Antimicrobial peptide mimics for improved therapeutic properties

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 8, 2009, Pages 1582-1592

  Rotem, Shahar ^a   Mor, Amram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Antibiotic; Antimicrobial peptide; Drug design; Drug resistance; Oligo acyl lysine; Peptidomimetic

Indexed keywords

AROMATIC AMIDE; DERMASEPTIN; PEPTIDOMIMETIC AGENT; PEPTOID; POLYPEPTIDE ANTIBIOTIC AGENT; SYNTHETIC PEPTIDE;

AMPHIBIA; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ANTIPROTOZOAL ACTIVITY; BACTERIAL CELL; BIOPHYSICS; CELL KILLING; CIRCULAR DICHROISM; DRUG BIOAVAILABILITY; DRUG DESIGN; DRUG STRUCTURE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEMOLYSIS; IMMUNE RESPONSE; IMMUNOGENICITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; STRUCTURE ACTIVITY RELATION; THREE DIMENSIONAL IMAGING;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; DRUG DESIGN; DRUG RESISTANCE, MICROBIAL; HEMOLYSIS; HUMANS; PEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

AMPHIBIA;

EID: 67649295450     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.10.020     Document Type: Review

References (141)

1. Jenssen H., Hamill P., and Hancock R.E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19 (2006) 491-511
2. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
3. Bush K. Antibacterial drug discovery in the 21st century. Clin. Microbiol. Infect. 10 Suppl. 4 (2004) 10-17
4. Poole K., Russell A.D., and Lambert P.A. Mechanisms of antimicrobial resistance: opportunities for new targeted therapies. Adv. Drug Deliv. Rev. 57 (2005) 1443-1445
5. D'Agata E.M. Rapidly rising prevalence of nosocomial multidrug-resistant, Gram-negative bacilli: a 9-year surveillance study. Infect. Control Hosp. Epidemiol. 25 (2004) 842-846
6. Deshpande L.M., Fritsche T.R., and Jones R.N. Molecular epidemiology of selected multidrug-resistant bacteria: a global report from the SENTRY Antimicrobial Surveillance Program. Diagn. Microbiol. Infect. Dis. 49 (2004) 231-236
7. Wright G.D. Bacterial resistance to antibiotics: enzymatic degradation and modification. Adv. Drug Deliv. Rev. 57 (2005) 1451-1470
8. Lambert P.A. Bacterial resistance to antibiotics: modified target sites. Adv. Drug Deliv. Rev. 57 (2005) 1471-1485
9. Li X.Z., and Nikaido H. Efflux-mediated drug resistance in bacteria. Drugs 64 (2004) 159-204
10. Stewart P.S., and Costerton J.W. Antibiotic resistance of bacteria in biofilms. Lancet 358 (2001) 135-138
11. Hancock R.E. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1 (2001) 156-164
12. Epand R.M., and Vogel H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462 (1999) 11-28
13. Baba T., and Schneewind O. Instruments of microbial warfare: bacteriocin synthesis, toxicity and immunity. Trends Microbiol. 6 (1998) 66-71
14. van Belkum M.J., Kok J., Venema G., Holo H., Nes I.F., Konings W.N., and Abee T. The bacteriocin lactococcin A specifically increases permeability of lactococcal cytoplasmic membranes in a voltage-independent, protein-mediated manner. J. Bacteriol. 173 (1991) 7934-7941
15. Garcia-Olmedo F., Molina A., Alamillo J.M., and Rodriguez-Palenzuela P. Plant defense peptides. Biopolymers 47 (1998) 479-491
16. Fernandez de C.R., Gonzalez-Pascual B., Garcia-Olmedo F., and Carbonero P. Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro. Appl. Microbiol. 23 (1972) 998-1000
17. Bulet P., and Stocklin R. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12 (2005) 3-11
