Action mechanism of tachyplesin I and effects of PEGylation

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 5, 2007, Pages 1160-1169

  Imura, Yuichi ^a   Nishida, Minoru ^a   Ogawa, Yoshiyuki ^a   Takakura, Yoshinobu ^a   Matsuzaki, Katsumi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Antimicrobial peptide; Lipid flip flop; Membrane permeabilization; PEGylation; Peptide lipid interaction; Tachyplesin I

Indexed keywords

CALCEIN; LEVO ALPHA PHOSPHATIDYLCHOLINE; LEVO ALPHA PHOSPHATIDYLGLYCEROL; PEPTIDOGLYCAN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; TACHYPLESIN; TACHYPLESIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; DNA BINDING; DRUG MECHANISM; LIPID BILAYER; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL DEATH; CELL MEMBRANE PERMEABILITY; CHO CELLS; CIRCULAR DICHROISM; CRICETINAE; CRICETULUS; DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI; FLUORESCEINS; FLUORESCENCE; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PEPTIDES; PEPTIDES, CYCLIC; POLYETHYLENE GLYCOLS; PROTEIN BINDING; PROTEIN TRANSPORT; STAPHYLOCOCCUS EPIDERMIDIS; TRYPTOPHAN; UNILAMELLAR LIPOSOMES;

TACHYPLEUS TRIDENTATUS;

EID: 34047271928     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.01.005     Document Type: Article

References (55)

1. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
2. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev., Microbiol. 3 (2005) 238-250
3. Harris J.M., and Chess R.B. Effect of PEGylation on pharmaceuticals. Nat. Rev., Drug Discov. 2 (2003) 214-221
4. Steinberg D.A., Hurst M.A., Fujii C.A., Kung A.H., Ho J.F., Cheng F.C., Loury D.J., and Fiddes J.C. Protegrin-1: a broad-spectrum, rapidly microbicidal peptide with in vivo activity. Antimicrob. Agents Chemother. 41 (1997) 1738-1742
5. Darveau R.P., Cunningham M.D., Seachord C.L., Cassiano-Clough L., Cosand W.L., Blake J., and Watkins C.S. Beta-lactam antibiotics potentiate magainin 2 antimicrobial activity in vitro and in vivo. Antimicrob. Agents Chemother. 35 (1991) 1153-1159
6. Johansson J., Gudmundsson G.H., Rottenberg M.E., Berndt K.D., and Agerberth B. Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem. 273 (1998) 3718-3724
7. Yeaman M.R., Gank K.D., Bayer A.S., and Brass E.P. Synthetic peptides that exert antimicrobial activities in whole blood and blood-derived matrices. Antimicrob. Agents Chemother. 46 (2002) 3883-3891
8. Matsuzaki K., Sugishita K., Harada M., Fujii N., and Miyajima K. Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of Gram-negative bacteria. Biochim. Biophys. Acta 1327 (1997) 119-130
9. Ahmad I., Perkins W.R., Lupan D.M., Selsted M.E., and Janoff A.S. Liposomal entrapment of the neutrophil-derived peptide indolicidin endows it with in vivo antifungal activity. Biochim. Biophys. Acta 1237 (1995) 109-114
10. Szebeni J., Baranyi L., Savay S., Bodo M., Morse D.S., Basta M., Stahl G.L., Bunger R., and Alving C.R. Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction. Am. J. Physiol, Heart Circ. Physiol. 279 (2000) H1319-H1328
11. Abuchowski A., McCoy J.R., Palczuk N.C., van Es T., and Davis F.F. Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase. J. Biol. Chem. 252 (1977) 3582-3586
12. Guiotto A., Pozzobon M., Canevari M., Manganelli R., Scarin M., and Veronese F.M. PEGylation of the antimicrobial peptide nisin A: problems and perspectives. Farmaco 58 (2003) 45-50
13. Nakamura T., Furunaka H., Miyata T., Tokunaga F., Muta T., Iwanaga S., Niwa M., Takao T., and Shimonishi Y. Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. J. Biol. Chem. 263 (1988) 16709-16713
14. Matsuzaki K., Yoneyama S., Fujii N., Miyajima K., Yamada K., Kirino Y., and Anzai K. Membrane permeabilization mechanisms of a cyclic antimicrobial peptide, tachyplesin I, and its linear analog. Biochemistry 36 (1997) 9799-9806
15. Ramamoorthy A., Thennarasu S., Tan A., Gottipati K., Sreekumar S., Heyl D.L., An F.Y., and Shelburne C.E. Deletion of all cysteines in tachyplesin I abolishes hemolytic activity and retains antimicrobial activity and lipopolysaccharide selective binding. Biochemistry 45 (2006) 6529-6540
16. Rao A.G. Conformation and antimicrobial activity of linear derivatives of tachyplesin lacking disulfide bonds. Arch. Biochem. Biophys. 361 (1999) 127-134
17. Doherty T., Waring A.J., and Hong M. Peptide-lipid interactions of the beta-hairpin antimicrobial peptide tachyplesin and its linear derivatives from solid-state NMR. Biochim. Biophys. Acta 1758 (2006) 1285-1291
18. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1376 (1998) 391-400
19. Huang H.W. Molecular mechanism of antimicrobial peptides: the origin of cooperativity. Biochim. Biophys. Acta 1758 (2006) 1292-1302
20. Yonezawa A., Kuwahara J., Fujii N., and Sugiura Y. Binding of tachyplesin I to DNA revealed by footprinting analysis: significant contribution of secondary structure to DNA binding and implication for biological action. Biochemistry 31 (1992) 2998-3004
21. Akaji K., Fujii N., Tokunaga F., Miyata T., Iwanaga S., and Yajima H. Studies on peptides: CLXVIII. Synthesis of three peptides isolated from horseshoe crab hemocytes, tachyplesin I, tachyplesin II, and polyphemusin I. Chem. Pharm. Bull. 37 (1989) 2661-2664
22. Matsuzaki K., Murase O., Tokuda H., Funakoshi S., Fujii N., and Miyajima K. Orientational and aggregational states of magainin 2 in phospholipid bilayers. Biochemistry 33 (1994) 3342-3349
23. Bartlett G.R. Phosphorus assay in column chromatography. J. Biol. Chem. 234 (1959) 466-468
24. Müller P., Schiller S., Wieprecht T., Dathe M., and Herrmann A. Continuous measurement of rapid transbilayer movement of a pyrene-labeled phospholipid analogue. Chem. Phys. Lipids 106 (2000) 89-99
25. Matsuzaki K., Nakai S., Handa T., Takaishi Y., Fujita T., and Miyajima K. Hypelcin A, an alpha-aminoisobutyric acid containing antibiotic peptide, induced permeability change of phosphatidylcholine bilayers. Biochemistry 28 (1989) 9392-9398
26. Matsuzaki K., Yoneyama S., and Miyajima K. Pore formation and translocation of melittin. Biophys. J. 73 (1997) 831-838
