Table of Contents Author Guidelines Submit a Manuscript
International Journal of Medicinal Chemistry
Volume 2014 (2014), Article ID 809283, 13 pages
http://dx.doi.org/10.1155/2014/809283
Research Article

Synthetic Antimicrobial Peptides Exhibit Two Different Binding Mechanisms to the Lipopolysaccharides Isolated from Pseudomonas aeruginosa and Klebsiella pneumoniae

1Department of Chemistry, East Carolina University, Science and Technology Building, Greenville, NC 27858, USA
2Department of Chemistry and Physics, Georgia Regents University, College of Science and Mathematics, Augusta, GA 30904, USA

Received 27 August 2014; Revised 26 November 2014; Accepted 26 November 2014; Published 28 December 2014

Academic Editor: Armando Rossello

Copyright © 2014 Hanbo Chai et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. E. W. Hancock, “The therapeutic potential of cationic peptides,” Expert Opinion on Investigational Drugs, vol. 7, no. 2, pp. 167–174, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. O. Toke, “Antimicrobial peptides: new candidates in the fight against bacterial infections,” Peptide Science, vol. 80, no. 6, pp. 717–735, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Zasloff, “Antimicrobial peptides of multicellular organisms,” Nature, vol. 415, no. 6870, pp. 389–395, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Zhang and T. J. Falla, “Host defense peptides for use as potential therapeutics,” Current Opinion in Investigational Drugs, vol. 10, no. 2, pp. 164–171, 2009. View at Google Scholar · View at Scopus
  5. M. R. Wenk and J. Seelig, “Magainin 2 amide interaction with lipid membranes: calorimetric detection of peptide binding and pore formation,” Biochemistry, vol. 37, no. 11, pp. 3909–3916, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Wieprecht, O. Apostolov, and J. Seelig, “Binding of the antibacterial peptide magainin 2 amide to small and large unilamellar vesicles,” Biophysical Chemistry, vol. 85, no. 2-3, pp. 187–198, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Wieprecht, O. Apostolov, M. Beyermann, and J. Seelig, “Membrane binding and pore formation of the antibacterial peptide PGLa: thermodynamic and mechanistic aspects,” Biochemistry, vol. 39, no. 2, pp. 442–452, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. R. E. W. Hancock and A. Patrzykat, “Clinical development of cationic antimicrobial peptides: from natural to novel antibiotics,” Current Drug Targets—Infectious Disorders, vol. 2, no. 1, pp. 79–83, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Papo and Y. Shai, “New lytic peptides based on the D,L-amphipathic helix motif preferentially kill tumor cells compared to normal cells,” Biochemistry, vol. 42, no. 31, pp. 9346–9354, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Huang, J. Huang, and Y. Chen, “Alpha-helical cationic antimicrobial peptides: relationships of structure and function,” Protein and Cell, vol. 1, no. 2, pp. 143–152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Ganz, “Defensins: antimicrobial peptides of innate immunity,” Nature Reviews Immunology, vol. 3, no. 9, pp. 710–720, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Simmaco, G. Mignogna, and D. Barra, “Antimicrobial peptides from amphibian skin: what do they tell us?” Biopolymers, vol. 47, pp. 435–450, 1999. View at Google Scholar
  13. S. R. Dennison, J. Wallace, F. Harris, and D. A. Phoenix, “Amphiphilic α-helical antimicrobial peptides and their structure/function relationships,” Protein and Peptide Letters, vol. 12, no. 1, pp. 31–39, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. D. A. Phoenix, F. Harris, S. Dennison, L. Chatfield, Z. Sayed, and S. Hussain, “Antimicrobial therapy: old problems—new solution,” JEC. Qual. L., vol. 1, pp. 44–61, 2003. View at Google Scholar
