Structural aspects of the interaction of peptidyl-glycylleucine-carboxyamide, a highly potent antimicrobial peptide from frog skin, with lipids

European Journal of Biochemistry

Volumn 248, Issue 3, 1997, Pages 938-946

  Latal, Angelika ^a   Degovics, Gabor ^a   Epand, Raquel F ^b   Epand, Richard M ^b   Lohner, Karl ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Calorimetry; Circular dichroism; Membrane domain; Peptide antibiotic; X ray diffraction

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT;

ANIMAL TISSUE; ARTICLE; ARTIFICIAL MEMBRANE; BACTERIAL MEMBRANE; CALORIMETRY; CIRCULAR DICHROISM; CONTROLLED STUDY; ERYTHROCYTE MEMBRANE; FROG; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SKIN; THERMODYNAMICS; X RAY DIFFRACTION;

ANIMALIA; ANURA; BACTERIA (MICROORGANISMS); XENOPUS (GENUS); XENOPUS LAEVIS;

EID: 0030863833     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00938.x     Document Type: Article

References (74)

1. a-(4-24)] from skin secretion of Xenopus laevis, Eur. J. Biochem. 149, 531-535.
2. Bartlett, G. R. (1959) Phosphorus assay in column chromatography, J. Biol. Chem. 234, 466-486.
3. Batenburg, A. M., van Esch, J. H. & de Kruijff, B. (1988) Melittin-induced changes of the macroscopic structure of phosphatidylethanolamines, Biochemistry 27, 2324-2331.
4. Bhakoo, M., Birkbeck, T. H. & Freer, J. H. (1982) Interaction of Staphylococcus aureus δ-lysin with phospholipid monolayers, Biochemistry 21, 6879-6883.
5. Boman, H. G., Wade, D., Boman, I. A., Wahlin, B. & Merrifield, R. B. (1989) Antibacterial and antimalarial properties of peptides that are cecropin-melittin hybrids, FEBS Lett. 259, 103-106.
6. Chang, C. T., Wu, C.-S. C. & Yang, J. T. (1978) Circular dichroic analysis of protein conformation: Inclusion of the β-turns, Anal. Biochem. 91, 13-31.
7. Chen, G. C. & Yang, J. T. (1977) 2-Point calibration of circular dichrometer with D-10-camphorsulfonic acid, Anal. Lett. 10, 1195-1207.
8. Chen, H. C., Brown, J. H., Morell, J. L. & Huang, C. M. (1988) Synthetic magainin analogs with improved antimicrobial activity, FEBS Lett. 236, 462-466.
9. Ceve, G., Marsh, D. & Watts, A. (1980) Non-electrostatic contribution to the titration of the ordered-fluid phase-transition of phosphatidylglycerol bilayers, FEBS Lett. 120, 267-270.
10. Dathe, M., Schümann, M., Wieprecht, T., Winkler, A., Beyermann, M., Krause, E., Matsuzaki, K., Murase, O. & Bienert, M. (1996) Peptide helicity and membrane surface charge modulate the balance of electrostatic and hydrophobic interactions with lipid bilayers and biological mebranes, Biochemistry 35, 12612-12622.
11. Davies, J. (1996) Bacteria on the rampage, Nature 383, 219-220.
12. Degovics, G., Latal, A., Prenner, E., Kriechbaum, M. & Lohner, K. (1997) Structure and thermotropic behaviour of mixed choline phospholipid model membranes, J. Appl. Crystallogr., in the press.
13. Dempsey, C. E. (1990) The actions of melittin on membranes, Biochim. Biophys. Acta 1031, 143-161.
14. Epand, R. M., Colescott, R. L., Epand, R. F. & Orlowski, R. C. (1986) Conformational flexibility and biological activity of Salmon-calcitonin, Biochemistry 25, 1964-1968.
15. Epand, R. M. & Hui, S.-W. (1986) Effect of electrostatic repulsion on the morphology and thermotropic transitions of anionic phospholipids, FEBS Lett. 209, 257-260.
16. Erspamer, V. (1984) Half a century of comparative research on biogenicamines and active peptides in amphibian skin and molluscan tissues, Comp. Biochem. Biophysiol. C-Comp. Pharmacol. Toxicol. 79, 1-7.
