Solution structure and membrane interactions of the antimicrobial peptide fallaxidin 4.1a: An NMR and QCM study

Biochemistry

Volumn 48, Issue 50, 2009, Pages 11892-11901

  Sherman, Patrick J ^a   Jackway, Rebecca J ^a   Gehman, John D ^b   Praporski, Slavica ^c   McCubbin, George A ^c   Mechler, Adam ^c   Martin, Lisandra L ^c   Separovic, Frances ^b   Bowie, John H ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CHAIN; ANTIMICROBIAL PEPTIDE; BI-LAYER; CATIONIC ANTIMICROBIAL PEPTIDES; CHEMICAL SHIFT ANISOTROPY; CYTOLYTIC ACTIVITIES; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HEAD GROUPS; HELICAL STRUCTURES; LATERAL PHASE SEPARATION; LIPID MOTIONS; MICROBIAL MEMBRANES; MODEL MEMBRANES; MULTI-LAMELLAR VESICLES; ORDER PARAMETER; PHOSPHOLIPID MEMBRANE; PREFERENTIAL INTERACTION; RANDOM COIL; REAL TIME; SOLUTION STRUCTURES; SUPPORTED LIPID BILAYERS; THRESHOLD CONCENTRATIONS; TRANS-MEMBRANE PORES;

AMINES; CHEMICAL SHIFT; DEUTERIUM; DYES; LIPID BILAYERS; MAGNETIC ANISOTROPY; MAMMALS; MEMBRANES; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDE MINERALS; PEPTIDES; PHASE SEPARATION; PHOSPHOLIPIDS; POLYPEPTIDES; QUARTZ; QUARTZ CRYSTAL MICROBALANCES; RESONANCE;

DRUG INTERACTIONS;

AMPHOLYTE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; DODECYLPHOSPHORYLCHOLINE; FALLAXIDIN 4.1; FALLAXIDIN 4.1A; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMPHIBIA; ANISOTROPY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEUTERON NUCLEAR MAGNETIC RESONANCE; DRUG BINDING; DRUG STRUCTURE; MICELLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPID MEMBRANE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; QUARTZ CRYSTAL MICROBALANCE; SOLID STATE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ANURA; CELL MEMBRANE; CRYSTALLIZATION; DIMYRISTOYLPHOSPHATIDYLCHOLINE; GRAM-POSITIVE BACTERIA; LIPID BILAYERS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; QUARTZ; SOLUTIONS;

AMPHIBIA; BACTERIA (MICROORGANISMS); LITORIA FALLAX; MAMMALIA; PROKARYOTA;

EID: 72449200543     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901668y     Document Type: Article

References (85)

