Zarate, F.d.l. Cruz, and F.M. Goni Release of lipid vesicle contents by the bacterial protein toxin alpha-hemolysin Biochimica et. Biophysica. Acta Biomembr. 1147 1993 81 88 (Pubitemid 23104891)
35. R.A. Parente, S. Nir, and F.C. Szoka Jr. Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA Biochemistry 29 1990 8720 8728 (Pubitemid 20302767)
36. R. Blumenthal, J.N. Weinstein, S.O. Sharrow, and P. Henkart Liposome-lymphocyte interaction: saturable sites for transfer and intracellular release of liposome contents Proc. Natl. Acad. Sci. U.S.A. 74 1977 5603 5607
37. G.R. Bartlett Phosphorus assay in column chromatography J. Biol. Chem. 234 1959 466 468
38. I. Fernandez David, P. Le Brun Anton, T.-H. Lee, P. Bansal, M.-I. Aguilar, M. James, and F. Separovic Structural effects of the antimicrobial peptide maculatin 1.1 on supported lipid bilayers Eur. Biophys. J. 42 2013 47 59
39. D.J. Hirst, T.-H. Lee, M.J. Swann, S. Unabia, Y. Park, K.-S. Hahm, and M.I. Aguilar Effect of acyl chain structure and bilayer phase state on binding and penetration of a supported lipid bilayer by HPA3 Eur. Biophys. J. 40 2011 503 514
40. T.-H. Lee, K.N. Hall, M.J. Swann, J.F. Popplewell, S. Unabia, Y. Park, K.-S. Hahm, and M.-I. Aguilar The membrane insertion of helical antimicrobial peptides from the N-terminus of Helicobacter pylori ribosomal protein L1 Biochim. Biophys. Acta Biomembr. 1798 2010 544 557
41. 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, destabilization and lysis Biochim. Biophys. Acta Biomembr. 1798 2010 1977 1986
42. A. Mashaghi, M. Swann, J. Popplewell, M. Textor, and E. Reimhult Optical anisotropy of supported lipid structures probed by waveguide spectroscopy and its application to study of supported lipid bilayer formation kinetics. [Erratum to document cited in CA148:466253] Anal. Chem. 80 2008 5276 (Washington, DC, U.S.) (Pubitemid 351956345)
43. N. Sanghera, M.J. Swann, G. Ronan, and T.J.T. Pinheiro Insight into early events in the aggregation of the prion protein on lipid membranes Biochim. Biophys. Acta Biomembr. 1788 2009 2245 2251
44. D. Gallez, M. Prevost, and A. Sanfeld Repulsive hydration forces between charged lipidic bilayers: a linear stability analysis Colloids Surf. 10 1984 123 131 (Pubitemid 15495112)
45. T.-H. Lee, K. Hall, A. Mechler, L. Martin, J. Popplewell, G. Ronan, and M.-I. Aguilar Molecular imaging and orientational changes of antimicrobial peptides in membranes Adv. Exp. Med. Biol. 611 2009 313 315
46. S.B. Nielsen, and D.E. Otzen Impact of the antimicrobial peptide Novicidin on membrane structure and integrity J. Colloid Interface Sci. 345 2010 248 256
47. L. Yu, L. Guo, J.L. Ding, B. Ho, S.-s. Feng, J. Popplewell, M. Swann, and T. Wohland Interaction of an artificial antimicrobial peptide with lipid membranes Biochim. Biophys. Acta 1788 2009 333 344
48. K. El Kirat, S. Morandat, and Y.F. Dufrene Nanoscale analysis of supported lipid bilayers using atomic force microscopy Biochimica et Biophysica Acta Biomembr. 1798 2010 750 765
49. J.T. Lewis, and H.M. McConnell Model lipid bilayer membranes as targets for antibody-dependent, cellular- and complement-mediated immune attack Ann. N. Y. Acad. Sci. 308 1978 124 138 (Pubitemid 8372522)
50. L.K. Tamm, and H.M. McConnell Supported phospholipid bilayers Biophys. J. 47 1985 105 113
51. M.R. Yeaman, and N.Y. Yount Mechanisms of antimicrobial peptide action and resistance Pharmacol. Rev. 55 2003 27 55 (Pubitemid 36268398)
52. V.V. Andrushchenko, M.H. Aarabi, L.T. Nguyen, E.J. Prenner, and H.J. Vogel Thermodynamics of the interactions of tryptophan-rich cathelicidin antimicrobial peptides with model and natural membranes Biochimica et. Biophysica. Acta Biomembr. 1778 2008 1004 1014
53. M. Hanulova, J. Andrae, P. Garidel, C. Olak, J. Howe, S.S. Funari, T. Gutsmann, and K. Brandenburg Interaction of melittin with phospholipid- and lipopolysaccharide-containing model membranes Anti-Infect. Agents Med. Chem. 8 2009 17 27
54. A.L. Russell, A.M. Kennedy, A.M. Spuches, D. Venugopal, J.B. Bhonsle, and R.P. Hicks Spectroscopic and thermodynamic evidence for antimicrobial peptide membrane selectivity Chem. Phys. Lipids 163 2010 488 497
55. J. Seelig Titration calorimetry of lipid-peptide interactions Biochimica et Biophysica Acta Rev. Biomembr. 1331 1997 103 116 (Pubitemid 27168150)
