Tryptophan- and arginine-rich antimicrobial peptides: Structures and mechanisms of action

Biochimica et Biophysica Acta - Biomembranes

Volumn 1758, Issue 9, 2006, Pages 1184-1202

  Chan, David I ^a   Prenner, Elmar J ^a   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Antimicrobial peptide; Arginine; Cation interaction; Structure; Tryptophan

Indexed keywords

ARGININE; INDOLICIDIN; LACTOFERRICIN; LYSOZYME; PEPTIDE DERIVATIVE; POLYPEPTIDE ANTIBIOTIC AGENT; PUROINDOLINE; TRITRPTICIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIMICROBIAL ACTIVITY; BETA SHEET; COMBINATORIAL CHEMISTRY; DIPOLE; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG STRUCTURE; ELECTROPORATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE ASPOROGENOUS ROD-SHAPED BACTERIA; HYDROGEN BOND; HYDROPHOBICITY; MEMBRANE STRUCTURE; MICELLE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; ARGININE; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; SPECIES SPECIFICITY; TRYPTOPHAN;

BACTERIA (MICROORGANISMS);

EID: 33748988741     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2006.04.006     Document Type: Review

References (134)

1. Zasloff M. 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 (1987) 5449-5453
2. Steiner H., Hultmark D., Engström A., Bennich H., and Boman H.G. Sequence and specificity of two anti-bacterial proteins involved in insect immunity. Nature 292 (1981) 246-248
3. Andersen J.H., Jenssen H., Sandvik K., and Gutteberg T.J. Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J. Med. Virol. 74 (2004) 262-271
4. De Lucca A.J., and Walsh T.J. Antifungal peptides: novel therapeutic compounds against emerging pathogens. Antimicrob. Agents Chemother. 43 (1999) 1-11
5. Theis T., and Stahl U. Antifungal proteins: targets, mechanisms and prospective applications. Cell. Mol. Life Sci. 61 (2004) 437-455
6. Papo N., and Shai Y. Host defense peptides as new weapons in cancer treatment. Cell. Mol. Life Sci. 62 (2005) 784-790
7. Jerala R., and Porro M. Endotoxin neutralizing peptides. Curr. Top. Med. Chem. 4 (2004) 1173-1184
8. McPhee J.B., Scott M.G., and Hancock R.E.W. Design of host defence peptides for antimicrobial and immunity enhancing activities. Comb. Chem. High Throughput Screen. 8 (2005) 257-272
9. Gifford J.L., Hunter H.N., and Vogel H.J. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell. Mol. Life Sci. 62 (2005) 2588-2598
10. Yang D., Chertov O., Bykovskaia N., Chen Q., Buffo M.J., Shogan J., Anderson M., Schröder J.M., Wang J.M., Howard O.M.Z., and Oppenheim J.J. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286 (1999) 525-528
11. Hoover D.M., Boulegue C., Yang D., Oppenheim J.J., Tucker K., Lu W.Y., and Lubkowski J. The structure of human macrophage inflammatory protein-3 alpha/CCL20-Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J. Biol. Chem. 277 (2002) 37647-37654
12. Finken M., Kirschner P., Meier A., Wrede A., and Böttger E.C. Molecular-basis of streptomycin resistance in mycobacterium-tuberculosis-Alterations of the ribosomal-protein S12 gene and point mutations within a functional 16S ribosomal-RNA pseudoknot. Mol. Microbiol. 9 (1993) 1239-1246
13. Spellberg B., Powers J.H., Brass E.P., Miller L.G., and Edwards J.E. Trends in antimicrobial drug development: implications for the future. Clin. Infect. Dis. 38 (2004) 1279-1286
14. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev., Microbiol. 3 (2005) 238-250
15. Giacometti A., Cirioni O., Kamysz W., Silvestri C., Del Prete M.S., Licci A., D'Amato G., Lukasiak J., and Scalise G. In vitro activity of citropin 1.1 alone and in combination with clinically used antimicrobial agents against Rhodococcus equi. J. Antimicrob. Chemother. 56 (2005) 410-412