1. Bowan, H. G. (2000) Innate immunity and the normal microflora. Immunol. Rev. 173, 5-16.
2. Strandberg, E., Tiltak, D., Ieronimo, M., Kanithasen, M., Wadhwani, P., and Ulrich, A. S. (2007) Influence of C-terminal amidation on the antimicrobial and haemolytic activities of cationic α-helical peptides. Pure Appl. Chem. 79, 717-728.
3. Simonetti, O., Cirioni, O., Goteri, G., Ghiselli, R., Kamysz, W., Kamysz, E., Silvestri, C., Orlando, F., Barucca, C., Scalise, A., Saba, V., Scalise, G., Giacometti, A., and Offidani, A. (2008) Temporin A is effective in MRSA-infected wounds through bactericidal activity and acceleration of wound repair in a murine model. Peptides 29, 520-528.
4. Livermore, D. (2004) Can better prescribing turn the tide of resistance? Nat. Rev. Microbiol. 2, 73-78.
5. Mazel, D., and Davies, J. (1999) Antibiotic resistance in microbes. Cell. Mol. Life Sci. 56, 742-754.
6. Bechinger, B. (1997) Structure and functions of channel-forming peptides - magainins, cecropins, melittin and alamethicin. J. Membr. Biol. 156, 197-211.
7. Epand, R. M., Shai, Y. C., Segrest, J. P., and Anantharamaiah, G. M. (1995) Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers 37, 319-338.
8. Matsuzaki, K., Sugishita, K., and Miyajima, K. (1999) Interactions of an antimicrobial peptide, magainin 2, with lipopolysaccharide-containing liposomes as a model for outer membranes of Gram-negative bacteria. FEBS Lett. 449, 221-224. (Pubitemid 29192910)
9. Oren, Z., and Shai, Y. (1998) Mode of action of linear amphipathic α-helical antimicrobial peptides. Biopolymers 47, 451-463. (Pubitemid 128637353)
10. Hori, Y., Demura, M., Niidome, T., Aoyagi, H., and Asakura, T. (1999) Orientational behavior of phospholipid membranes with mastoparan studied by 31P solid state NMR. FEBS Lett. 455, 228-232. (Pubitemid 29333041)
11. Sitaram, N., and Nagaraj, R. (2002) The therapeutic potential of host-defense antimicrobial peptides. Curr. Drug Targets 3, 259-267. (Pubitemid 34555498)
12. Van Compernolle, S. E., Taylor, R. J., Oswald-Richter, K., Jiang, J., Youree, B. E., Bowie, J. H., Tyler, M. J., Conlon, J. M., Wade, D., Aiken, C., Dermody, T. S., KewalRamani, V. N., Rollins-Smith, L. A., and Unutmaz, D. (2005) Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J. Virol. 79, 11598-11606. (Pubitemid 41279278)
13. Barra, D., Simmaco, M., and Boman, H. G. (1998) Gene-encoded peptide antibiotics and innate immunity. Do 'animalcules' have defence budgets? FEBS Lett. 430, 130-134.
14. Andreu, D., and Rivas, L. (1998) Animal antimicrobial peptides: An overview. Biopolymers 47, 415-433.
15. Pukala, T. L., Bowie, J. H., Maselli, V. M., Musgrave, I. F., and Tyler, M. J. (2006) Host-defence peptides from the glandular secretions of amphibians: Structure and activity. Nat. Prod. Rep. 23, 368-393.
16. Shai, Y. (1995) Molecular recognition between membrane-spanning polypeptides. Trends Biochem. Sci. 20, 460-464.
17. Shai, Y., and Oren, Z. (2001) From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides 22, 1629-1641.
18. Huang, H. W. (2000) Action of antimicrobial peptides: Two-state model. Biochemistry 39, 8347-8352.
19. Andreu, D., Ubach, J., Boman, A., Wahlin, B., Wade, D., Merrifield, R. B., and Boman, H. G. (1992) Shortened cecropin A-melittin hybrids - significant size reduction retains potent antibiotic activity. FEBS Lett. 296, 190-194.
20. Cornell, B. A., Separovic, F., Baldassi, A. J., and Smith, R. (1988) Conformation and orientation of gramicidin A in oriented phospholipid bilayers measured by solid state carbon-13 NMR. Biophys. J. 53, 67-76. (Pubitemid 18009693)
21. Rozek, T., Bowie, J. H., Wallace, J. C., and Tyler, M. J. (2000) 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, 2002-2011.
22. Wegener, K. L., Wabnitz, P. A., Carver, J. A., Bowie, J. H., Chia, B. C. S., Wallace, J. C., and Tyler, M. J. (1999) Host defence peptides from the skin glands of the Australian Blue Mountains tree frog Litoria citropa. Solution structure of the antibacterial peptide citropin 1.1. Eur. J. Biochem. 265, 627-637.