  15. M. R. Yeaman and N. Y. Yount, “Mechanisms of antimicrobial peptide action and resistance,” Pharmacological Reviews, vol. 55, no. 1, pp. 27–55, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. M. Song, Y. Park, S. S. Lim et al., “Cell selectivity and mechanism of action of antimicrobial model peptides containing peptoid residues,” Biochemistry, vol. 44, no. 36, pp. 12094–12106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. D. A. Devine and R. E. W. Hancock, “Cationic peptides: distribution and mechanisms of resistance,” Current Pharmaceutical Design, vol. 8, no. 9, pp. 703–714, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. M. A. Fox, J. E. Thwaite, D. O. Ulaeto, T. P. Atkins, and H. S. Atkins, “Design and characterization of novel hybrid antimicrobial peptides based on cecropin A, LL-37 and magainin II,” Peptides, vol. 33, no. 2, pp. 197–205, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. K. A. Brogden, “Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?” Nature Reviews Microbiology, vol. 3, no. 3, pp. 238–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. U. H. N. Dürr, U. S. Sudheendra, and A. Ramamoorthy, “LL-37, the only human member of the cathelicidin family of antimicrobial peptides,” Biochimica et Biophysica Acta—Biomembranes, vol. 1758, no. 9, pp. 1408–1425, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. D. W. Hoskin and A. Ramamoorthy, “Studies on anticancer activities of antimicrobial peptides,” Biochimica et Biophysica Acta: Biomembranes, vol. 1778, no. 2, pp. 357–375, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Dhople, A. Krukemeyer, and A. Ramamoorthy, “The human beta-defensin-3, an antibacterial peptide with multiple biological functions,” Biochimica et Biophysica Acta: Biomembranes, vol. 1758, no. 9, pp. 1499–1512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Aisenbrey, P. Bertani, and B. Bechinger, “Solid-state NMR investigations of membrane-associated antimicrobial peptides,” Methods in Molecular Biology, vol. 618, pp. 209–233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Tang and M. Hong, “Structure and mechanism of β-hairpin antimicrobial peptides in lipid bilayers from solid-state NMR spectroscopy,” Molecular BioSystems, vol. 5, no. 4, pp. 317–322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Ramamoorthy, S. Thennarasu, D.-K. Lee, A. Tan, and L. Maloy, “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, vol. 91, no. 1, pp. 206–216, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Bertelsen, B. Vad, E. H. Nielsen et al., “Long-term-stable ether-lipid vs conventional ester-lipid bicelles in oriented solid-state NMR: altered structural information in studies of antimicrobial peptides,” The Journal of Physical Chemistry B, vol. 115, no. 8, pp. 1767–1774, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Lorin, M. Noël, M.-È. Provencher et al., “Determining the mode of action involved in the antimicrobial activity of synthetic peptides: a solid-state NMR and FTIR study,” Biophysical Journal, vol. 103, no. 7, pp. 1470–1479, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. T.-J. Park, J.-S. Kim, H.-C. Ahn, and Y. Kim, “Solution and solid-state NMR structural studies of antimicrobial peptides LPcin-I and LPcin-II,” Biophysical Journal, vol. 101, no. 5, pp. 1193–1201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Ramamoorthy, “Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights,” Solid State Nuclear Magnetic Resonance, vol. 35, no. 4, pp. 201–207, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. H. G. Boman, “Antibacterial peptides: basic facts and emerging concepts,” Journal of Internal Medicine, vol. 254, no. 3, pp. 197–215, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Elsbach, “What is the real role of antimicrobial polypeptides that can mediate several other inflammatory