16. Giacometti A., Cirioni O., Kamysz W., D'Amato G., Silvestri C., Licci A., Nadolski P., Riva A., Lukasiak J., and Scalise G. In vitro activity of MSI-78 alone and in combination with antibiotics against bacteria responsible for bloodstream infections in neutropenic patients. Int. J. Antimicrob. Agents 26 (2005) 235-240
17. Pellegrini A. Antimicrobial peptides from food proteins. Curr. Pharm. Des. 9 (2003) 1225-1238
18. Bradshaw J. Cationic antimicrobial peptides: issues for potential clinical use. BioDrugs 17 (2003) 233-240
19. Ginsburg I. Bactericidal cationic peptides can also function as bacteriolysis-inducing agents mimicking beta-lactam antibiotics? It is enigmatic why this concept is consistently disregarded. Med. Hypotheses 62 (2004) 367-374
20. Miteva M., Andersson M., Karshikoff A., and Otting G. Molecular electroporation: a unifying concept for the description of membrane pore formation by antibacterial peptides, exemplified with NK-lysin. FEBS Lett. 462 (1999) 155-158
21. Pokorny A., and Almeida P.F.F. Kinetics of dye efflux and lipid flip-flop induced by delta-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic, alpha-helical peptides. Biochemistry 43 (2004) 8846-8857
22. Pokorny A., and Almeida P.F.F. Permeabilization of raft-containing lipid vesicles by delta-lysin: a mechanism for cell sensitivity to cytotoxic peptides. Biochemistry 44 (2005) 9538-9544
23. Hwang P.M., and Vogel H.J. Structure-function relationships of antimicrobial peptides. Biochem. Cell Biol. 76 (1998) 235-246
24. Vogel H.J., Schibli D.J., Jing W., Lohmeier-Vogel E.M., Epand R.F., and Epand R.M. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell Biol. 80 (2002) 49-63
25. Strøm M.B., Haug B.E., Rekdal Ø., Skar M.L., Stensen W., and Svendsen J.S. Important structural features of 15-residue lactoferricin derivatives and methods for improvement of antimicrobial activity. Biochem. Cell Biol. 80 (2002) 65-74
26. Yau W.M., Wimley W.C., Gawrisch K., and White S.H. The preference of tryptophan for membrane interfaces. Biochemistry 37 (1998) 14713-14718
27. Persson S., Killian J.A., and Lindblom G. Molecular ordering of interfacially localized tryptophan analogs in ester- and ether-lipid bilayers studied by H-2-NMR. Biophys. J. 75 (1998) 1365-1371
28. Killian J.A., Salemink I., de Planque M.R.R., Lindblom G., Koeppe R.E., and Greathouse D.V. Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane alpha-helical peptides: Importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry 35 (1996) 1037-1045
29. Klein-Seetharaman J., Oikawa M., Grimshaw S.B., Wirmer J., Duchardt E., Ueda T., Imoto T., Smith L.J., Dobson C.M., and Schwalbe H. Long-range interactions within a nonnative protein. Science 295 (2002) 1719-1722
30. Blondelle S.E., and Houghten R.A. Use of nonsupport-bound synthetic combinatorial libraries in cell-based bioassay systems. Methods Mol. Cell. Biol. 6 (1996) 8-16
31. Mazze F.M., Fuzo C.A., and Degreve L. A new amphipathy scale I. Determination of the scale from molecular dynamics data. Biochim. Biophys. Acta 1747 (2005) 35-46
32. Dougherty D.A. Cation-pi interactions in chemistry and biology: a new view of benzene Phe, Tyr, and Trp. Science 271 (1996) 163-168
33. Ma J.C., and Dougherty D.A. The cation-pi interaction. Chem. Rev. 97 (1997) 1303-1324
34. Flanagan J.F., Mi L.Z., Chruszcz M., Cymborowski M., Clines K.L., Kim Y.C., Minor W., Rastinejad F., and Khorasanizadeh S. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438 (2005) 1181-1185
35. Brehm A., Tufteland K.R., Aasland R., and Becker P.B. The many colours of chromodomains. BioEssays 26 (2004) 133-140
