Wasp mastoparans follow the same mechanism as the cell-penetrating peptide transportan 10

Biochemistry

Volumn 48, Issue 30, 2009, Pages 7342-7351

  Yandek, Lindsay E ^a   Pokorny, Antje ^a   Almeida, Paulo F F ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC LIPIDS; CELL-PENETRATING PEPTIDE; EXPERIMENTAL DATA; KINETIC MODELS; MECHANISM AND KINETICS; NON-POLAR; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID MEMBRANE; PHOSPHOLIPID VESICLES;

AMINES; CHEMICAL PROPERTIES; LIPOSOMES; PEPTIDES; PHOSPHOLIPIDS; RATE CONSTANTS;

CELL MEMBRANES;

CELL PENETRATING PEPTIDE; DYE; MASTOPARAN; MASTOPARAN L; MASTOPARAN X; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID; TRANSPORTAN 10 PEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL SPECIFICITY; KINETICS; PARAMETER; PRIORITY JOURNAL; PROTEIN BINDING; WASP;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE PERMEABILITY; FLUORESCEINS; FLUORESCENT DYES; GALANIN; HUMANS; LIPID BILAYERS; MEMBRANE LIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NAPHTHALENES; PEPTIDES; PHOSPHOLIPIDS; PROTEIN ISOFORMS; PYRIDINIUM COMPOUNDS; RECOMBINANT FUSION PROTEINS; THERMODYNAMICS; WASP VENOMS; WASPS;

VESPA XANTHOPTERA; VESPULA LEWISII;

EID: 68049089697     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9008243     Document Type: Article

References (56)