17. Fasman, G. D. (1989) Prediction of protein structure and the principles of protein conformation (Fasman, G. D., ed.) pp. 193-316, Plenum Press, New York.
18. Gazit, E., Lee, W.-J, Brey, P. T. & Shai, Y. (1994) Mode of action of the antibacterial cecropin B2: A spectrofluorometric study, Biochemistry 33, 10 681-10 692.
19. Gazit, E., Boman, A., Boman, H. G. & Shai, Y. (1995) Interaction of the mammalian antibacterial peptide cecropin P1 with phospholipid vesicles, Biochemistry 34, 11 479-11 488.
20. Giovannini, M. G., Poulter, L., Gibson, B. W. & Williams, D. H. (1987) Biosynthesis and degradation of peptides derived from Xenopus laevis prohormones, Biochem. J. 234, 113-120.
21. Glatter, O. (1991) Scattering studies on colloids of biological interest (amphiphilic systems), Prog. Colloid Polym. Sci. 84, 46-54.
22. Habermann, E. & Jentsch, J. (1967) Sequenzanalyse des Melittins aus den tryptischen und peptischen Spaltstücken des Bienengiftes, Hoppe-Seyler's Z. Physiol. Chem. 348, 37-50.
23. Hamed, M. M., Mattice, W. L. & Robinson, R. M. (1983) Behavior of amphipathic helices on analysis via matrix-methods, with application to glucagon, secretin, and vasoactive intestinal peptide, Biopolymers 22, 1003-1021.
24. Hill, C. P., Yee, J., Selsted, M. E. & Eisenberg, D. (1991) Crystal structure of defensin HNP-3, an amphiphilic dimer: Mechanisms of membrane permeabilization, Science 251, 1481-1485.
25. Hirsch, D. J., Hammer, J., Maloy, W. L., Blazyk, J. & Schaefer, J. (1996) Secondary structure and location of a magainin analogue in synthetic phospholipid bilayers, Biochemistry 35, 12 733-12 741.
26. a and its precursor as predicted from cloned mRNA of Xenopus laevis skin, EMBO J. 2, 711-714.
27. Holak, T. A., Engström, A., Kraulis, P. J., Lindeberg, G., Bennich, H., Jones, T. A., Gronenborn, A. M. & Clore, G. M. (1988) The solution conformation of the antibacterial peptide cecropin A: a nuclear magnetic resonance and dynamical simulated annealing study, Biochemistry 27, 7620-7629.
28. Jackson, M., Mantsch, H. H. & Spencer, J. H. (1992) Conformation of magainin-2 and related peptides in aqueous solution and membrane environments probed by Fourier transform infrared spectroscopy, Biochemistry 31, 7289-7293.
29. Juretic, D., Hendler, R. W., Brown, J. H., Chen, H. C., Morell, J. L. & Westerhoff, H. V. (1989) Magainin-2 amide and analogs - antimicrobial activity, membrane depolarization and susceptibility to proteolysis, FEBS Lett. 249, 219-223.
30. Karplus, P. A. & Schulz, G. E. (1985) Prediction of chain flexibility in proteins - a tool for the selection of peptide antigens, Naturwissenschaften 72, 212-213.
31. Kawano, K., Yoneya, T., Miyata, T., Yoshikawa, K., Tokunaga, F., Terada, Y. & Iwanega, S. (1990) Antimicrobial peptide, tachyplesin-I, isolated from hemocytes of the horseshoe-crab (Tachypleus tridentatus) - NMR determination of the beta-sheet structure, J. Biol. Chem. 265, 5365-5367.
32. Kiyota, T., Lee, S. & Sugihara, G. (1996) Design and synthesis of amphiphilic alpha-helical model peptides with systematically varied hydrophobic-hydrophilic balance and their interaction with lipid-membrane and bio-membrane, Biochemistry 35, 13 196-13 204.
33. Kokryakov, V. N., Harwig, S. S. L., Panyutich, E. A., Shevchenko, A. A., Aleshina, G. M., Shamova, O. V., Korneva, H. A. & Lehrer, R. I. (1993) Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins, FEBS Lett. 327, 231-236.