36. Minoux H., and Chipot C. Cation-pi interactions in proteins: can simple models provide an accurate description?. J. Am. Chem. Soc. 121 (1999) 10366-10372
37. Aliste M.P., MacCallum J.L., and Tieleman D.P. Molecular dynamics simulations of pentapeptides at interfaces: salt bridge and cation-pi interactions. Biochemistry 42 (2003) 8976-8987
38. Mitchell J.B.O., Nandi C.L., Mcdonald I.K., Thornton J.M., and Price S.L. Amino/aromatic interactions in proteins-Is the evidence stacked against hydrogen-bonding. J. Mol. Biol. 239 (1994) 315-331
39. Jing W., Demcoe A.R., and Vogel H.J. Conformation of a bactericidal domain of puroindoline a: structure and mechanism of action of a 13-residue antimicrobial peptide. J. Bacteriol. 185 (2003) 4938-4947
40. Shepherd C.M., Vogel H.J., and Tieleman D.P. Interactions of the designed antimicrobial peptide MB21 and truncated dermaseptin S3 with lipid bilayers: molecular-dynamics simulations. Biochem. J. 370 (2003) 233-243
41. Petersen F.N., Jensen M.Ø., and Nielsen C.H. Interfacial tryptophan residues: a role for the cation-pi effect?. Biophys. J. 89 (2005) 3985-3996
42. Selsted M.E., Novotny M.J., Morris W.L., Tang Y.Q., Smith W., and Cullor J.S. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267 (1992) 4292-4295
43. Hsu C.H., Chen C., Jou M.L., Lee A.Y., Lin Y.C., Yu Y.P., Huang W.T., and Wu S.H. Structural and DNA-binding studies on the bovine antimicrobial peptide, indolicidin: evidence for multiple conformations involved in binding to membranes and DNA. Nucleic Acids Res. 33 (2005) 4053-4064
44. Rozek A., Friedrich C.L., and Hancock R.E. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 39 (2000) 15765-15774
45. Wu M.H., Maier E., Benz R., and Hancock R.E.W. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38 (1999) 7235-7242
46. Subbalakshmi C., and Sitaram N. Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett. 160 (1998) 91-96
47. Ryge T.S., Doisy X., Ifrah D., Olsen J.E., and Hansen P.R. New indolicidin analogues with potent antibacterial activity. J. Pept. Res. 64 (2004) 171-185
48. Krajewski K., Marchand C., Long Y.Q., Pommier Y., and Roller P.P. Synthesis and HIV-1 integrase inhibitory activity of dimeric and tetrameric analogs of indolicidin. Bioorg. Med. Chem. Lett. 14 (2004) 5595-5598
49. Friedrich C.L., Rozek A., Patrzykat A., and Hancock R.E. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria. J. Biol. Chem. 276 (2001) 24015-24022
50. Falla T.J., and Hancock R.E.W. Improved activity of a synthetic indolicidin analog. Antimicrob. Agents Chemother. 41 (1997) 771-775
51. Halevy R., Rozek A., Kolusheva S., Hancock R.E., and Jelinek R. Membrane binding and permeation by indolicidin analogs studied by a biomimetic lipid/polydiacetylene vesicle assay. Peptides 24 (2003) 1753-1761
52. Rozek A., Powers J.P., Friedrich C.L., and Hancock R.E. Structure-based design of an indolicidin peptide analogue with increased protease stability. Biochemistry 42 (2003) 14130-14138
53. Lawyer C., Pai S., Watabe M., Borgia P., Mashimo T., Eagleton L., and Watabe K. Antimicrobial activity of a 13 amino acid tryptophan-rich peptide derived from a putative porcine precursor protein of a novel family of antibacterial peptides. FEBS Lett. 390 (1996) 95-98
54. Schibli D.J., Hwang P.M., and Vogel H.J. Structure of the antimicrobial peptide tritrpticin bound to micelles: a distinct membrane-bound peptide fold. Biochemistry 38 (1999) 16749-16755
55. Schibli D.J., Epand R.F., Vogel H.J., and Epand R.M. Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions. Biochem. Cell Biol. 80 (2002) 667-677
56. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