18. Habermann E. Bee and wasp venoms. Science 177 (1972) 314-322
19. Hultmark D., Steiner H., Rasmuson T., and Boman H.G. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 106 (1980) 7-16
20. Naitza S., and Ligoxygakis P. Antimicrobial defences in Drosophila: the story so far. Mol. Immunol. 40 (2004) 887-896
21. Nascimento A.C., Fontes W., Sebben A., and Castro M.S. Antimicrobial peptides from anurans skin secretions. Protein Pept. Lett. 10 (2003) 227-238
22. Charpentier S., Amiche M., Mester J., Vouille V., Le Caer J.P., Nicolas P., and Delfour A. Structure, synthesis, and molecular cloning of dermaseptins B, a family of skin peptide antibiotics. J. Biol. Chem. 273 (1998) 14690-14697
23. Csordas A., and Michl H. Primary structure of two oligopeptides of the toxin of Bombina variegata L. Toxicon 7 (1969) 103-108
24. Mor A., Nguyen V.H., Delfour A., Migliore-Samour D., and Nicolas P. Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry 30 (1991) 8824-8830
25. 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
26. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3 (2003) 710-720
27. Ganz T., Selsted M.E., Szklarek D., Harwig S.S., Daher K., Bainton D.F., and Lehrer R.I. Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Invest. 76 (1985) 1427-1435
28. Travis S.M., Anderson N.N., Forsyth W.R., Espiritu C., Conway B.D., Greenberg E.P., McCray Jr. P.B., Lehrer R.I., Welsh M.J., and Tack B.F. Bactericidal activity of mammalian cathelicidin-derived peptides. Infect. Immun. 68 (2000) 2748-2755
29. Ganz T. Defensins and host defense. Science 286 (1999) 420-421
30. Yang D., Chertov O., Bykovskaia S.N., Chen Q., Buffo M.J., Shogan J., Anderson M., Schroder J.M., Wang J.M., Howard O.M., and Oppenheim J.J. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286 (1999) 525-528
31. Selsted M.E., and Ouellette A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6 (2005) 551-557
32. Merrifield R.B., Juvvadi P., Andreu D., Ubach J., Boman A., and Boman H.G. Retro and retroenantio analogs of cecropin-melittin hybrids. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 3449-3453
33. Hancock R.E., and Chapple D.S. Peptide antibiotics. Antimicrob. Agents Chemother. 43 (1999) 1317-1323
34. Shai Y., and Oren Z. From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides 22 (2001) 1629-1641
35. Hancock R.E. The bacterial outer membrane as a drug barrier. Trends Microbiol. 5 (1997) 37-42
36. Tossi A., Sandri L., and Giangaspero A. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55 (2000) 4-30
37. Christensen B., Fink J., Merrifield R.B., and Mauzerall D. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 5072-5076
38. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1376 (1998) 391-400
39. Yang L., Harroun T.A., Weiss T.M., Ding L., and Huang H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81 (2001) 1475-1485
40. 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
41. Porcelli F., Buck B., Lee D.K., Hallock K.J., Ramamoorthy A., and Veglia G. Structure and orientation of pardaxin determined by NMR experiments in model membranes. J. Biol. Chem. 279 (2004) 45815-45823
42. Porcelli F., Verardi R., Shi L., Henzler-Wildman K.A., Ramamoorthy A., and Veglia G. NMR structure of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles. Biochemistry 47 (2008) 5565-5572
43. Porcelli F., Buck-Koehntop B.A., Thennarasu S., Ramamoorthy A., and Veglia G. Structures of the dimeric and monomeric variants of magainin antimicrobial peptides (MSI-78 and MSI-594) in micelles and bilayers, determined by NMR spectroscopy. Biochemistry 45 (2006) 5793-5799