1. Pokorny, A., Birkbeck, T. H., and Almeida, P. F. F. (2002) Mechanism and kinetics of δ-lysin interaction with phospholipid vesicles. Biochemistry 41, 11044-11056.
2. Pokorny, A., and Almeida, P. F. F. (2004) Kinetics of dye efflux and lipid flip-flop induced by δ-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic. α-helical peptides. Biochemistry 43, 8846-8857.
3. Gregory, S. M., Cavenaugh, A. C., Journigan, V., Pokorny, A., and Almeida, P. F. F. (2008) A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide cecropin A. Biophys. J. 94, 1667-1680.
4. Gregory, S. M., Pokorny, A., and Almeida, P. F. F. (2009) Magainin 2 revisited: a test of the quantitative model for the all-or-none permeabilization of phospholipid vesicles. Biophys. J. 96, 116-131.
5. Yandek, L. E., Pokorny, A., Floren, A., Knoelke, K., Langel, U., and Almeida, P. F. F. (2007) Mechanism of the cell-penetrating peptide Tp10 permeation of lipid bilayers. Biophys. J. 92, 2434-2444.
6. Yandek, L. E., Pokorny, A., and Almeida, P. F. F. (2008) Small changes in the primary structure of transportan 10 alter the thermodynamics and kinetics of its interaction with phospholipid vesicles. Biochemistry 47, 3051-3060.
7. Soomets, U., Lindgren, M., Gallet, X., Hallbrink, M., Elmquist, A., Balaspiri, L., Zorko, M., Pooga, M., Brasseur, R., and Langel, U. (2000) Deletion analogues of transportan. Biochim. Biophys. Acta 1467, 165-176.
8. Hällbrink, M., Floren, A., Elmquist, A., Pooga, M., Bartfai, T., and Langel, U. (2001) Cargo delivery kinetics of cell-penetrating peptides. Biochim. Biophys. Acta 1515, 101-109.
9. Hirai, Y. (1978) A new mast cell degranulating peptide "mastoparan" in the wasp venom, in .Peptide Chemistry (Shiba, T., Ed.) pp 155-160, Protein Research Foundation, Osaka, Japan.
10. Hirai, Y., Yasuhara, T., Yoshida, H., Nakajima, T., Fujino, M., and Kitada, C. (1979) A new mast cell degranulating peptide "mastoparan" in the venom of Vespula lewisii. Chem. Pharm. Bull. 27, 1942-1944.
11. Higashijima, T., Wakamatsu, K., Takemitsu, M., Fujino, M., Nakajima, T., and Miyazawa, T. (1983) Conformational change of mastoparan from wasp venomon binding with phospholipid membrane. FEBS Lett. 152, 227-230.
12. Vold, R. R., Prosser, R. S., and Deese, A. J. (1997) Isotropic solutions of phospholipid bicelles: A new membrane mimetic for high-resolution NMR studies of polypeptides. J. Biomol. NMR 9, 329-335.
13. 15N-NMR spectroscopy in oriented lipid bilayers. Eur. J. Biochem. 268, 302-309.
14. Wakamatsu, K., Higashijima, T., Fujino, M., Nakajima, T., and Miyazawa, T. (1983) Tranferred NOE analyses of conformations of peptides as bound to membrane bilayer of phospholipid; mastoparan-X. FEBS Lett. 162, 123-126.
15. Whiles, J. A., Brasseur, R., Glover, K. J., Melacini, G., Komives, E. A., and Vold, R. R. (2001) Orientation and effects of mastoparan X on phospholipid bicelles. Biophys. J. 80, 280-293.
16. 1H-depolarization under magic-angle spinning. J. Am. Chem. Soc. 128, 10654-10655.
17. Todokoro, Y., Yumen, I., Fukushima, K., Kang, S.-W., Park, J.-S., Kohno, T., Wakamatsu, K., Akutsu, H., and Fujiwara, T. (2006) Structure of tightly membrane-bound mastoparan-X, a G-protein-activating peptide, determined by solid-state NMR. Biophys. J. 91, 1368-1379.
18. Sforça, M. L., Oyama, S. Jr., Canduri, F., Lorenzi, C. C. B., Pertinhez, T. A., Konno, K., Souze, B. M., Palma, M. S., Neto, J. R., Azavedo, W. F. Jr., and Spisni, A. (2004) How C-terminal carboxyamidation alters the biological activity of peptides from the venom of the eumenine solitary wasp. Biochemistry 43, 5608-5617.
19. Arbuzova, A., and Schwarz, G. (1999) Pore-forming action of mastoparan peptides on liposomes: a quantitative analysis. Biochim. Biophys. Acta 1420, 139-152.
20. Hellmann, N., and Schwarz, G. (1998) Peptide-liposome association. A critical examination with mastoparan-X. Biochim. Biophys. Acta 1369, 267-277.
21. Matsuzaki, K., Yoneyama, S., Murase, O., and Miyajima, K. (1996) Transbilayer transport of ions and lipids coupled with mastoparan X translocation. Biochemistry 35, 8450-8456.
22. Tang, J., Signarvic, R. S., DeGrado, W. F., and Gai, F. (2007) Role of helix nucleation in the kinetics of binding of mastoparan X to phospholipid bilayers. Biochemistry 46, 13865-113863
23. Schwarz, G., and Arbuzova, A. (1995) Pore kinetics reflected in the dequenching of a lipid vesicle entrapped fluorescent dye. Biochim. Biophys. Acta 1239, 51-57.
24. Arbuzova, A., and Schwarz, G. (1996) Pore kinetics of mastoparan peptides in large unilamellar lipid vesicles. Prog. Colloid Polym. Sci. 100, 345-350.
25. Schwarz, G., and Robert, C. H. (1990) Pore formation kinetics in membranes, determined from the release of marker molecules out of liposomes or cells. Biophys. J. 58, 577-583.
