Does cholesterol play a role in the bacterial selectivity of antimicrobial peptides?

Frontiers in Immunology

Volumn 3, Issue JUL, 2012, Pages

  Brender, Jeffrey R ^a   McHenry, Austin J ^a   Ramamoorthy, Ayyalusamy ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868335740     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00195     Document Type: Article

References (52)

1. Allende, D., Simon, S. A., and Mcintosh, T. J. (2005). Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 88, 1828-1837.
2. Bechinger, B. (1999). The structure, dynamics and ori- entation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462, 157-183.
3. Bechinger, B. (2011). Insights into the mechanisms of action of host defence peptides from biophysical and structural investigations. J. Pept. Sci. 17, 306-314.
4. Benachir, T., Monette, M., Grenier, J., and Lafleur, M. (1997). Melittin-induced leakage from phosphati- dylcholine vesicles is modulated by cholesterol: a property used for membrane targeting. Eur. Biophys. J. 25, 201-210.
5. Bhattacharjya, S., and Ramamoorthy, A. (2009). Multifunctional host defense peptides: functional and mechanistic insights from NMR structures of potent antimicrobial peptides. FEBS J. 276, 6465-6473.
6. Bhunia, A., Domadia, P. N., Torres, J., Hallock, K. J., Ramamoorthy, A., and Bhattacharjya, S. (2010). NMR structure of pardaxin, a pore-forming antimicrobial peptide, in lipopolysaccharide micelles mechanism of outer membrane permeabilization. J. Biol. Chem. 285, 3883-3895.
7. Bhunia, A., Ramamoorthy, A., and Bhattacharjya, S. (2009). Helical hairpin structure of a potent anti- microbial peptide MSI-594 in lipopolysaccharide micelles by NMR spectroscopy. Chemistry 15, 2036-2040.
8. Dhople, V., Krukemeyer, A., and Ramamoorthy, A. (2006). The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta 1758, 1499-1512.
9. Domadia, P. N., Bhunia, A., Ramamoorthy, A., and Bhattacharjya, S. (2010). 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. J. Am. Chem. Soc. 132, 18417-18428.
10. Durr, U. H. N., Sudheendra, U. S., and Ramamoorthy, A. (2006). Ll-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758, 1408-1425.
11. Epand, R. F., Maloy, W. L., Ramamoorthy, A., and Epand, R. M. (2010). Probing the "charge cluster mechanism" in amphipathic helical cationic antimicrobial pep- tides. Biochemistry 49, 4076-4084.
12. Epand, R. F., Ramamoorthy, A., and Epand, R. M. (2006a). Membrane lipid composition and the interaction of pardaxin: the role of cholesterol. Protein Pept. Lett. 13, 1-5.
13. Epand, R. F., Schmitt, M. A., Gellman, S. H., and Epand, R. M. (2006b). Role. Of membrane lipids in the mech- anism of bacterial species selective toxicity by two alpha/beta-antimicrobial peptides. Biochim. Biophys. Acta 1758, 1343-1350.
14. Epand, R. M., and Vogel, H. J. (1999). Diversity of anti- microbial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462, 11-28.
15. Evans, E. A., and Waugh, R. (1977). Mechano-chemistry of closed, vesicular membrane systems. J. Colloid Interface Sci. 60, 286-298.
16. Feigin, A. M., Teeter, J. H., and Brand, J. G. (1995). The influence of sterols on the sensitivity of lipid bilay- ers to melittin. Biochem. Biophys. Res. Commun. 211, 312-317.
17. Glukhov, E., Stark, M., Burrows, L. L., and Deber, C. M. (2005). Basis for selectivity of cationic antimicrobial peptides for bacterial versus mammalian membranes. J. Biol. Chem. 280, 33960-33967.
18. Gottler, L. M., and Ramamoorthy, A. (2009). Structure, membrane orientation, mechanism, and function of pexiganan - a highly potent antimicrobial peptide designed from magainin. Biochim. Biophys. Acta 1788, 1680-1686.
19. Hallock, K. J., Lee, D. K., Omnaas, J., Mosberg, H. I., and Ramamoorthy, A. (2002). Membrane composition determines pardaxin's mechanism of lipid bilayer disruption. Biophys. J. 83, 1004-1013.
20. Hallock, K. J., Lee, D. K., and Ramamoorthy, A. (2003). MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys. J. 84, 3052-3060.
21. Henriksen, J., Rowat, A. C., Brief, E., Hsueh, Y. W., Thewalt, J. L., Zuckermann, M. J., and Ipsen, J. H. (2006). Universal behavior of membranes with sterols. Biophys. J. 90, 1639-1649.
22. Hoskin, D. W., and Ramamoorthy, A. (2008). Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 1778, 357-375.
23. Mangoni, M. L., Papo, N., Saugar, J. M., Barra, D., Shai, Y. C., Simmaco, M., and Rivas, L. (2006). Effect of natural L- to D-amino acid conversion on the organization, membrane binding, and biological function of the antimicrobial peptides bombinins H. Biochemistry 45, 4266-4276.
24. Marquette, A., Mason, A. J., and Bechinger, B. (2008). Aggregation and membrane permeabilizing proper- ties of designed histidine-containing cationic linear peptide antibiotics. J. Pept. Sci. 14, 488-495.
25. Marsh, E. N. G., Buer, B. C., and Ramamoorthy, A. (2009). Fluorine-a new element in the design of membrane- active peptides. Mol. Biosyst. 5, 1143-1147.
26. Matsuzaki, K. (1999). Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462, 1-10.