56. J.R. Lai, R.F. Epand, B. Weisblum, R.M. Epand, and S.H. Gellman Roles of salt and conformation in the biological and physicochemical behavior of protegrin-1 and designed analogues: correlation of antimicrobial, hemolytic, and lipid bilayer-perturbing activities Biochem. 45 2006 15718 15730 (Pubitemid 46032492)
57. V.K. Misra, K.A. Sharp, R.A. Friedman, and B. Honig Salt effects on ligand-DNA binding. Minor groove binding antibiotics J. Mol. Biol. 238 1994 245 263
58. M. Pasupuleti, M. Davoudi, M. Malmsten, and A. Schmidtchen Antimicrobial activity of a C-terminal peptide from human extracellular superoxide dismutase BMC Res. Notes 2 2009 (Article no. 136)
59. J.-P.S. Powers, A. Rozek, and R.E.W. Hancock Structure-activity relationships for the beta-hairpin cationic antimicrobial peptide polyphemusin I Biochim. Biophys. Acta Protein Proteomics 1698 2004 239 250 (Pubitemid 38591479)
60. N. Sreerama, S.Y. Venyaminov, and R.W. Woody Estimation of the number of α-helical and β-strand segments in proteins using circular dichroism spectroscopy Protein Sci. 8 1999 370 380 (Pubitemid 29072437)
61. N. Sreerama, S.Y. Venyaminov, and R.W. Woody Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis Anal. Biochem. 287 2000 243 251 (Pubitemid 32006233)
62. N. Sreerama, and R.W. Woody Protein secondary structure from circular dichroism spectroscopy. Combining variable selection principle and cluster analysis with neural network, ridge regression and self-consistent methods J. Mol. Biol. 242 1994 497 507
63. 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)
64. C.-C. Lee, Y. Sun, and H.W. Huang Membrane-mediated peptide conformation change from alpha-monomers to beta-aggregates Biophys. J. 98 2010 2236 2245
65. L. Hugonin, V. Vukojevic, G. Bakalkin, and A. Graeslund Membrane leakage induced by dynorphins FEBS Lett. 580 2006 3201 3205 (Pubitemid 43729662)
66. A. Arbuzova, and G. Schwarz Pore-forming action of mastoparan peptides on liposomes: a quantitative analysis Biochimica et. Biophyica. Acta Biomembr. 1420 1999 139 152 (Pubitemid 29369026)
67. J.M. Rausch, J.R. Marks, R. Rathinakumar, and W.C. Wimley β-Sheet pore-forming peptides selected from a rational combinatorial library: mechanism of pore formation in lipid vesicles and activity in biological membranes Biochemistry 46 2007 12124 12139 (Pubitemid 350022368)
68. M.M. Domingues, P.S. Santiago, M.A.R.B. Castanho, and N.C. Santos What can light scattering spectroscopy do for membrane-active peptide studies? J. Pept. Sci. 14 2008 394 400 (Pubitemid 351540897)
69. A. Marquette, B. Lorber, and B. Bechinger Reversible liposome association induced by LAH4: a peptide with potent antimicrobial and nucleic acid transfection activities Biophys. J. 98 2010 2544 2553
70. M.P. Goertz, N. Goyal, B.C. Bunker, and G.A. Montano Substrate effects on interactions of lipid bilayer assemblies with bound nanoparticles J. Colloid Interface Sci. 358 2011 635 638
71. E.T. Castellana, and P.S. Cremer Solid supported lipid bilayers: from biophysical studies to sensor design Surf. Sci. Rep. 61 2006 429 444 (Pubitemid 44634133)
72. B.H. Honig, W.L. Hubbell, and R.F. Flewelling Electrostatic interactions in membranes and proteins Annu. Rev. Biophys. Biophys. Chem. 15 1986 163 193
73. S. Nirasay, A. Badia, G. Leclair, J. Claverie, and I. Marcotte Polydopamine-supported lipid bilayers Mater. 5 2012 2621 2636
74. J. Murray, L. Cuccia, A. Ianoul, J.J. Cheetham, and L.J. Johnston Imaging the selective binding of synapsin to anionic membrane domains ChemBioChem 5 2004 1489 1494 (Pubitemid 39531661)
75. K. Mulligan, Z.J. Jakubek, and L.J. Johnston Supported lipid bilayers on biocompatible polysaccharide multilayers Langmuir 27 2011 14352 14359
76. M.L. Wagner, and L.K. Tamm Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane- polyethyleneglycol-lipid as a cushion and covalent linker Biophys. J. 79 2000 1400 1414
77. T. Wang, D. Li, X. Lu, A. Khmaladze, X. Han, S. Ye, P. Yang, G. Xue, N. He, and Z. Chen Single lipid bilayers constructed on polymer cushion studied by sum frequency generation vibrational spectroscopy J. Phys. Chem. C 115 2011 7613 7620
78. M.J. Goldman, G.M. Anderson, E.D. Stolzenberg, U.P. Kari, M. Zasloff, and J.M. Wilson Human β-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis Cell 88 1997 553 560 (Cambridge, Mass.) (Pubitemid 27154420)