57. 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
58. Matsuzaki K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462 (1999) 1-10
59. 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
60. Yang L., Weiss T.M., Lehrer R.I., and Huang H.W. Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys. J. 79 (2000) 2002-2009
61. Salay L.C., Procopio J., Oliveira E., Nakaie C.R., and Schreier S. Ion channel-like activity of the antimicrobial peptide tritrpticin in planar lipid bilayers. FEBS Lett. 565 (2004) 171-175
62. Blochet J.E., Chevalier C., Forest E., Pebay-Peyroula E., Gautier M.F., Joudrier P., Pézolet M., and Marion D. Complete amino acid sequence of puroindoline, a new basic and cystine-rich protein with a unique tryptophan-rich domain, isolated from wheat endosperm by Triton X-114 phase partitioning. FEBS Lett. 329 (1993) 336-340
63. Morris C.F. Puroindolines: the molecular genetic basis of wheat grain hardness. Plant Mol. Biol. 48 (2002) 633-647
64. Krishnamurthy K., Balconi C., Sherwood J.E., and Giroux M.J. Wheat puroindolines enhance fungal disease resistance in transgenic rice. Mol. Plant-Microb. Interact. 14 (2001) 1255-1260
65. Capparelli R., Amoroso M.G., Palumbo D., Iannaccone M., Faleri C., and Cresti M. Two plant puroindolines colocalize in wheat seed and in vitro synergistically fight against pathogens. Plant Mol. Biol. 58 (2005) 857-867
66. Mattei C., Elmorjani K., Molgó J., Marion D., and Benoit E. The wheat proteins puroindoline-a and alpha 1-purothionin induce nodal swelling in myelinated axons. NeuroReport 9 (1998) 3803-3807
67. Le Guernevé C., Seigneuret M., and Marion D. Interaction of the wheat endosperm lipid-binding protein puroindoline-a with phospholipids. Arch. Biochem. Biophys. 360 (1998) 179-186
68. Dubreil L., Vié V., Beaufils S., Marion D., and Renault A. Aggregation of puroindoline in phospholipid monolayers spread at the air-liquid interface. Biophys. J. 85 (2003) 2650-2660
69. Hughes P., Dennis E., Whitecross M., Llewellyn D., and Gage P. The cytotoxic plant protein, beta-purothionin, forms ion channels in lipid membranes. J. Biol. Chem. 275 (2000) 823-827
70. Charnet P., Molle G., Marion D., Rousset M., and Lullien-Pellerin V. Puroindolines form ion channels in biological membranes. Biophys. J. 84 (2003) 2416-2426
71. Blondelle S.E., Takahashi E., Dinh K.T., and Houghten R.A. The antimicrobial activity of hexapeptides derived from synthetic combinatorial libraries. J. Appl. Bacteriol. 78 (1995) 39-46
72. Blondelle S.E., Takahashi E., Houghten R.A., and Pérez-Payá E. Rapid identification of compounds with enhanced antimicrobial activity by using conformationally defined combinatorial libraries. Biochem. J. 313 Pt 1 (1996) 141-147
73. Blondelle S.E., and Houghten R.A. Novel antimicrobial compounds identified using synthetic combinatorial library technology. Trends Biotechnol. 14 (1996) 60-65
74. Jing W., Hunter H.N., Hagel J., and Vogel H.J. The structure of the antimicrobial peptide Ac-RRWWRF-NH2 bound to micelles and its interactions with phospholipid bilayers. J. Pept. Res. 61 (2003) 219-229
75. Rezansoff A.J., Hunter H.N., Jing W., Park I.Y., Kim S.C., and Vogel H.J. Interactions of the antimicrobial peptide Ac-FRWWHR-NH(2) with model membrane systems and bacterial cells. J. Pept. Res. 65 (2005) 491-501
76. Park C.B., Yi K.S., Matsuzaki K., Kim M.S., and Kim S.C. Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8245-8250
77. Derossi D., Chassaing G., and Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8 (1998) 84-87