27. Matsuzaki, K., Murase, O., Fujii, N., and Miyajima, K. (1995a). Translocation of a channel-forming antimi- crobial peptide, magainin-2, across lipid bilayers by forming a pore. Biochemistry 34, 6521-6526.
28. Matsuzaki, K., Sugishita, K., Fujii, N., and Miyajima, K. (1995b). Molecular-basis for membrane selectivity of an antimicrobial peptide, magainin-2. Biochemistry 34, 3423-3429.
29. M'Baye, G., Mely, Y., Duportail, G., and Klymchenko, A. S. (2008). Liquid ordered and gel phases of lipid bilayers: fluorescent probes reveal close fluidity but different hydration. Biophys. J. 95, 1217-1225.
30. Nguyen, L. T., Haney, E. F., and Vogel, H. J. (2011). The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29, 464-472.
31. Oren, Z., and Shai, Y. (1998). Mode of action of linear amphipathic alpha-helical antimicrobial peptides. Biopolymers 47, 451-463.
32. Pius, J., Morrow, M. R., and Booth, V. (2012). H-2 solid- state nuclear magnetic resonance investigation of whole Escherichia coli interacting with antimicrobial peptide MSI-78. Biochemistry 51, 118-125.
33. Pokorny, A., and Almeida, P. F. F. (2005). Permeabilization of raft-containing lipid vesicles by delta-lysin: a mechanism for cell sensitivity to cytotoxic peptides. Biochemistry 44, 9538-9544.
34. Pokorny, A., Yandek, L. E., Elegbede, A. I., Hinderliter, A., and Almeida, P. F. F. (2006). Temperature and com- position dependence of the interaction of delta-lysin with ternary mixtures of sphingomyelin/cholesterol/ popc. Biophys. J. 91, 2184-2197.
35. Porcelli, F., Buck, B., Lee, D. K., Hallock, K. J., Ramamoorthy, A., and Veglia, G. (2004). Structure and orientation of pardaxin determined by NMR experiments in model membranes. J. Biol. Chem. 279, 45815-45823.
36. Porcelli, F., Verardi, R., Shi, L., Henzler-Wildman, K. A., Ramamoorthy, A., and Veglia, G. (2008). NMR struc- ture of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles. Biochemistry 47, 5565-5572.
37. Raghuraman, H., and Chattopadhyay, A. (2004). Interaction of melittin with membrane cholesterol: a fluorescence approach. Biophys. J. 87, 2419-2432.
38. Ramamoorthy, A. (2009). Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State Nucl. Magn. Reson. 35, 201-207.
39. Ramamoorthy, A., Lee, D. K., Narasimhaswamy, T., and Nanga, R. P. R. (2010). Cholesterol reduces pardaxin's dynamics-a barrel-stave mechanism of membrane disruption investigated by solid-state NMR. Biochim. Biophys. Acta 1798, 223-227.
40. Ramamoorthy, A., Lee, D. K., Santos, J. S., and HenzlerWildman, K. A. (2008). Nitrogen-14 solid-state NMR spectroscopy of aligned phospholipid bilayers to probe peptide-lipid interaction and oligomerization of membrane associated peptides. J. Am. Chem. Soc. 130, 11023-11029.
41. Ramamoorthy, A., Thennarasu, S., Lee, D. K., Tan, A. M., and Maloy, L. (2006). Solid-state NMR investigation of the membrane-disrupting mechanism of antimi- crobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91, 206-216.
42. Shai, Y. (2002). Mode of action of membrane active anti- microbial peptides. Biopolymers 66, 236-248.
43. Shai, Y. (2004). Antimicrobial peptides: a lesson from nature for future antibiotics. J. Pept. Sci. 10, 112-112.
44. Strandberg, E., Kanithasen, N., Tiltak, D., Burck, J., Wadhwani, P., Zwernemann, O., and Ulrich, A. S. (2008). Solid-state NMR analysis comparing the designer-made antibiotic MSI-103 with its parent pep- tide PGLa in lipid bilayers. Biochemistry 47, 2601-2616.
45. Thennarasu, S., Huang, R., Lee, D. K., Yang, P., Maloy, L., Chen, Z., and Ramamoorthy, A. (2010). Limiting an antimicrobial peptide to the lipid-water interface enhances its bacterial membrane selectivity: a case study of MSI-367. Biochemistry 49, 10595-10605.
46. Toke, O., O'Connor, R. D., Weldeghiorghis, T. K., Maloy, W. L., Glaser, R. W., Ulrich, A. S., and Schaefer, J. (2004). Structure of (KIAGKIA)(3) aggregates in phospholipid bilayers by solid-state NMR. Biophys. J. 87, 675-687.
47. Tremouilhac, P., Strandberg, E., Wadhwani, P., and Ulrich, A. S. (2006). Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin. J. Biol. Chem. 281, 32089-32094.
48. Tytler, E. M., Anantharamaiah, G. M., Walker, D. E., Mishra, V. K., Palgunachari, M. N., and Segrest, J. P. (1995). Molecular-basis for prokaryotic speci- ficity of magainin-induced lysis. Biochemistry 34, 4393-4401.
49. van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124.
50. Verly, R. M., Rodrigues, M. A., Daghastanli, K. R. P., Denadai, A. M. L., Cuccovia, I. M., Bloch, C., Frezard, F., Santoro, M. M., Pilo-Veloso, D., and Bemquerer, M. P. (2008). Effect of cholesterol on the interaction of the amphibian antimicrobial peptide DD K with liposomes. Peptides 29, 15-24.
51. Wildman, K. A. H., Lee, D. K., and Ramamoorthy, A. (2003). Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42, 6545-6558.
52. Wu, G. Q., Wu, H. B., Fan, X. B., Zhao, R., Li, X. F., Wang, S. L., Ma, Y. H., Shen, Z. L., and Xi, T. (2010). Selective toxicity of antimicrobial peptide s-thanatin on bac- teria. Peptides 31, 1669-1673.