44. Leontiadou H., Mark A.E., and Marrink S.J. Antimicrobial peptides in action. J. Am. Chem. Soc. 128 (2006) 12156-12161
45. 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
46. Yeaman M.R., and Yount N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55 (2003) 27-55
47. Epand R.F., Ramamoorthy A., and Epand R.M. Membrane lipid composition and the interaction of pardaxin: the role of cholesterol. Protein Pept. Lett. 13 (2006) 1-5
48. Hallock K.J., Lee D.K., Omnaas J., Mosberg H.I., and Ramamoorthy A. Membrane composition determines pardaxin's mechanism of lipid bilayer disruption. Biophys. J. 83 (2002) 1004-1013
49. McPhee J.B., Scott M.G., and Hancock R.E. Design of host defence peptides for antimicrobial and immunity enhancing activities. Comb. Chem. High Throughput Screen. 8 (2005) 257-272
50. Blondelle S.E., and Houghten R.A. Hemolytic and antimicrobial activities of the twenty-four individual omission analogues of melittin. Biochemistry 30 (1991) 4671-4678
51. Radzishevsky I.S., Rotem S., Zaknoon F., Gaidukov L., Dagan A., and Mor A. Effects of acyl versus aminoacyl conjugation on the properties of antimicrobial peptides. Antimicrob. Agents Chemother. 49 (2005) 2412-2420
52. Rotem S., Radzishevsky I., and Mor A. Physicochemical properties that enhance discriminative antibacterial activity of short dermaseptin derivatives. Antimicrob. Agents Chemother. 50 (2006) 2666-2672
53. Stallmann H.P., Faber C., Bronckers A.L., de Blieck-Hogervorst J.M., Brouwer C.P., Amerongen A.V., and Wuisman P.I. Histatin and lactoferrin derived peptides: antimicrobial properties and effects on mammalian cells. Peptides 26 (2005) 2355-2359
54. Laroche G., Dufourc E.J., Pezolet M., and Dufourcq J. Coupled changes between lipid order and polypeptide conformation at the membrane surface. A deuterium-NMR and Raman study of polylysine-phosphatidic acid systems. Biochemistry 29 (1990) 6460-6465
55. Shaw J.E., Epand R.F., Hsu J.C., Mo G.C., Epand R.M., and Yip C.M. Cationic peptide-induced remodelling of model membranes: direct visualization by in situ atomic force microscopy. J. Struct. Biol. 162 (2008) 121-138
56. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3 (2005) 238-250
57. 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
58. Otvos Jr. L., Insug O., Rogers M.E., Consolvo P.J., Condie B.A., Lovas S., Bulet P., and Blaszczyk-Thurin M. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39 (2000) 14150-14159
59. Kragol G., Lovas S., Varadi G., Condie B.A., Hoffmann R., and Otvos Jr. L. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40 (2001) 3016-3026
60. Boman H.G., Agerberth B., and Boman A. Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect. Immun. 61 (1993) 2978-2984
61. 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
62. 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
63. Patrzykat A., Friedrich C.L., Zhang L., Mendoza V., and Hancock R.E. Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob. Agents Chemother. 46 (2002) 605-614
64. Subbalakshmi C., and Sitaram N. Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett. 160 (1998) 91-96
65. Mor A. Peptide-based antibiotics: a potential answer to raging antimicrobial resistance. Drug Dev. Res. 50 (2000) 440-447
66. Perron G.G., Zasloff M., and Bell G. Experimental evolution of resistance to an antimicrobial peptide. Proc. Biol. Sci. 273 (2006) 251-256
