Cholesterol reduces pardaxin's dynamics-a barrel-stave mechanism of membrane disruption investigated by solid-state NMR

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 2, 2010, Pages 223-227

  Ramamoorthy, Ayyalusamy ^a   Lee, Dong Kuk ^a   Narasimhaswamy, Tennaru ^a   Nanga, Ravi P R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Antimicrobial peptide; Barrel stave; Dynamic; Membrane orientation; Pardaxin

Indexed keywords

CHOLESTEROL; PARDAXIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ANIMALS; ANTI-INFECTIVE AGENTS; CHOLESTEROL; FISH PROTEINS; FISH VENOMS; FISHES; LIPID BILAYERS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOLIPIDS; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP;

PARDACHIRUS MARMORATUS;

EID: 74249106455     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.08.012     Document Type: Article

References (60)

1. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
2. Hancock R.E., and Diamond G. The role of cationic antimicrobial peptides in innate host defences. Trends in microbiol. 8 (2000) 402-410
3. Dhople V., Krukemeyer A., and Ramamoorthy A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta 1758 (2006) 1499-1512
4. Shai Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462 (1999) 55-70
5. Epand R.M., and Vogel H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462 (1999) 11-28
6. 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
7. Huang H.W., Chen F.Y., and Lee M.T. Molecular mechanism of peptide-induced pores in membranes. Phys. Rev. Lett. 92 (2004) 198304
8. Kandasamy S.K., Lee D.K., Nanga R.P., Xu J., Santos J.S., Larson R.G., and Ramamoorthy A. Solid-state NMR and molecular dynamics simulations reveal the oligomeric ion-channels of TM2-GABA(A) stabilized by intermolecular hydrogen bonding. Biochim. Biophys. Acta 1788 (2009) 686-695
9. Maloy W.L., and Kari U.P. Structure-activity studies on magainins and other host defense peptides. Biopolymers 37 (1995) 105-122
10. Gottler L.M., de la Salud Bea R., Shelburne C.E., Ramamoorthy A., and Marsh E.N. Using fluorous amino acids to probe the effects of changing hydrophobicity on the physical and biological properties of the beta-hairpin antimicrobial peptide protegrin-1. Biochemistry 47 (2008) 9243-9250
11. Gottler L.M., Lee H.Y., Shelburne C.E., Ramamoorthy A., and Marsh E.N. Using fluorous amino acids to modulate the biological activity of an antimicrobial peptide. ChemBioChem 9 (2008) 370-373
12. Lipsky B.A., Holroyd K.J., and Zasloff M. Topical versus systemic antimicrobial therapy for treating mildly infected diabetic foot ulcers: a randomized, controlled, double-blinded, multicenter trial of pexiganan cream. Clin. Infect. Dis. 47 (2008) 1537-1545
13. Giuliani A., Pirri G., and Nicoletto S.F. Antimicrobial peptides: an overview of a promising class of therapeutics. Cent. Eur. J. Biol. 2 (2007) 1-33
14. Hoskin D.W., and Ramamoorthy A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 1778 (2008) 357-375
15. Gottler L.M., and Ramamoorthy A. Structure, membrane orientation, mechanism, and function of pexiganan-a highly potent antimicrobial peptide designed from magainin. BBA Biomembranes 1788 (2009) 1680-1686
16. Rapaport D., Peled R., Nir S., and Shai Y. Reversible surface aggregation in pore formation by pardaxin. Biophys. J. 70 (1996) 2502-2512
17. Oren Z., and Shai Y. A class of highly potent antibacterial peptides derived from pardaxin, a pore-forming peptide isolated from Moses sole fish Pardachirus marmoratus. Eur. J. Biochem. 237 (1996) 303-310