responses?” Journal of Clinical Investigation, vol. 111, no. 11, pp. 1643–1645, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. R. E. W. Hancock and G. Diamond, “The role of cationic antimicrobial peptides in innate host defences,” Trends in Microbiology, vol. 8, no. 9, pp. 402–410, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. R. E. Hancock, “Cationic peptides: effectors in innate immunity and novel antimicrobials,” Lancet Infectious Diseases, vol. 1, no. 3, pp. 156–164, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Porcelli, R. Verardi, L. Shi, K. A. Henzler-Wildman, A. Ramamoorthy, and G. Veglia, “NMR structure of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles,” Biochemistry, vol. 47, no. 20, pp. 5565–5572, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J.-P. S. Powers and R. E. W. Hancock, “The relationship between peptide structure and antibacterial activity,” Peptides, vol. 24, no. 11, pp. 1681–1691, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Seelig, “Titration calorimetry of lipid-peptide interactions,” Biochimica et Biophysica Acta—Reviews on Biomembranes, vol. 1331, no. 1, pp. 103–116, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. R. P. Hicks, J. B. Bhonsle, D. Venugopal, B. W. Koser, and A. J. Magill, “De novo design of selective antibiotic peptides by incorporation of unnatural amino acids,” Journal of Medicinal Chemistry, vol. 50, no. 13, pp. 3026–3036, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Findlay, G. G. Zhanel, and F. Schweizer, “Cationic amphiphiles, a new generation of antimicrobials inspired by the natural antimicrobial peptide scaffold,” Antimicrobial Agents and Chemotherapy, vol. 54, no. 10, pp. 4049–4058, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Godballe, L. L. Nilsson, P. D. Petersen, and H. Jenssen, “Antimicrobial β-peptides and α-peptoids,” Chemical Biology and Drug Design, vol. 77, no. 2, pp. 107–116, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Glukhov, M. Stark, L. L. Burrows, and C. M. Deber, “Basis for selectivity of cationic antimicrobial peptides for bacterial versus mammalian membranes,” The Journal of Biological Chemistry, vol. 280, no. 40, pp. 33960–33967, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Giangaspero, L. Sandri, and A. Tossi, “Amphipathic α helical antimicrobial peptides: a systematic study of the effects of structural and physical properties on biological activity,” European Journal of Biochemistry, vol. 268, no. 21, pp. 5589–5600, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Goodman and H. Shao, “Peptidomimetic building blocks for drug discovery: an overview,” Pure and Applied Chemistry, vol. 66, pp. 1303–1308, 1996. View at Google Scholar
  43. T. L. Hendrickson, V. de Crécy-Lagard, and P. Schimmel, “Incorporation of nonnatural amino acids into proteins,” Annual Review of Biochemistry, vol. 73, pp. 147–176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Andersson and L. Mäler, “Motilin-bicelle interactions: membrane position and translational diffusion,” FEBS Letters, vol. 545, no. 2-3, pp. 139–143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. W. C. Johnson, “Analyzing protein circular dichroism spectra for accurate secondary structures,” Proteins: Structure, Function and Genetics, vol. 35, no. 3, pp. 307–312, 1999. View at Google Scholar
  46. P. G. Vasudev, S. Chatterjee, S. Narayanaswamy, and B. Padmanabhan, “Structural chemistry of peptides containing backbone expanded amino acid residues: conformational features of β, γ, and hybrid peptides,” Chemical Reviews, vol. 111, no. 2, pp. 657–687, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. 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,” Chemistry and Physics of Lipids, vol. 163, no. 6, pp. 488–497, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. A. L. Russell, D. Klapper, A. H. Srouji et al., “The design of bacteria strain selective antimicrobial peptides based on the incorporation of unnatural amino acids,” in A Search for Antibacterial Agents, V. Bobbarala, Ed., vol. 2, chapter 14, InTech, 2012. View at Publisher · View at Google Scholar