67. Bals R., Wang X., Wu Z., Freeman T., Bafna V., Zasloff M., and Wilson J.M. Human beta-defensin 2 is a salt-sensitive peptide antibiotic expressed in human lung. J. Clin. Invest. 102 (1998) 874-880
68. Goldman M.J., Anderson G.M., Stolzenberg E.D., Kari U.P., Zasloff M., and Wilson J.M. Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88 (1997) 553-560
69. Minahk C.J., and Morero R.D. Inhibition of enterocin CRL35 antibiotic activity by mono- and divalent ions. Lett. Appl. Microbiol. 37 (2003) 374-379
70. Rydlo T., Rotem S., and Mor A. Antibacterial properties of dermaseptin S4 derivatives under extreme incubation conditions. Antimicrob. Agents Chemother. 50 (2006) 490-497
71. Lee I.H., Cho Y., and Lehrer R.I. Effects of pH and salinity on the antimicrobial properties of clavanins. Infect. Immun. 65 (1997) 2898-2903
72. 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
73. Gordon Y.J., Romanowski E.G., and McDermott A.M. A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Curr. Eye Res. 30 (2005) 505-515
74. Marr A.K., Gooderham W.J., and Hancock R.E. Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr. Opin. Pharmacol. 6 (2006) 468-472
75. Bradshaw J. Cationic antimicrobial peptides: issues for potential clinical use. Bio. Drugs 17 (2003) 233-240
76. Bessalle R., Kapitkovsky A., Gorea A., Shalit I., and Fridkin M. All-d-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett. 274 (1990) 151-155
77. Wade D., Boman A., Wahlin B., Drain C.M., Andreu D., Boman H.G., and Merrifield R.B. All-d amino acid-containing channel-forming antibiotic peptides. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 4761-4765
78. Blondelle S.E., Perez-Paya E., and Houghten R.A. Synthetic combinatorial libraries: novel discovery strategy for identification of antimicrobial agents. Antimicrob. Agents Chemother. 40 (1996) 1067-1071
79. Blondelle S.E., and Lohner K. Combinatorial libraries: a tool to design antimicrobial and antifungal peptide analogues having lytic specificities for structure-activity relationship studies. Biopolymers 55 (2000) 74-87
80. Eichler J., and Houghten R.A. Generation and utilization of synthetic combinatorial libraries. Mol. Med. Today 1 (1995) 174-180
81. Epand R.F., Lehrer R.I., Waring A., Wang W., Maget-Dana R., Lelievre D., and Epand R.M. Direct comparison of membrane interactions of model peptides composed of only Leu and Lys residues. Biopolymers 71 (2003) 2-16
82. 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
83. Tiozzo E., Rocco G., Tossi A., and Romeo D. Wide-spectrum antibiotic activity of synthetic, amphipathic peptides. Biochem. Biophys. Res. Commun. 249 (1998) 202-206
84. Tossi A., Tarantino C., and Romeo D. Design of synthetic antimicrobial peptides based on sequence analogy and amphipathicity. Eur. J. Biochem. 250 (1997) 549-558
85. Patch J.A., and Barron A.E. Mimicry of bioactive peptides via non-natural, sequence-specific peptidomimetic oligomers. Curr. Opin. Chem. Biol. 6 (2002) 872-877
86. Adessi C., and Soto C. Converting a peptide into a drug: strategies to improve stability and bioavailability. Curr. Med. Chem. 9 (2002) 963-978
87. Latham P.W. Therapeutic peptides revisited. Nat. Biotechnol. 17 (1999) 755-757
88. Som A., Vemparala S., Ivanov I., and Tew G.N. Synthetic mimics of antimicrobial peptides. Biopolymers 90 (2008) 83-93
89. Gabriel G.J., Som A., Madkour A.E., Eren T., and Tew G.N. Infectious disease: connecting innate immunity to biocidal polymers. Mater. Sci. Eng. R. Rep. 57 (2007) 28-64