27. Vanderkooi J.M., Callis J.B., and Pyrene. A probe of lateral diffusion in the hydrophobic region of membranes. Biochemistry 13 (1974) 4000-4006
28. Kobayashi S., Takeshima K., Park C.B., Kim S.C., and Matsuzaki K. Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry 39 (2000) 8648-8654
29. Ishiyama M., Shiga M., Sasamoto K., Mizoguchi M., and He P.G. A new sulfonated tetrazolium salt that produces a highly water-soluble formazan dye. Chem. Pharm. Bull. 41 (1993) 1118-1122
30. Lehrer R.I., Barton A., Daher K.A., Harwig S.S., Ganz T., and Selsted M.E. Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity. J. Clin. Invest. 84 (1989) 553-561
31. Hancock R.E. Alterations in outer membrane permeability. Annu. Rev. Microbiol. 38 (1984) 237-264
32. Huber R.E., Parfett C., Woulfe-Flanagan H., and Thompson D.J. Interaction of divalent cations with beta-galactosidase (Escherichia coli). Biochemistry 18 (1979) 4090-4095
33. Birdsell D.C., and Cota-Robles E.H. Production and ultrastructure of lysozyme and ethylenediaminetetraacetate-lysozyme spheroplasts of Escherichia coli. J. Bacteriol. 93 (1967) 427-437
34. Hirakura Y., Kobayashi S., and Matsuzaki K. Specific interactions of the antimicrobial peptide cyclic beta-sheet tachyplesin I with lipopolysaccharides. Biochim. Biophys. Acta 1562 (2002) 32-36
35. Matsuzaki K., Murase O., Fujii N., and Miyajima K. Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 34 (1995) 6521-6526
36. Matsuzaki K., Murase O., Fujii N., and Miyajima K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35 (1996) 11361-11368
37. Ludtke S.J., He K., Heller W.T., Harroun T.A., Yang L., and Huang H.W. Membrane pores induced by magainin. Biochemistry 35 (1996) 13723-13728
38. 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
39. Henzler Wildman K.A., Lee D.K., and Ramamoorthy A. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42 (2003) 6545-6558
40. 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
41. Powers J.P., Tan A., Ramamoorthy A., and Hancock R.E. Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes. Biochemistry 44 (2005) 15504-15513
42. Laederach A., Andreotti A.H., and Fulton D.B. Solution and micelle-bound structures of tachyplesin I and its active aromatic linear derivatives. Biochemistry 41 (2002) 12359-12368
43. Hinds K.D., Campbell K.M., Holland K.M., Lewis D.H., Piche C.A., and Schmidt P.G. PEGylated insulin in PLGA microparticles. In vivo and in vitro analysis. J. Control. Release 104 (2005) 447-460
44. Ogris M., Brunner S., Schuller S., Kircheis R., and Wagner E. PEGylated DNA/transferrin-PEI complexes: reduced interaction with blood components, extended circulation in blood and potential for systemic gene delivery. Gene Ther. 6 (1999) 595-605
45. Dhalluin C., Ross A., Huber W., Gerber P., Brugger D., Gsell B., and Senn H. Structural, kinetic, and thermodynamic analysis of the binding of the 40 kDa PEG-interferon-alpha2a and its individual positional isomers to the extracellular domain of the receptor IFNAR2. Bioconjug. Chem. 16 (2005) 518-527
46. Kubetzko S., Sarkar C.A., and Pluckthun A. Protein PEGylation decreases observed target association rates via a dual blocking mechanism. Mol. Pharmacol. 68 (2005) 1439-1454
47. Yang K., Basu A., Wang M., Chintala R., Hsieh M.C., Liu S., Hua J., Zhang Z., Zhou J., Li M., Phyu H., Petti G., Mendez M., Janjua H., Peng P., Longley C., Borowski V., Mehlig M., and Filpula D. Tailoring structure-function and pharmacokinetic properties of single-chain Fv proteins by site-specific PEGylation. Protein Eng. 16 (2003) 761-770
48. Matsuzaki K., Sugishita K., Fujii N., and Miyajima K. Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2. Biochemistry 34 (1995) 3423-3429
49. Ziegler A., Nervi P., Durrenberger M., and Seelig J. The cationic cell-penetrating peptide CPP(TAT) derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: optical, biophysical, and metabolic evidence. Biochemistry 44 (2005) 138-148
50. Fuchs S.M., and Raines R.T. Pathway for polyarginine entry into mammalian cells. Biochemistry 43 (2004) 2438-2444
51. Tyagi M., Rusnati M., Presta M., and Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276 (2001) 3254-3261
52. Matsuzaki K., Fukui M., Fujii N., and Miyajima K. Interactions of an antimicrobial peptide, tachyplesin I, with lipid membranes. Biochim. Biophys. Acta 1070 (1991) 259-264
53. Scherrer R., and Gerhardt P. Molecular sieving by the Bacillus megaterium cell wall and protoplast. J. Bacteriol. 107 (1971) 718-735
54. Tateno M., Yamasaki K., Amano N., Kakinuma J., Koike H., Allen M.D., and Suzuki M. DNA recognition by beta-sheets. Biopolymers 44 (1997) 335-359
55. Caliceti P., and Veronese F.M. Pharmacokinetic and biodistribution properties of poly(ethylene glycol)-protein conjugates. Adv. Drug Deliv. Rev. 55 (2003) 1261-1277