78. Wessolowski A., Bienert M., and Dathe M. Antimicrobial activity of arginine- and tryptophan-rich hexapeptides: the effects of aromatic clusters, D-amino acid substitution and cyclization. J. Pept. Res. 64 (2004) 159-169
79. Dathe M., Nikolenko H., Klose J., and Bienert M. Cyclization increases the antimicrobial activity and selectivity of arginine- and tryptophan-containing hexapeptides. Biochemistry 43 (2004) 9140-9150
80. Appelt C., Wessolowski A., Söderhäll J.A., Dathe M., and Schmieder P. Structure of the antimicrobial, cationic hexapeptide cyclo(RRWWRF) and its analogues in solution and bound to detergent micelles. ChemBioChem 6 (2005) 1654-1662
81. Appelt C., Eisenmenger F., Kühne R., Schmieder P., and Söderhäll J.A. Interaction of the antimicrobial peptide cyclo(RRWWRF) with membranes by molecular dynamics simulations. Biophys. J. 89 (2005) 2296-2306
82. Levay P.F., and Viljoen M. Lactoferrin: a general review. Haematologica 80 (1995) 252-267
83. Singh P.K., Parsek M.R., Greenberg E.P., and Welsh M.J. A component of innate immunity prevents bacterial biofilm development. Nature 417 (2002) 552-555
84. Tomita M., Bellamy W., Takase M., Yamauchi K., Wakabayashi H., and Kawase K. Potent antibacterial peptides generated by pepsin digestion of bovine lactoferrin. J. Dairy Sci. 74 (1991) 4137-4142
85. van der Kraan M.I., Groenink J., Nazmi K., Veerman E.C., Bolscher J.G., and Amerongen A.V.N. Lactoferrampin: a novel antimicrobial peptide in the N1-domain of bovine lactoferrin. Peptides 25 (2004) 177-183
86. Pellegrini A., Thomas U., Bramaz N., Klauser S., and von Fellenberg R. Identification and isolation of a bactericidal domain in chicken egg white lysozyme. J. Appl. Microbiol. 82 (1997) 372-378
87. Bellamy W., Takase M., Yamauchi K., Wakabayashi H., Kawase K., and Tomita M. Identification of the bactericidal domain of lactoferrin. Biochim. Biophys. Acta 1121 (1992) 130-136
88. Yamauchi K., Tomita M., Giehl T.J., and Ellison R.T. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun. 61 (1993) 719-728
89. Bellamy W., Takase M., Wakabayashi H., Kawase K., and Tomita M. Antibacterial spectrum of lactoferricin-B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin. J. Appl. Bacteriol. 73 (1992) 472-479
90. Bellamy W., Yamauchi K., Wakabayashi H., Takase M., Takakura N., Shimamura S., and Tomita M. Antifungal properties of lactoferricin-B, a peptide derived from the N-terminal region of bovine lactoferrin. Lett. Appl. Microbiol. 18 (1994) 230-233
91. Rekdal Ø., Andersen J., Vorland L.H., and Svendsen J.S. Construction and synthesis of lactoferricin derivatives with enhanced antibacterial activity. J. Pept. Sci. 5 (1999) 32-45
92. Kang J.H., Lee M.K., Kim K.L., and Hahm K.S. Structure-biological activity relationships of 11-residue highly basic peptide segment of bovine lactoferrin. Int. J. Pept. Protein Res. 48 (1996) 357-363
93. Tomita M., Takase M., Bellamy W., and Shimamura S. A review: the active peptide of lactoferrin. Acta Paediatr. Jpn. 36 (1994) 585-591
94. Hwang P.M., Zhou N., Shan X., Arrowsmith C.H., and Vogel H.J. Three-dimensional solution structure of lactoferricin B, an antimicrobial peptide derived from bovine lactoferrin. Biochemistry 37 (1998) 4288-4298
95. Moore S.A., Anderson B.F., Groom C.R., Haridas M., and Baker E.N. Three-dimensional structure of diferric bovine lactoferrin at 2.8 angstrom resolution. J. Mol. Biol. 274 (1997) 222-236
96. Zhou N., Tieleman D.P., and Vogel H.J. Molecular dynamics simulations of bovine lactoferricin: turning a helix into a sheet. Biometals 17 (2004) 217-223
97. Schibli D.J., Hwang P.M., and Vogel H.J. The structure of the antimicrobial active center of lactoferricin B bound to sodium dodecyl sulfate micelles. FEBS Lett. 446 (1999) 213-217