90. Lai X.Z., Feng Y., Pollard J., Chin J.N., Rybak M.J., Bucki R., Epand R.F., Epand R.M., and Savage P.B. Ceragenins: cholic Acid-Based Mimics of Antimicrobial Peptides, Acc. Acc. Chem. Res. 40 (2008) 1233-1240
91. Shai Y., and Oren Z. Diastereoisomers of cytolysins, a novel class of potent antibacterial peptides. J. Biol. Chem. 271 (1996) 7305-7308
92. Zuckermann R.N., Kerr J.M., Kent S.B.H., and Moos W.H. Efficient method for the preparation of peptoids [oligo(N-substituted glycines)] by submonomer solid-phase synthesis. J. Am. Chem. Soc. 114 (1992) 10646-10647
93. Miller S.M., Simon R.J., Ng S., Zuckermann R.N., Kerr J.M., and Moos W.H. Proteolytic studies of homologous peptide and N-substituted glycine peptoid oligomers. Bioorg. Med. Chem. Lett. 4 (1994) 2657-2662
94. Wu C.W., Sanborn T.J., Huang K., Zuckermann R.N., and Barron A.E. Peptoid oligomers with alpha-chiral, aromatic side chains: sequence requirements for the formation of stable peptoid helices. J. Am. Chem. Soc. 123 (2001) 6778-6784
95. Wu C.W., Kirshenbaum K., Sanborn T.J., Patch J.A., Huang K., Dill K.A., Zuckermann R.N., and Barron A.E. Structural and spectroscopic studies of peptoid oligomers with alpha-chiral aliphatic side chains. J. Am. Chem. Soc. 125 (2003) 13525-13530
96. Armand P., Kirshenbaum K., Goldsmith R.A., Farr-Jones S., Barron A.E., Truong K.T.V., Dill K.A., Mierke D.F., Cohen F.E., Zuckermann R.N., and Bradley E.K. NMR determination of the major solution conformation of a peptoid pentamer with chiral side chains. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 4309-4314
97. Kirshenbaum K., Barron A.E., Goldsmith R.A., Armand P., Bradley E.K., Truong K.T.V., Dill K.A., Cohen F.E., and Zuckermann R.N. Sequence-specific polypeptoids: a diverse family of heteropolymers with stable secondary structure. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 4303-4308
98. Chongsiriwatana N.P., Patch J.A., Czyzewski A.M., Dohm M.T., Ivankin A., Gidalevitz D., Zuckermann R.N., and Barron A.E. Peptoids that mimic the structure, function, and mechanism of helical antimicrobial peptides. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 2794-2799
99. Hamuro Y., Schneider J.P., and DeGrado W.F. De novo design of antibacterial β-peptides. J. Am. Chem. Soc. 121 (1999) 12200-12201
100. Liu D., and DeGrado W.F. De novo design, synthesis, and characterization of antimicrobial beta-peptides. J. Am. Chem. Soc. 123 (2001) 7553-7559
101. Arvidsson P.I., Frackenpohl J., Ryder N.S., Liechty B., Petersen F., Zimmermann H., Camenisch G.P., Woessner R., and Seebach D. On the antimicrobial and hemolytic activities of amphiphilic beta-peptides. Chembiochem. 2 (2001) 771-773
102. Arvidsson P.I., Ryder N.S., Weiss H.M., Gross G., Kretz O., Woessner R., and Seebach D. Antibiotic and hemolytic activity of a beta2/beta3 peptide capable of folding into a 12/10-helical secondary structure. Chembiochem. 4 (2003) 1345-1347
103. Wiegand H., Wirz B., Schweitzer A., Gross G., Perez M.I., Andres H., Kimmerlin T., Rueping M., and Seebach D. Pharmacokinetic investigation of a 14C-labelled beta 3/alpha tetrapeptide in rats. Chem. Biodivers. 1 (2004) 1812-1828
104. Porter E.A., Wang X., Lee H.S., Weisblum B., and Gellman S.H. Non-haemolytic beta-amino-acid oligomers. Nature 404 (2000) 565