  49. L. M. Gottler, R. D. L. S. Bea, C. E. Shelburne, A. Ramamoorthy, and E. N. G. Marsh, “Using fluorous amino acids to probe the effects of changing hydrophobicity on the physical and biological properties of the β-hairpin antimicrobial peptide protegrin-1,” Biochemistry, vol. 47, no. 35, pp. 9243–9250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. L. M. Gottler, H.-Y. Lee, C. E. Shelburne, A. Ramamoorthy, and E. N. G. Marsh, “Using fluorous amino acids to modulate the biological activity of an antimicrobial peptide,” ChemBioChem, vol. 9, no. 3, pp. 370–373, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. M. Rowe, S. Miller, and E. J. Sorscher, “Cystic fibrosis,” The New England Journal of Medicine, vol. 352, no. 19, pp. 1992–2001, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. A. K. Marr, W. J. Gooderham, and R. E. Hancock, “Antibacterial peptides for therapeutic use: obstacles and realistic outlook,” Current Opinion in Pharmacology, vol. 6, no. 5, pp. 468–472, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. W. J. Gooderham, M. Bains, J. B. McPhee, I. Wiegand, and R. E. W. Hancock, “Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa,” Journal of Bacteriology, vol. 190, no. 16, pp. 5624–5634, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Overhage, A. Campisano, M. Bains, E. C. W. Torfs, B. H. A. Rehm, and R. E. W. Hancock, “Human host defense peptide LL-37 prevents bacterial biofilm formation,” Infection and Immunity, vol. 76, no. 9, pp. 4176–4182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. J. W. Costerton, P. S. Stewart, and E. P. Greenberg, “Bacterial biofilms: a common cause of persistent infections,” Science, vol. 284, no. 5418, pp. 1318–1322, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. R. S. Dieter, “Coronary artery stent infection,” Catheterization and Cardiovascular Interventions, vol. 62, p. 281, 2004. View at Google Scholar
  57. Centers for Disease Control and Prevention, “Vital signs: carbapenem-resistant enterobacteriaceae,” Morbidity and Mortality Weekly Report, vol. 62, no. 9, pp. 165–170, 2013. View at Google Scholar
  58. A. Bhunia, P. N. Domadia, J. Torres, K. J. Hallock, A. Ramamoorthy, and S. Bhattacharjya, “NMR structure of pardaxin, a pore-forming antimicrobial peptide, in lipopolysaccharide micelles: mechanism of outer membrane permeabilization,” Journal of Biological Chemistry, vol. 285, no. 6, pp. 3883–3895, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. A. S. Altieri, D. P. Hinton, and R. A. Byrd, “Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements,” Journal of the American Chemical Society, vol. 117, no. 28, pp. 7566–7567, 1995. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Bhunia, H. Mohanram, P. Domadia, J. Torres, and S. Bhattacharjya, “Designed β-boomerang antiendotoxic and antimicrobial peptides. Structures and activities in lipopolysaccharide,” The Journal of Biological Chemistry, vol. 284, no. 33, pp. 21991–22004, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. C. R. H. Raetz and C. Whitfield, “Lipopolysaccharide endotoxins,” Annual Review of Biochemistry, vol. 71, pp. 635–700, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. E. T. Rietschhel, T. Kirikae, F. U. Schde et al., “Bacterial endotoxin: molecular relationships of structure to activity and function,” The FASEB Journal, vol. 8, no. 2, pp. 217–225, 1994. View at Google Scholar