18. Shai Y. Pardaxin-channel formation by a shark repellant peptide from fish. Toxicology 87 (1994) 109-129
19. Rapaport D., and Shai Y. Aggregation and organization of pardaxin in phospholipid-membranes-a Fluorescence Energy-Transfer Study. J. Biol. Chem. 267 (1992) 6502-6509
20. Shai Y., Hadari Y.R., and Finkels A. pH-dependent pore formation properties of pardaxin analogues. J. Biol. Chem. 266 (1991) 22346-22354
21. Shai Y., Bach D., and Yanovsky A. Channel formation properties of synthetic pardaxin and analogues. J. Biol. Chem. 265 (1990) 20202-20209
22. Zagorski M.G., Norman D.G., Barrow C.J., Iwashita T., Tachibana K., and Patel D.J. Solution structure of pardaxin P-2. Biochemistry 30 (1991) 8009-8017
23. 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
24. Hallock K.J., Lee D.K., Omnaas J., Mosberg H.I., and Ramamoorthy A. Membrane composition determines pardaxin's mechanism of lipid bilayer disruption. Biophys. J. 83 (2002) 1004-1013
25. Thennarasu S., and Nagaraj R. Specific antimicrobial and hemolytic activities of 18-residue peptides derived from the amino terminal region of the toxin pardaxin. Protein Eng. 9 (1996) 1219-1224
26. Yamamoto K., Lee D.K., and Ramamoorthy A. Broadband-PISEMA solid-state NMR spectroscopy. Chem. Phys. Lett. 407 (2005) 289-293
27. Wu C.H., Ramamoorthy A., and Opella S.J. High-resolution heteronuclear dipolar solid-state NMR-spectroscopy. J. Magn. Reson. Ser. A 109 (1994) 270-272
28. Ramamoorthy A., Wei Y.F., and Lee D.K. PISEMA solid-state NMR spectroscopy. Annu. Rep. NMR Spectrosc. 52 (2004) 1-52
29. Hallock K.J., Henzler Wildman K., Lee D.K., and Ramamoorthy A. An innovative procedure using a sublimable solid to align lipid bilayers for solid-state NMR studies. Biophys. J. 82 (2002) 2499-2503
30. Page R.C., Kim S., and Cross T.A. Transmembrane helix uniformity examined by spectral mapping of torsion angles. Structure 16 (2008) 787-797
31. Page R.C., Li C., Hu J., Gao F.P., and Cross T.A. Lipid bilayers: an essential environment for the understanding of membrane proteins. Magn. Reson. Chem. 45 (2007) S2-S11
32. Opella S.J., and Marassi F.M. Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104 (2004) 3587-3606
33. Marassi F.M., and Opella S.J. A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson. 144 (2000) 150-155
34. Wang J., Denny J., Tian C., Kim S., Mo Y., Kovacs F., Song Z., Nishimura K., Gan Z., Fu R., Quine J.R., and Cross T.A. Imaging membrane protein helical wheels. J. Magn. Reson. 144 (2000) 162-167
35. Dürr U.H., Waskell L., and Ramamoorthy A. The cytochromes P450 and b5 and their reductases-promising targets for structural studies by advanced solid-state NMR spectroscopy. Biochim. Biophys. Acta 1768 (2007) 3235-3259
36. Buffy J.J., Traaseth N.J., Mascioni A., Gor'kov P.L., Chekmenev E.Y., Brey W.W., and Veglia G. Two-dimensional solid-state NMR reveals two topologies of sarcolipin in oriented lipid bilayers. Biochemistry 45 (2006) 10939-10946
37. Dürr U.H., Sudheendra U.S., and Ramamoorthy A. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758 (2006) 1408-1425
38. 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 (19)F NMR spectroscopy. J. Am. Chem. Soc. 130 (2008) 16512-16514
39. Bak M., Bywater R.P., Hohwy M., Thomsen J.K., Adelhorst K., Jakobsen H.J., Sorensen O.W., and Nielsen N.C. Conformation of alamethicin in oriented phospholipid bilayers determined by (15)N solid-state nuclear magnetic resonance. Biophys. J. 81 (2001) 1684-1698
40. Aisenbrey C., Bertani P., Henklein P., and Bechinger B. Structure, dynamics and topology of membrane polypeptides by oriented 2H solid-state NMR spectroscopy. Eur. Biophys. J. 36 (2007) 451-460