98. Nguyen L.T., Schibli D.J., and Vogel H.J. Structural studies and model membrane interactions of two peptides derived from bovine lactoferricin. J. Pept. Sci. 11 (2005) 379-389
99. Strøm M.B., Rekdal Ø., and Svendsen J.S. Antibacterial activity of 15-residue lactoferricin derivatives. J. Pept. Res. 56 (2000) 265-274
100. Haug B.E., Skar M.L., and Svendsen J.S. Bulky aromatic amino acids increase the antibacterial activity of 15-residue bovine lactoferricin derivatives. J. Pept. Sci. 7 (2001) 425-432
101. Haug B.E., and Svendsen J.S. The role of tryptophan in the antibacterial activity of a 15-residue bovine lactoferricin peptide. J. Pept. Sci. 7 (2001) 190-196
102. Hunter H.N., Demcoe A.R., Jenssen H., Gutteberg T.J., and Vogel H.J. Human lactoferricin is partially folded in aqueous solution and is better stabilized in a membrane mimetic solvent. Antimicrob. Agents Chemother 49 (2005) 3387-3395
103. Schwaiger M., Lebendiker M., Yerushalmi H., Coles M., Gröger A., Schwarz C., Schuldiner S., and Kessler H. NMR investigation of the multidrug transporter EmrE, an integral membrane protein. Eur. J. Biochem. 254 (1998) 610-619
104. Girvin M.E., Rastogi V.K., Abildgaard F., Markley J.L., and Fillingame R.H. Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry 37 (1998) 8817-8824
105. Sun X.L., Baker H.M., Shewry S.C., Jameson G.B., and Baker E.N. Structure of recombinant human lactoferrin expressed in Aspergillus awamori. Acta Crystallogr., D Biol. Crystallogr. 55 (1999) 403-407
106. Chapple D.S., Hussain R., Joannou C.L., Hancock R.E.W., Odell E., Evans R.W., and Siligardi G. Structure and association of human lactoferrin peptides with Escherichia coli lipopolysaccharide. Antimicrob. Agents Chemother. 48 (2004) 2190-2198
107. Shin K., Yamauchi K., Teraguchi S., Hayasawa H., Tomita M., Otsuka Y., and Yamazaki S. Antibacterial activity of bovine lactoferrin and its peptides against enterohaemorrhagic Escherichia coli O157 : H7. Lett. Appl. Microbiol. 26 (1998) 407-411
108. Haukland H.H., Ulvatne H., Sandvik K., and Vorland L.H. The antimicrobial peptides lactoferricin B and magainin 2 cross over the bacterial cytoplasmic membrane and reside in the cytoplasm. FEBS Lett. 508 (2001) 389-393
109. He J.L., and Furmanski P. Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature 373 (1995) 721-724
110. Joliot A., and Prochiantz A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 6 (2004) 189-196
111. Lensink M.F., Christiaens B., Vandekerckhove J., Prochiantz A., and Rosseneu M. Penetratin-membrane association: W48/R52/W56 shield the peptide from the aqueous phase. Biophys.J. 88 (2005) 939-952
112. Ulvatne H., Samuelsen O., Haukland H.H., Kramer M., and Vorland L.H. Lactoferricin B inhibits bacterial macromolecular synthesis in Escherichia coli and Bacillus subtilis. FEMS Microbiol. Lett. 237 (2004) 377-384
113. Jolles P., and Jolles J. What's new in lysozyme research-Always a model system, today as yesterday. Mol. Cell. Biochem. 63 (1984) 165-189
114. Pellegrini A., Thomas U., Von Fellenberg R., and Wild P. Bactericidal activities of lysozyme and aprotinin against Gram-negative and Gram-positive bacteria related to their basic character. J. Appl. Bacteriol. 72 (1992) 180-187
115. Ibrahim H.R., Inazaki D., Abdou A., Aoki T., and Kim M. Processing of lysozyme at distinct loops by pepsin: a novel action for generating multiple antimicrobial peptide motifs in the newborn stomach. Biochim. Biophys. Acta 1726 (2005) 102-114
116. Mine Y., Ma F., and Lauriau S. Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme. J. Agric. Food Chem. 52 (2004) 1088-1094