23. Stone, D. J. M., Waugh, R. J., Bowie, J. H., Wallace, J. C., and Tyler, M. J. (1993) Peptides from Australian frogs. The structures of the caerins from Litoria caerulea, J. Chem. Res. (S) 138, (M) 910-936.
24. Waugh, R. J., Stone, D. J. M., Bowie, J. H., Wallace, J. C., and Tyler, M. J. (1993) Peptides from Australian frogs. The structures of the caerins and caeridins from Litoria gilleni, J. Chem. Res. (S) 139, (M) 937-961.
25. Wegener, K. L., Brinkworth, C. S., Bowie, J. H., Wallace, J. C., and Tyler, M. J. (2001) Bioactive dahlein peptides from the skin secretions of the Australian aquatic frog Litoria dahlii: Sequence determination by electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 15, 1726-1734.
26. Waugh, R. J., Raftery, M. J., Bowie, J. H., Wallace, J. C., and Tyler, M. J. (1996) The structures of the frenatin peptides from the skin secretions of the giant tree frog, Litoria infrafrenata. J. Pept. Sci. 2, 117-124.
27. Rozek, T., Waugh, R. J., Steinborner, S. T., Bowie, J. H., Tyler, M. J., and Wallace, J. C. (1998) The maculatin peptides from the skin glands of the tree frog Litoria genimaculata - a comparison of the structures and antibacterial activities of maculatin 1.1 and caerin 1.1. J. Peptide Sci. 4, 111-115. (Pubitemid 128543157)
28. Brinkworth, C. S., Bowie, J. H., Tyler, M. J., and Wallace, J. C. (2002) A comparison of the host defence skin peptides of the New Guinea tree frog (Litoria genimaculata) and the fringed tree frog (Litoria eucnemis). The link between the caerin and the maculatin antimicrobial peptides. Aust. J. Chem. 55, 605-610.
29. Wong, H., Bowie, J. H., and Carver, J. A. (1997) The solution structure and activity of caerin 1.1, an antimicrobial peptide from the Australian green tree frog, Litoria splendida. Eur. J. Biochem. 247, 545-557.
30. Gehman, J. D., Luc, F., Hall, K., Lee, T.-H., Boland, M. P., Pukala, T. L., Bowie, J. H., Aguilar, M.-I., and Separovic, F. (2008) Effect of antimicrobial peptides from Australian tree frogs on anionic phospholipid membranes. Biochemistry 47, 8557-8565.
31. Apponyi, M. A., Pukala, T. L., Brinkworth, C. S., Maselli, V. M., Bowie, J. H., Tyler, M. J., Booker, G. W., Wallace, J. C., Carver, J. A., Separovic, F., Doyle, J., and Llewellyn, L. E. (2004) Host-defence peptides of Australian anurans: Structure, mechanism of action and evolutionary significance. Peptides 25, 1035-1054. (Pubitemid 38760293)
32. Jackway, R. J., Bowie, J. H., Bilusich, D., Musgrave, I. F., Surinya-Johnson, K. H., Tyler, M. J., and Eichinger, P. C. (2008) The fallaxidin peptides from the skin secretion of the Eastern Dwarf Tree Frog Litoria fallax. Sequence determination by positive and negative ion electrospray mass spectrometry: antimicrobial activity and cDNA cloning of the fallaxidins. Rapid Commun. Mass Spectrom. 22, 3211-3519.
33. Smet, K., and Contreras, R. (2005) Human antimicrobial peptides: Defensins, cathelicidins and histatins. Biotechnol. Lett. 27, 1337-1347.
34. Wang, Z., and Wang, G. (2004) APD: The antimicrobial peptide database. Nucleic Acids Res. 32, D590-D592.
35. Bechinger, B. (2005) Detergent-like properties of magainin antibiotic peptides: a 31P solid-state NMR spectroscopy study. Biochim. Biophys. Acta 1712, 101-108.
36. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462, 157-183.
37. Lu, J., Damodaran, K., Blazyk, J., and Lorigan, G. A. (2005) Solid-state nuclear magnetic resonance relaxation studies of the interaction mechanism of antimicrobial peptides with phospholipid bilayer systems. Biochemistry 44, 10208-10217. (Pubitemid 41076816)
38. Spooner, P. J. R., and Watts, A. (1991) Reversible unfolding of cytochrome c upon interaction with cardiolipin bilayers. II. Evidence from phosphorus-31 NMR measurements doi:10.1021/bi00230a011, Biochemistry 30, 3880-3885.
39. Pukala, T. L., Boland, M. P., Gehman, J. D., Kuhn-Nentwig, L., Separovic, F., and Bowie, J. H. (2007) Solution structure and interaction of cupiennin 1a, a spider venom peptide, with phospholipid bilayers. Biochemistry 46, 3576-3585. (Pubitemid 46449174)