41. Brender J.R., Durr U.H., Heyl D., Budarapu M.B., and Ramamoorthy A. Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. Biochim. Biophys. Acta 1768 (2007) 2026-2029
42. Hallock K.J., Lee D.K., and Ramamoorthy A. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys. J. 84 (2003) 3052-3060
43. Wi S., and Kim C. Pore structure, thinning effect, and lateral diffusive dynamics of oriented lipid membranes interacting with antimicrobial peptide protegrin-1: 31P and 2H solid-state NMR study. J. Phys. Chem. 112 (2008) 11402-11414
44. Andersson A., Biverstahl H., Nordin J., Danielsson J., Lindahl E., and Maler L. The membrane-induced structure of melittin is correlated with the fluidity of the lipids. Biochim. Biophys. Acta-Biomembr. 1768 (2007) 115-121
45. Wessman P., Stromstedt A.A., Malmsten M., and Edwards K. Melittin-lipid bilayer interactions and the role of cholesterol. Biophys. J. 95 (2008) 4324-4336
46. Raghuraman H., and Chattopadhyay A. Cholesterol inhibits the lytic activity of melittin in erythrocytes. Chem. Phys. Lipids 134 (2005) 183-189
47. Allende D., Simon S.A., and McIntosh T.J. Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 88 (2005) 1828-1837
48. Constantinescu I., and Lafleur M. Influence of the lipid composition on the kinetics of concerted insertion and folding of melittin in bilayers. Biochim. Biophys. Acta-Biomembr. 1667 (2004) 26-37
49. Raghuraman H., and Chattopadhyay A. Interaction of melittin with membrane cholesterol: a fluorescence approach. Biophys. J. 87 (2004) 2419-2432
50. Benachir T., Monette M., Grenier J., and Lafleur M. Melittin-induced leakage from phosphatidylcholine vesicles is modulated by cholesterol: a property used for membrane targeting. Eur. Biophys. J. Biophys. Lett. 25 (1997) 201-210
51. Epand R.M. Proteins and cholesterol-rich domains. Biochim. Biophys. Acta-Biomembr. 1778 (2008) 1576-1582
52. Epand R.M. Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta-Biomembr. 1614 (2003) 116-121
53. Cecchi C., Baglioni S., Fiorillo C., Pensalfini A., Liguri G., Nosi D., Rigacci S., Bucciantini M., and Stefani M. Insights into the molecular basis of the differing susceptibility of varying cell types to the toxicity of amyloid aggregates. J. Cell Sci. 118 (2005) 3459-3470
54. Kakio A., Nishimoto S., Yanagisawa K., Kozutsumi Y., and Matsuzaki K. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J. Biol. Chem. 276 (2001) 24985-24990
55. Lau T.L., Gehman J.D., Wade J.D., Masters C.L., Barnham K.J., and Separovic F. Cholesterol and clioquinol modulation of A beta(1-42) interaction with phospholipid bilayers and metals. Biochim. Biophys. Acta-Biomembr. 1768 (2007) 3135-3144
56. Reid P.C., Urano Y., Kodama T., and Hamakubo T. Alzheimer's disease: cholesterol, membrane rafts, isoprenoids and statins. J. Cell. Mol. Med. 11 (2007) 383-392
57. Sponne I., Fifre A., Kriem B., Koziel V., Bihain B., Oster T., Olivier J.L., and Pillot T. Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of the amyloid-beta peptide. FASEB J. 18 (2004) 836-+
58. Ramamoorthy A., Thennarasu S., Tan A., Lee D.K., Clayberger C., and Krensky A.M. Cell selectivity correlates with membrane-specific interactions: a case study on the antimicrobial peptide G15 derived from granulysin. Biochim. Biophys. Acta 1758 (2006) 154-163
59. Ramamoorthy A. Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State NMR Spectrosc. 35 (2009) 201-207
60. Epand R.F., Ramamoorthy A., and Epand R.M. Membrane lipid composition and the interaction of pardaxin: the role of cholesterol. Prot. Peptide Letters 13 (2006) 1-5