26. Schwarz, G., and Robert, C. H. (1992) Kinetics of pore-mediated release of marker molecules from liposomes or cells. Biophys. Chem. 42, 291-296.
27. Rex, S., and Schwarz, G. (1998) Quantitative studies of the melittin-induced leakagemechanism of lipid vesicles. Biochemistry 37, 2336-2345.
28. Sakai, N., and Matile, S. (2003) Anion-mediated transfer of polyarginine across liquid and bilayer membranes. J. Am. Chem. Soc. 125, 14348-14356.
29. Sakai, N., Takeuchi, T., Futaki, S., and Matile, S. (2005) Direct observation of anion-mediated translocation of fluorescent oligoarginine carriers into and cacross bulk liquid and anionic bilayer membranes. ChemBioChem 6, 114-122.
30. White, S. H., and Wimley, W. C. (1999) Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28, 319-365.
31. Haugland, R. P. (2002) Handbook of Fluorescent Probes and Research Products , 9th ed., pp 66-73, Molecular Probes, Eugene, OR.
32. Bartlett, G. R. (1959) Phosphorous assay in column chromatography. J. Biol. Chem. 234, 466-468.
33. Luo, P., and Baldwin, R. L. (1997) Mechanism of helix induction by trifluoroethanol: A framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry 36, 8413-8421.
34. Wimley, W. C., Selsted, M. E., and White, S. H. (1994) Interactions between human defensins and lipid bilayers: Evidence for formation of multimeric pores. Protein Sci. 3, 1362-1373.
35. Ladokhin, A. S., Wimley, W. C., and White, S. H. (1995) Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching. Biophys. J. 69, 1964-1971.
36. Ladokhin, A. S., Wimley, W. C., Hristova, K., and White, S. H. (1997) Mechanism of leakage of contents of membrane vesicles determined by fluorescence requenching. Methods Enzymol. 278, 474-486.
37. Press, W. H., Teukolsky, S. A., Vetterling, W. T., and Flannery, B. P. (1994) Numerical Recipes in Fortran , 2nd ed., Cambridge University Press, New York.
38. Jaysinghe, S., Hristova, K., Wimley, W., Snider, C., and White, S. H. (2009) http://blanco.biomol.uci.edu/mpex.
39. Helfrich, W. (1973) Elastic properties of lipid bilayers: Theory anbd possible experiments. Z. Naturforsch. 28c, 693-703.
40. Pokorny, A., Kilelee, E. M., Wu, D., and Almeida, P. F. F. (2008) The activity of the amphipathic peptide δ-lysin correlates with phospholipid acyl chain structure and bilayer elastic properties. Biophys. J. 95, 4748-4755.
41. Wimley, W. C., and White, S. H. (1996) Experimentally determined hydrophobicity scale of proteins at membrane interfaces. Nat. Struct. Biol. 3, 842-848.
42. Hristova, K., and White, S. H. (2005) An experiment-based algorithm for predicting the partitioning of unfolded peptides into phosphatidylcholine bilayer interfaces. Biochemistry 44, 12614-12619.
43. Ladokhin, A. S., and White, S. H. (1999) Folding if amphipathic R-helices on membranes: Energetics of helix formation by melittin. J. Mol. Biol. 285, 1363-1369.
44. Wimley, W. C., Creamer, T. P., and White, S. H. (1996) Solvation energies of amino acid side chains and backbone in a family of host-guest peptapeptides. Biochemistry 35, 5109-5124.
45. Jaysinghe, S., Hristova, K., and White, S. H. (2001) Energetics, stability, and prediction of transmembrane helices. J. Mol. Biol. 312, 927-934.
46. Matsuzaki, K., Sugishita, K., Ishibe, N., Ueha, M., Nakata, S., Miyajima, K., and Epand, R. M. (1998) Relationship of membrane curvature to formation of pores by magainin 2. Biochemistry 37, 11856-11863.
47. 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.
48. Huang, H. W. (2000) Action of antimicrobial peptides: two-state model. Biochemistry 39, 8347-8352.
49. Ludtke, S. J., He, K., and Huang, H. W. (1995) Membrane thinning by magainin 2. Biochemistry 34, 16764-16769.
50. Lee, M. T., Chen, F. Y., and Huang, H. W. (2004) Energetics of pore formation induced by membrane active peptides. Biochemistry 43, 3590-3599.
51. Huang, H. W., Chen, F.-Y., and Lee, M.-T. (2004) Molecular mechanism of peptide-induced pores inmembranes. Phys. Rev. Lett. 92, 198304.
52. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236-248.
53. Magzoub, M., Kilk, K., Eriksson, L. E .G., Langel, U., and Gräslund, A. (2001) Interaction and struture induction of cell-penetrating peptides in the presence of phospholipid vesicles. Biochim. Biophys. Acta 1512, 77-89.
54. Leontiadou, H., Mark, A. E., and Marrink, S. J. (2006) Antimicrobial peptides in action. J. Am. Chem. Soc. 128, 12156-12161.
55. Herce, H. D., and Garcia, A. E. (2007) Molecular dynamics simulations suggest amechanismfor translocation of the HIV-1TATpeptide across lipid membranes. Proc. Natl. Acad. Sci. U.S.A. 104, 20805-20810.
56. Binder, H., and Lindblom, G. (2003) Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes. Biophys. J. 85, 982-995.