40. Lu, D., Vavasour, I., and Morrow, M. R. (1995) Smoothed acyl chain orientational order parameter profiles in dimyristoylphosphatidylcholine- distearoylphosphatidylcholine mixtures: a 2H-NMR study. Biophys. J. 68, 574-583
41. Watts, A. (1998) Solid-state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochim. Biophys. Acta 1376, 297-318.
42. Tiburu, E. K., Karp, E. S., Birrane, G., Struppe, J. O., Chu, S., Lorigan, G. A., Avraham, S., and Avraham, H. K. (2006) 31P and 2H Relaxation studies of helix vii and the cytoplasmic helix of the human cannabinoid receptors utilizing solid-state NMR techniques. Biochemistry. 45, 7356-7365. (Pubitemid 43877422)
43. Mechler, A., Praporski, S., Piantavigna, S., Heaton, S. M., Hall, K. N., Aguilar, M.-I., and Martin, L. L. (2009) Structure and homogeneity of pseudo-physiological phospholipid bilayers and their deposition characteristics on carboxylic acid terminated self-assembled monolayers. Biomaterials 30, 682-689.
44. Piantavigna, S., Czihal, P., Mechler, A., Richter, M., Hoffmann, R., and Martin, L. (2009) Cell penetrating apidaecin peptide interactions with biomimetic phospholipid membranes. Int. J. Pept. Res. Therap. 15, 139-146.
45. Mechler, A., Praporski, S., Atmuri, K., Boland, M., Separovic, F., and Martin, L. L. (2007) Specific and selective peptide-membrane interactions revealed using quartz crystal microbalance. Biophys. J. 93, 3907-3916. (Pubitemid 350223808)
46. Maeji, N. J., Bray, A. M., Valerio, R. M., and Wang, W. (1995) Larger scale multipin peptide synthesis. J. Pept. Res. 8, 33-38.
47. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967-974.
48. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
49. c-src SH2 domain complexed with a phosphorylated tyrosine pentapeptide. Biochemistry 34, 2107-2121.
50. Nilges, M., Macias, M. J., Odonoghue, S. I., and Oschkinat, H. (1997) Automated NOESY interpretation with ambiguous distance restraints - the refined NMR solution structure of the pleckstrin homology domain from β-spectrin. J. Mol. Biol. 269, 408-422.
51. Linge, J. P., Habeck, M., Rieping, W., and Nilges, M. (2003) ARIA: Automated NOE assignment and NMR structure calculation. Bioinformatics 19, 315-316. (Pubitemid 36181930)
52. Folmer, R. H. A., Hilbers, C. W., Konings, R. N. H., and Nilges, M. (1997) Floating stereospecific assignment revisited - application to an 18 kDa protein and comparison with J-coupling data. J. Biomol. NMR 9, 245-258.
53. Pari, K., Mueller, G. A., DeRose, E. F., Kirby, T. W., and London, R. E. (2003) Solution structure of the RNase H domain of the HIV-1 reverse transcriptase in the presence of magnesium. Biochemistry 42, 639-650. (Pubitemid 36133288)
54. Kang, R. S., Daniels, C. M., Francis, S. A., Shih, S. C., Salerno, W. J., Hicke, L., and Radhakrishnan, I. (2003) Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding. Cell 113, 621-630. (Pubitemid 36694187)
55. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD - visual molecular dynamics. J. Mol. Graphics 14, 33-38.
56. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL - a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55. (Pubitemid 26152976)
57. Massiot, D., Fayon, F., Capron, M., King, I., Le Calvé, S., Durand, J.-O., Bujoli, B., Gan, Z., and Hoatson, G. (2002) Modelling one- and two-dimensional solid-state NMR spectra. Magn. Reson. Chem. 40, 70-76.
58. Smith, I. C. P., and Ekiel, I. H. (1984) Phosphorus-31 NMR of phospholipids in membranes in Phosphorus-31 NMR. Principles and Applications (Garenstein, D. G., Ed.) pp 447-475, Academic Press Inc., London.
59. Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I., and Higgs, T. P. (1976) Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42, 390-394.
60. Whittall, K. P., Sternin, E., Bloom, M., and Mackay, A. L. (1989) Time- and frequency-domain "dePakeing" using inverse theory. J. Magn. Reson. 84, 64-71.