117. Düring K., Porsch P., Mahn A., Brinkmann O., and Gieffers W. The non-enzymatic microbicidal activity of lysozymes. FEBS Lett. 449 (1999) 93-100
118. Ibrahim H.R., Thomas U., and Pellegrini A. A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action. J. Biol. Chem. 276 (2001) 43767-43774
119. Hunter H.N., Jing W., Schibli D.J., Trinh T., Park I.Y., Kim S.C., and Vogel H.J. The interactions of antimicrobial peptides derived from lysozyme with model membrane systems. Biochim. Biophys. Acta 1668 (2005) 175-189
120. Park C.B., Kim H.S., and Kim S.C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244 (1998) 253-257
121. Pellegrini A., Thomas U., Wild P., Schraner E., and von Fellenberg R. Effect of lysozyme or modified lysozyme fragments on DNA and RNA synthesis and membrane permeability of Escherichia coli. Microbiol. Res. 155 (2000) 69-77
122. Wei S.Y., Wu J.M., Kuo Y.Y., Chen H.L., Yip B.S., Tzeng S.R., and Cheng J.W. Solution structure of a novel tryptophan-rich peptide with bidirectional antimicrobial activity. J. Bacteriol. 188 (2006) 328-334
123. Deslouches B., Islam K., Craigo J.K., Paranjape S.M., Montelaro R.C., and Mietzner T.A. Activity of the de novo engineered antimicrobial peptide WLBU2 against Pseudomonas aeruginosa in human serum and whole blood: implications for systemic applications. Antimicrob. Agents Chemother. 49 (2005) 3208-3216
124. Deslouches B., Phadke S.M., Lazarevic V., Cascio M., Islam K., Montelaro R.C., and Mietzner T.A. De novo generation of cationic antimicrobial peptides: influence of length and tryptophan substitution on antimicrobial activity. Antimicrob. Agents Chemother. 49 (2005) 316-322
125. Yoo Y.C., Watanabe R., Koike Y., Mitobe M., Shimazaki K., Watanabe S., and Azuma I. Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-derived peptide: involvement of reactive oxygen species. Biochem. Biophys. Res. Commun. 237 (1997) 624-628
126. Yoo Y.C., Watanabe S., Watanabe R., Hata K., Shimazaki K., and Azuma I. Bovine lactoferrin and lactoferricin, a peptide derived from bovine lactoferrin, inhibit tumor metastasis in mice. Jpn. J. Cancer Res. 88 (1997) 184-190
127. Eliassen L.T., Berge G., Sveinbjørnsson B., Svendsen J.S., Vorland L.H., and Rekdal Ø. Evidence for a direct antitumor mechanism of action of bovine lactoferricin. Anticancer Res. 22 (2002) 2703-2710
128. Yang S.T., Shin S.Y., Kim Y.C., Kim Y., Hahm K.S., and Kim J.I. Conformation-dependent antibiotic activity of tritrpticin, a cathelicidin-derived antimicrobial peptide. Biochem. Biophys. Res. Commun. 296 (2002) 1044-1050
129. Falla T.J., Karunaratne D.N., and Hancock R.E. Mode of action of the antimicrobial peptide indolicidin. J. Biol. Chem. 271 (1996) 19298-19303
130. Vorland L.H., Ulvatne H., Andersen J., Haukland H., Rekdal Ø., Svendsen J.S., and Gutteberg T.J. Lactoferricin of bovine origin is more active than lactoferricins of human, murine and caprine origin. Scand. J. Infect. Dis. 30 (1998) 513-517
131. Wakabayashi H., Takase M., and Tomita M. Lactoferricin derived from milk protein lactoferrin. Curr. Pharm. Des 9 (2003) 1277-1287
132. Chapple D.S., Mason D.J., Joannou C.L., Odell E.W., Gant V., and Evans R.W. Structure-function relationship of antibacterial synthetic peptides homologous to a helical surface region on human lactoferrin against Escherichia coli serotype O111. Infect. Immun. 66 (1998) 2434-2440
133. Lupetti A., Paulusma-Annema A., Welling M.M., Senesi S., van Dissel J.T., and Nibbering P.H. Candidacidal activities of human lactoferrin peptides derived from the N terminus. Antimicrob. Agents Chemother. 44 (2000) 3257-3263
134. Tieleman D.P. The molecular basis of electroporation. BMC Biochem. 5 (2004) 10