34. Laggner, P. & Mio, H. (1992) SWAX - A dual-detector camera for simultaneous small- and wide-angle X-ray diffraction in polymer and liquid crystall research, Nucl. Instr. Methods Phys. Res. A 323, 86-90.
35. Laggner, P (1994) X-Ray diffraction on biomembranes with emphasis on lipid moiety, Subcell. Biochem. 23, 451-491.
36. Latal, A., Lehrer, R., Harwig, S. S. L. & Lohner, K. (1996) Interaction of enantiometric protegrins with liposomes, Prog. Biophys. Mol. Biol. 65 (Suppl. 1), 121.
37. Lehrer, R. I., Ganz, T. & Selsted, M. E. (1991) Defensins: endogenous antibiotic peptides of animal cells, Cell 64, 229-230.
38. Lohner, K. (1991) Effects of small organic molecules on phospholipid phase transitions, Chem. Phys. Lipids 57, 341-362.
39. Lohner, K. & Epand R. M. (1997) Membrane interactions of hemolytic and antibacterial peptides, Adv. Biophys. Chem. 6, 53-56.
40. Lohner, K., Latal, A., Lehrer, R. I. & Ganz, T. (1997) Differential scanning microcalorimetry indicates that human defensin, HNP-2, interacts specifically with biomembrane mimetic systems, Biochemistiy 6, 1525-1531.
41. Manavalan, P. & Ponnuswamy, P. K. (1978) Hydrophobic character of amino acid residues in globular proteins, Nature 275, 673-674.
42. Marsh, D. (1990) Handbook of lipid bilayers (D. Marsh, ed.) pp. 135-162, CRC Press, Boca Raton FL.
43. Matsuzaki, K., Miyajima, K., Funakoshi, S., Fujii, N., Handa, T., Harada, M. & Yajima, H. (1989) Magainin 1-induced leakage of entrapped calcein out of negatively-charged lipid vesicles, Biochim. Biophys. Acta 981, 130-134.
44. Matsuzaki, K., Fukui, M., Fujii, N. & Miyjima, K. (1993) Permeabilization and morphological changes in phosphatidylglycerol bilayers induced by an antimicrobial peptide, tachyplesin-I, Colloid Polym. Sci. 271, 901-908.
45. Matsuzaki, K., Murase, O., Tokuda, H., Funakoshi, S., Fujii, N. & Miyajima, K. (1994) Orientational and aggregational states of magainin 2 in phospholipid bilayers, Biochemistry 33, 3342-3349.
46. Matsuzaki, K., Murase, O., Fujii, N. & Miyajima, K. (1995) Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore, Biochemistry 34, 6521-6526.
47. Matsuzaki, K., Murase, O., Fujii, N. & Miyajima, K. (1996a) An antimicrobal peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation, Biochemistry 35, 11 361-11 368.
48. Matsuzaki, K., Yoneyama, S., Murase, O. & Miyajima, K. (1996b) Transbilayer transport of ions and lipids coupled with mastoparan-X translocation, Biochemistry 35, 8450-8456.
49. Mattice, W. L. & Robinson, R. M. (1981) Conformational properties of central nervous-system myelin basic-protein, beta-endorphin, and beta-lipotropin in water and in the presence of anionic lipids, Biopolymers 20, 1421-1434.
50. McElhaney, R. N. (1982) The use of differential scanning calorimetry and differential thermal-analysis in studies of model and biological-membranes, Chem. Phys. Lipids 30, 229-259.
51. Mchaourab, H. S., Hyde, J. S. & Feix, J. B. (1994) Binding and state of aggregation of spin-labelled cecropin AD in phospholipid bilayers: effects of surface charge and fatty acyl chain length, Biochemistry 33, 6691-6699.
52. Merrifield, R. B. (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide, J. Am. Chem. Soc. 85, 2149-2154.
53. Mor, A. & Nicolas, P. (1994) Isolation and structure of novel defensive peptides from frog skin, Eur. J. Biochem. 219, 145-154.
54. Nakamura, T., Furunaka, H., Miyata, T., Tokunaga, F., Muta, T., Iwanaga, S., Niwa, M., Takao, T. & Shimonishi, Y. (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoecrab (Tachyplesus tridentatus) - isolation and chemical structure, J. Biol. Chem. 263, 6709-6713.