61. Sternin, E., Bloom, M., and MacKay, A. L. (1983) De-Pake-ing of NMR spectra. J. Magn. Reson. 55, 274-282.
62. Galassi, M., Davies, J., Theiler, J., Gough, B., Jungman, G., Booth, M., and Rossi, F. (2008) GNU Scientific Library , 1.11 ed.
63. Williams, T., Kelley, C., Campbell, J., Kotz, D., and Lang, R. (2007) gnuplot, An Interactive Plotting Program, The Free Software Foundation.
64. Jackway, R. J. (2008) Biologically active peptides from Australian amphibians, Ph.D. Thesis, University of Adelaide.
65. Zhou, N. E., Zhu, B., Sykes, B. D., and Hodges, R. S. (1992) Relationship between amide proton chemical shifts and hydrogen bonding in amphipathic α-helical peptides. J. Am. Chem. Soc. 114, 4320-4326.
66. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., and Sykes, B. D. (1995) H-1, C-13 and N-15 random coil NMR chemical shifts of the common amino acids. 1. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5, 67-81.
67. Zhou, N. E., Zhu, B. Y., Sykes, B. D., and Hodges, R. S. (2002) Relationship between amide proton chemical shifts and hydrogen bonding in amphipathic α-helical peptides. J. Am. Chem. Soc. 114, 4320-4326.
68. Wüthrich, K., Billeter, M., and Braun, W. (1984) Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol. 180, 715-740.
69. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta 515, 105-140.
70. Davis, J. H. (1983) The description of membrane lipid conformation, order and dynamics by 2H-NMR. Biochim. Biophys. Acta 737, 117-171.
71. Boden, N., Jones, S. A., and Sixl, F. (1991) On the use of deuterium nuclear magnetic resonance as a probe of chain packing in lipid bilayers. Biochemistry 30, 2146-2155.
72. Lafleur, M., Fine, B., Sternin, E., Cullis, P. R., and Bloom, M. (1989) Smoothed orientational order profile of lipid bilayers by 2H-nuclear magnetic resonance. Biophys. J. 56, 1037-1041
73. Fyfe, C. A. (1983) Solid State NMR for Chemists , CFC Press, Ontario.
74. Balla, M. S., Bowie, J. H., and Separovic, F. (2004) Solid-state NMR study of antimicrobial peptides from Australian frogs in phospholipid membranes. Eur. Biophys. J. 33, 109-116.
75. 31P MAS NMR. Phys. Chem. Chem. Phys. 3, 2904-2910.
76. Otten, D., Brown, M. F., and Beyer, K. (2000) Softening of membrane bilayers by detergents elucidated by deuterium NMR spectroscopy. J. Phys. Chem. B 104, 12119-12129.
77. Zasloff, M. (1987) 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, 5449-5453.
78. Giangaspero, A., Sandri, L., and Tossi, A. (2001) Amphipathic alpha helical antimicrobial peptides. Eur. J. Biochem. 268, 5589-5600.
79. Zelezetsky, I., and Tossi, A. (2006) Alpha-helical antimicrobial peptides - using a sequence template to guide structure-activity relationship studies. Biochim. Biophys. Acta 1758, 1436-1449.
80. Gunasekaran, K., Nagarajaram, H. A., Ramakrishnan, C., and Balaram, P. (1998) Stereochemical punctuation marks in protein structures: glycine and proline containing helix stop signals. J. Mol. Biol. 275, 917-932.
81. Woolfson, D. N., and Williams, D. H. (1990) The influence of proline residues on [alpha]-helical structure. FEBS Lett. 277, 185-188.
82. Pukala, T. L., Bowie, J. H., Maselli, V. M., Musgrave, I. F., and Tyler, M. J. (2006) Host-defense peptides from the glandular secretions of amphibians: structure and activity. Nat. Prod. Rep. 23, 368-393.
83. Rozek, T., Wegener, K. L., Bowie, J. H., Olver, I. N., Carver, J. A., Wallace, J. C., and Tyler, M. J. (2000) The antibiotic and anticancer active aurein peptides from the Australian bell frogs Litoria aurea and Litoria raniformis. The solution structure of aurein 1.2. Eur. J. Biochem. 267, 5330-5341.
84. Kohler, S. J., and Klein, M. P. (1977) Orientation and dynamics of phospholipid head groups in bilayers and membranes determined from 31P nuclear magnetic resonance chemical shielding tensors. Biochemistry 16, 519-526.
85. Yang, L., Harroun, T. A., Weiss, T. M., Ding, L., and Huang, H. W. (2001) Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81, 1475-1485. (Pubitemid 32783588)