  63. M. D. Lad, F. Birembaut, L. A. Clifton, R. A. Frazier, J. R. P. Webster, and R. J. Green, “Antimicrobial peptide-lipid binding interactions and binding selectivity,” Biophysical Journal, vol. 92, no. 10, pp. 3575–3586, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Ding, L. Yang, T. M. Weiss, A. J. Waring, R. I. Lehrer, and H. W. Huang, “Interaction of antimicrobial peptides with lipopolysaccharides,” Biochemistry, vol. 42, no. 42, pp. 12251–12259, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. P. N. Domadia, A. Bhunia, A. Ramamoorthy, and S. Bhattacharjya, “Structure, interactions, and antibacterial activities of MSI-594 derived mutant peptide MSI-594F5A in lipopolysaccharide micelles: role of the helical hairpin conformation in outer-membrane permeabilization,” Journal of the American Chemical Society, vol. 132, no. 51, pp. 18417–18428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. A. H. Delcour, “Outer membrane permeability and antibiotic resistance,” Biochimica et Biophysica Acta—Proteins and Proteomics, vol. 1794, no. 5, pp. 808–816, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. R. E. Hancock, “Alterations in outer membrane permeability,” Annual Review of Microbiology, vol. 38, pp. 237–264, 1984. View at Publisher · View at Google Scholar · View at Scopus
  68. R. E. W. Hancock and D. S. Chapple, “Peptide antibiotics,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 6, pp. 1317–1323, 1999. View at Google Scholar · View at Scopus
  69. V. Frecer, B. Ho, and J. L. Ding, “De novo design of potent antimicrobial peptides,” Antimicrobial Agents and Chemotherapy, vol. 48, no. 9, pp. 3349–3357, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. H. G. Boman, “Peptide antibiotics and their role in innate immunity,” Annual Review of Immunology, vol. 13, pp. 61–92, 1995. View at Publisher · View at Google Scholar · View at Scopus
  71. P. M. Hwang and H. J. Vogel, “Structure-function relationships of antimicrobial peptides,” Biochemistry and Cell Biology, vol. 76, no. 2-3, pp. 235–246, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. N. Papo and Y. Shai, “A molecular mechanism for lipopolysaccharide protection of gram-negative bacteria from antimicrobial peptides,” Journal of Biological Chemistry, vol. 280, no. 11, pp. 10378–10387, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. T. J. Falla, D. N. Karunaratne, and R. E. W. Hancock, “Mode of action of the antimicrobial peptide indolicidin,” The Journal of Biological Chemistry, vol. 271, no. 32, pp. 19298–19303, 1996. View at Publisher · View at Google Scholar · View at Scopus
  74. Y. Shai, “Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides,” Biochimica et Biophysica Acta—Biomembranes, vol. 1462, no. 1-2, pp. 55–70, 1999. View at Publisher · View at Google Scholar · View at Scopus
  75. N. Papo and Y. Shai, “Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes?” Peptides, vol. 24, no. 11, pp. 1693–1703, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Stark, L.-P. Liu, and C. M. Deber, “Cationic hydrophobic peptides with antimicrobial activity,” Antimicrobial Agents and Chemotherapy, vol. 46, no. 11, pp. 3585–3590, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. J. B. Bhonsle, T. Clark, L. Bartolotti, and R. P. Hicks, “A brief overview of antimicrobial peptides containing unnatural amino acids and Ligand-based approaches for peptide Ligands,” Current Topics in Medicinal Chemistry, vol. 13, no. 24, pp. 3205–3224, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. R. P. Hicks, J. J. Abercrombie, R. K. Wong, and K. P. Leung, “Antimicrobial peptides containing unnatural amino acid exhibit potent bactericidal activity against ESKAPE pathogens,” Bioorganic and Medicinal Chemistry, vol. 21, no. 1, pp. 205–214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. G. A. Grant, Synthetic Peptides: A User's Guide, Oxford University Press, New York, NY, USA, 2nd edition, 2002.