55. O'Leary, W. M. & Wilkinson, S. G. (1988) Gram-positive bacteria, in Microbial lipids (Ratledge, C. & Wilkinson, S. G., eds) pp. 117-201, Academic Press, London.
56. Opden-Kamp J. A. F. (1979) Lipid asymmetry in membranes, Annu. Rev. Biochem. 48, 47-71.
57. Oren, Z. & Shai, Y. (1997) Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study, Biochemistry 36, 1826-1835.
58. Saberwal, G. & Nagaraj, R. (1994) Cell-lytic and antibacterial peptides that act by perturbing the barrier function of membranes - facets of their conformational features, structure-function correlations and membrane-perturbing abilities, Biochim. Biophys. Acta 1197, 109-131.
59. Service, R. F. (1995) Antibiotics that resist resistance, Science 5237, 724-727.
60. Sessa, G., Freer, J. H., Colacicco, G. & Weissmann, G. (1969) Interaction of a lytic polypeptide, melittin, with lipid membrane systems, J. Biol. Chem. 244, 3575-3582.
61. Sipos, D., Andersson, M & Ehrenberg, A. (1992) The structure of the mammalian antibacterial peptide cecropin-P1 in solution, determined by proton-NMR, Eur J. Biochem. 209, 163-169.
62. Sitaram, N. & Nagaraj, R. (1993) Interaction of the 47-residue antibacterial peptide seminalplasmin and its 13-residue fragment which has antibacterial and hemolytic activities with model membranes, Biochemistry 32, 3124-3130.
63. Soravia, E., Martini, G. & Zasloff, M. (1988) Antimicrobial properties of peptides from Xenopus granular gland secretions, FEBS Lett. 228, 337-340.
64. Strahilevitz, J., Mor, A., Nicolas, P. & Shai, Y. (1994) Spectrum of antimicrobial activity and assembly of dermaseptin-b and its precursor form in phospholipid membranes, Biochemistry 33, 10 951-10 960.
65. Takahashi, H., Matuoka, S., Kato, S., Ohki, K. & Hatta, I. (1992) Effects of poly(l-lysine) on the structural and thermotropic properties of dipalmitoylglycerophosphoglycerol bilayers, Biochim. Biophys. Acta 1110, 29-36.
66. Tardieu, A., Luzzati, V. & Reman, F. C. (1973) Structure and polymorphism of the hydrocarbon chains of lipids: a study of lecithin-water phases, J. Mol. Biol. 75, 711-733.
67. Tenchov, B. (1991) On the reversibility of the phase transitions in lipid-water systems, Chem. Phys. Lipids 57, 165-177.
68. Tytler, E. M., Anantharamaiah, G. M. Walker, D. E., Mishra, V. K., Palgunachari, M. N. & Segrest, J. P. (1995) Molecular basis for prokaryotic specificity of magainin-induced lysis, Biochemistry 34, 4393-4401.
69. Wade, D., Boman, A., Wahlin, B., Drain, C. M., Andreu, D., Boman, H. G. & Merrifield, R. B. (1990) All-d amino acid-containing channel-forming antibiotic peptides, Proc. Natl Acad. Sci. USA 87, 4761-4765.
70. Watts, A., Harlos, K. & Marsh, D. (1981) Charge-induced tilt in ordered-phase phosphatidylglycerol bilayers - evidence from X-ray diffraction, Biochim. Biophys. Acta 645, 91-96.
71. White, S. H., Wimley, W. C. & Selsted, M. E. (1995) Structure, function, and membrane integration of defensins, Curr. Opin. Struct Biol. 5, 521-527.
72. Wilkinson, D. A., Tirrell, D. A., Turek, A. B. & McIntosh, T. J. (1987) Tris buffer causes acyl chain interdigitation in phosphatidylglycerol, Biochim. Biophys. Acta 905, 447-453.
73. Wilkinson, D. A. & McIntosh, T. J. (1986) A subtransition in a phospholipid with a net charge, dipalmitoylglycerol, Biochemistry 25, 295-298.
74. Williams, R. W., Starman, R., Taylor, K. M. P., Gable, K., Beeler, T., Zasloff, M. & Covell, D. (1990) Raman spectroscopy of synthetic antimicrobial frog peptides magainin 2a and PGLa, Biochemistry 29, 4490-4496.