105. Raguse T.L., Porter E.A., Weisblum B., and Gellman S.H. Structure-activity studies of 14-helical antimicrobial beta-peptides: probing the relationship between conformational stability and antimicrobial potency. J. Am. Chem. Soc. 124 (2002) 12774-12785
106. Schmitt M.A., Weisblum B., and Gellman S.H. Unexpected relationships between structure and function in alpha,beta-peptides: antimicrobial foldamers with heterogeneous backbones. J. Am. Chem. Soc. 126 (2004) 6848-6849
107. Schmitt M.A., Weisblum B., and Gellman S.H. Interplay among folding, sequence, and lipophilicity in the antibacterial and hemolytic activities of alpha/beta-peptides. J. Am. Chem. Soc. 129 (2007) 417-428
108. Tew G.N., Liu D., Chen B., Doerksen R.J., Kaplan J., Carroll P.J., Klein M.L., and DeGrado W.F. De novo design of biomimetic antimicrobial polymers. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 5110-5114
109. Tang H., Doerksen R.J., Jones T.V., Klein M.L., and Tew G.N. Biomimetic facially amphiphilic antibacterial oligomers with conformationally stiff backbones. Chem. Biol. 13 (2006) 427-435
110. Liu D., Choi S., Chen B., Doerksen R.J., Clements D.J., Winkler J.D., Klein M.L., and DeGrado W.F. Nontoxic membrane-active antimicrobial arylamide oligomers. Angew. Chem. Int. Ed. Engl. 43 (2004) 1158-1162
111. Rennie J., Arnt L., Tang H., Nusslein K., and Tew G.N. Simple oligomers as antimicrobial peptide mimics. J. Ind. Microbiol. Biotech. 32 (2005) 296-300
112. Tew G.N., Clements D., Tang H., Arnt L., and Scott R.W. Antimicrobial activity of an abiotic host defense peptide mimic. Biochim. Biophys. Acta 1758 (2006) 1387-1392
113. Beckloff N., Laube D., Castro T., Furgang D., Park S., Perlin D., Clements D., Tang H., Scott R.W., Tew G.N., and Diamond G. Activity of an antimicrobial peptide mimetic against planktonic and biofilm cultures of oral pathogens. Antimicrob. Agents Chemother. 51 (2007) 4125-4132
114. Arnt L., and Tew G.N. New poly(phenyleneethynylene)s with cationic, facially amphiphilic structures. J. Am. Chem. Soc. 124 (2002) 7664-7665
115. Arnt L., and Tew G.N. Cationic facially amphiphilic poly(phenylene ethynylene)s studied at the air-water interface. Langmuir 19 (2003) 2404-2408
116. Ishitsuka Y., Arnt L., Majewski J., Frey S., Ratajczek M., Kjaer K., Tew G.N., and Lee K.Y. Amphiphilic poly(phenyleneethynylene)s can mimic antimicrobial peptide membrane disordering effect by membrane insertion. J. Am. Chem. Soc. 128 (2006) 13123-13129
117. Yang L., Gordon V.D., Mishra A., Som A., Purdy K.R., Davis M.A., Tew G.N., and Wong G.C. Synthetic antimicrobial oligomers induce a composition-dependent topological transition in membranes. J. Am. Chem. Soc. 129 (2007) 12141-12147
118. Chen X., Tang H., Even M.A., Wang J., Tew G.N., and Chen Z. Observing a molecular knife at work. J. Am. Chem. Soc. 128 (2006) 2711-2714
119. Shalev D.E., Rotem S., Fish A., and Mor A. Consequences of N-acylation on structure and membrane binding properties of dermaseptin derivative K4-S4-(1-13). J. Biol. Chem. 281 (2006) 9432-9438
120. Kustanovich I., Shalev D.E., Mikhlin M., Gaidukov L., and Mor A. Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives. J. Biol. Chem. 277 (2002) 16941-16951
121. Lequin O., Ladram A., Chabbert L., Bruston F., Convert O., Vanhoye D., Chassaing G., Nicolas P., and Amiche M. Dermaseptin S9, an alpha-helical antimicrobial peptide with a hydrophobic core and cationic termini. Biochemistry 45 (2006) 468-480
122. Shalev D.E., Mor A., and Kustanovich I. Structural consequences of carboxyamidation of dermaseptin S3. Biochemistry 41 (2002) 7312-7317