  80. N. L. Benoiton, Chemistry of Peptide Synthesis, Taylor and Francis (CRC Press), Boca Raton, Fla, USA, 2006.
  81. J. B. Bhonsle, D. Venugopal, D. P. Huddler, A. J. Magill, and R. P. Hicks, “Application of 3D-QSAR for identification of descriptors defining bioactivity of antimicrobial peptides,” Journal of Medicinal Chemistry, vol. 50, no. 26, pp. 6545–6553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. D. Venugopal, D. Klapper, A. H. Srouji et al., “Novel antimicrobial peptides that exhibit activity against select agents and other drug resistant bacteria,” Bioorganic& Medicinal Chemistry, vol. 18, no. 14, pp. 5137–5147, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. S. Ladokhin, M. Fernández-Vidal, and S. H. White, “CD spectroscopy of peptides and proteins bound to large unilamellar vesicles,” The Journal of Membrane Biology, vol. 236, no. 3, pp. 247–253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. A. Glättli, X. Daura, D. Seebach, and W. F. van Gunsteren, “Can one derive the conformational preference of a β-peptide from its CD spectrum?” Journal of the American Chemical Society, vol. 124, no. 44, pp. 12972–12978, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. A. S. Ladokhin, M. E. Selsted, and S. H. White, “CD spectra of indolicidin antimicrobial peptides suggest turns, not polyproline helix,” Biochemistry, vol. 38, no. 38, pp. 12313–12319, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Singh, G. Kasetty, A. Schmidtchen, and M. Malmsten, “Membrane and lipopolysaccharide interactions of C-terminal peptides from S1 peptidases,” Biochimica et Biophysica Acta: Biomembranes, vol. 1818, no. 9, pp. 2244–2251, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. F. Bringezu, S. Wen, S. Dante, T. Hauss, M. Majerowicz, and A. Waring, “The insertion of the antimicrobial peptide dicynthaurin monomer in model membranes: thermodynamics and structural characterization,” Biochemistry, vol. 46, no. 19, pp. 5678–5686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. S.-Y. Wei, J.-M. Wu, Y.-Y. Kuo et al., “Solution structure of a novel tryptophan-rich peptide with bidirectional antimicrobial activity,” Journal of Bacteriology, vol. 188, no. 1, pp. 328–334, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. A. Bax and D. G. Davis, “MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy,” Journal of Magnetic Resonance (1969), vol. 65, no. 2, pp. 355–360, 1985. View at Publisher · View at Google Scholar · View at Scopus
  90. G. Eich, G. Bodenhausen, and R. R. Ernst, “Coherence transfer by isotropic mixing: application to proton correlation spectroscopy,” Journal of the American Chemical Society, vol. 104, no. 13, pp. 3731–3732, 1982. View at Publisher · View at Google Scholar
  91. D. J. States, R. A. Haberkorn, and D. J. Ruben, “A two-dimensional nuclear overhauser experiment with pure absorption phase in four quadrants,” Journal of Magnetic Resonance, vol. 48, no. 2, pp. 286–292, 1982. View at Publisher · View at Google Scholar · View at Scopus
  92. J. Andrä, M. H. J. Koch, R. Bartels, and K. Brandenburg, “Biophysical characterization of endotoxin inactivation by NK-2, an antimicrobial peptide derived from mammalian NK-lysin,” Antimicrobial Agents and Chemotherapy, vol. 48, no. 5, pp. 1593–1599, 2004. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Brandenburg, S. Kusumoto, and U. Seydel, “Conformational studies of synthetic lipid A analogues and partial structures by infrared spectroscopy,” Biochimica et Biophysica Acta, vol. 1329, no. 1, pp. 183–201, 1997. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Snyder, D. Kim, and T. J. McIntosh, “Lipopolysaccharide bilayer structure: effect of chemotype, core mutations, divalent cations, and temperature,” Biochemistry, vol. 38, no. 33, pp. 10758–10767, 1999. View at Publisher · View at Google Scholar · View at Scopus
  95. D. Allende and T. J. McIntosh, “Lipopolysaccharides in bacterial membranes act like cholesterol in eukaryotic plasma membranes in providing protection against melittin-induced bilayer lysis,” Biochemistry, vol. 42, no. 4, pp. 1101–1108, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. P. Plesiat and H. Nikaido, “Outer membranes of Gram-negative bacteria are permeable to steroid probes,” Molecular Microbiology, vol. 6, no. 10, pp. 1323–1333, 1992. View at Publisher · View at Google Scholar · View at Scopus
  97. E. A. Porter, B. Weisblum, and S. H. Gellman, “Use of parallel synthesis to probe structure-activity relationships among 12-helical β-peptides: evidence of a limit on antimicrobial activity,” Journal of the American Chemical Society, vol. 127, no. 32, pp. 11516–11529, 2005. View at Publisher · View at Google Scholar · View at Scopus