123. Krugliak M., Feder R., Zolotarev V.Y., Gaidukov L., Dagan A., Ginsburg H., and Mor A. Antimalarial activities of dermaseptin S4 derivatives. Antimicrob. Agents Chemother. 44 (2000) 2442-2451
124. Navon-Venezia S., Feder R., Gaidukov L., Carmeli Y., and Mor A. Antibacterial properties of dermaseptin S4 derivatives with in vivo activity. Antimicrob. Agents Chemother. 46 (2002) 689-694
125. Feder R., Dagan A., and Mor A. Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity. J. Biol. Chem. 275 (2000) 4230-4238
126. Marynka K., Rotem S., Portnaya I., Cogan U., and Mor A. In vitro discriminative antipseudomonal properties resulting from acyl substitution of N-terminal sequence of dermaseptin s4 derivatives. Chem. Biol. 14 (2007) 75-85
127. Radzishevsky I.S., Kovachi T., Porat Y., Ziserman L., Zaknoon F., Danino D., and Mor A. Structure-activity relationships of antibacterial acyl-lysine oligomers. Chem. Biol 15 (2008) 354-362
128. Sarig H., Rotem S., Ziserman L., Danino D., and Mor A. Impact of self-assembly properties on antibacterial activity of short acyl-lysine oligomers. Antimicrob. Agents Chemother 52 (2008) 4308-4314
129. Radzishevsky I., Krugliak M., Ginsburg H., and Mor A. Antiplasmodial activity of lauryl-lysine oligomers. Antimicrob. Agents Chemother. 51 (2007) 1753-1759
130. Radzishevsky I.S., Rotem S., Bourdetsky D., Navon-Venezia S., Carmeli Y., and Mor A. Improved antimicrobial peptides based on acyl-lysine oligomers. Nat. Biotechnol. 25 (2007) 657-659
131. Greenfield N.J., and Fasman G.D. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 8 (1969) 4108-4116
132. Avrahami D., Oren Z., and Shai Y. Effect of multiple aliphatic amino acids substitutions on the structure, function, and mode of action of diastereomeric membrane active peptides. Biochemistry 40 (2001) 12591-12603
133. Rotem S., Radzishevsky I.S., Bourdetsky D., Navon-Venezia S., Carmeli Y., and Mor A. Analogous oligo-acyl-lysines with distinct antibacterial mechanisms. FASEB J. 22 (2008) 2652-2661
134. Epand R.F., Rotem S., Mor A., and Epand R.M. Bacterial membranes as a predictor of antimicrobial potency. J. Am. Chem. Soc. 130 (2008) 14346-14352
135. 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
136. Xiong Y.Q., Yeaman M.R., and Bayer A.S. In vitro antibacterial activities of platelet microbicidal protein and neutrophil defensin against Staphylococcus aureus are influenced by antibiotics differing in mechanism of action. Antimicrob. Agents Chemother. 43 (1999) 1111-1117
137. Mor A., Hani K., and Nicolas P. The vertebrate peptide antibiotics dermaseptins have overlapping structural features but target specific microorganisms. J. Biol. Chem. 269 (1994) 31635-31641
138. Levy O., Ooi C.E., Weiss J., Lehrer R.I., and Elsbach P. Individual and synergistic effects of rabbit granulocyte proteins on Escherichia coli. J. Clin. Invest. 94 (1994) 672-682
139. Dagan A., Efron L., Gaidukov L., Mor A., and Ginsburg H. In vitro antiplasmodium effects of dermaseptin S4 derivatives. Antimicrob. Agents Chemother. 46 (2002) 1059-1066
140. Efron L., Dagan A., Gaidukov L., Ginsburg H., and Mor A. Direct interaction of dermaseptin S4 aminoheptanoyl derivative with intraerythrocytic malaria parasite leading to increased specific antiparasitic activity in culture. J. Biol. Chem. 277 (2002) 24067-24072
141. Mor A., and Nicolas P. Isolation and structure of novel defensive peptides from frog skin. Eur. J. Biochem. 219 (1994) 145-154