Antimicrobial peptides as an opportunity against bacterial diseases

Current Medicinal Chemistry

Volumn 22, Issue 14, 2015, Pages 1665-1677

  Galdiero, Stefania ^a   Falanga, Annarita ^a   Berisio, Rita ^b   Grieco, Paolo ^a   Morelli, Giancarlo ^a   Galdiero, Massimiliano ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

Author keywords

Amphipathic helical peptides; Antimicrobial peptide; Conformational flexibility; Multidrug resistant strain

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL INFECTION; DRUG DESIGN; DRUG MECHANISM; MEMBRANE DAMAGE; NONHUMAN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; BACTERIAL INFECTIONS; BACTERIUM; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; STATIC ELECTRICITY;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; BACTERIAL INFECTIONS; MICROBIAL SENSITIVITY TESTS; STATIC ELECTRICITY;

EID: 84931274697     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867322666150311145632     Document Type: Article

References (155)

1. Aiello, A. E.; Larson, E. Antibacterial cleaning and hygiene products as an emerging risk factor for antibiotic resistance in the community. Lancet Infect Dis., 2003, 3(8), 501-506.
2. Arnold, S. R. Revenge of the killer microbe. CMAJ, 2007, 177(8), 895-896.
3. Gammon, K. Drug discovery: Leaving no stone unturned. Nature, 2014, 509(7498), S10-12.
4. Enserink, M. Resistant Staph Finds New Niches. Science, 2003, 299(5613), 1639-1641.
5. Balows, A. MRSA: current perspectives. Diagnos. Microbiol. Infect. Dis., 2004, 49(1), 75.
6. Chang, S.; Sievert, D. M.; Hageman, J. C.; Boulton, M. L.; Tenover, F. C.; Downes, F. P.; Shah, S.; Rudrik, J. T.; Pupp, G. R.; Brown, W. J.; Cardo, D.; Fridkin, S. K. Infection with vancomycinresistant staphylococcus aureus containing the vana resistance gene. N. Engl. J. Med., 2003, 348(14), 1342-1347.
7. Nakatsuji, T.; Gallo, R. L. Antimicrobial peptides: old molecules with new ideas. J. Invest. Dermatol., 2012, 132(3 Pt 2), 887-895.
8. Gordon, Y. J.; Romanowski, E. G.; McDermott, A. M. A review of antimicrobial peptides and their therapeutic potential as antiinfective drugs. Curr. Eye Res., 2005, 30(7), 505-515.
9. Lazarev, V. N.; Govorun, V. M. Antimicrobial peptides and their use in medicine. Appl. Biochem. Microbiol., 2010, 46(9), 803-814.
10. Hancock, R. E. W.; Sahl, H.-G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotech., 2006, 24(12), 1551-1557.
11. Marr, A. K.; Gooderham, W. J.; Hancock, R. E. Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr. Opin. Pharmacol., 2006, 6(5), 468-472.
12. Yeaman, M. R.; Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev., 2003, 55(1), 27-55.
13. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415(6870), 389-395.
14. Powers, J. P.; Hancock, R. E. The relationship between peptide structure and antibacterial activity. Peptides, 2003, 24(11), 1681-1691.
15. Cruz, J.; Ortiz, C.; Guzman, F.; Fernandez-Lafuente, R.; Torres, R. Antimicrobial peptides: promising compounds against pathogenic microorganisms. Curr. Med. Chem. 2014, 21(20), 2299-2321.
16. Dathe, M.; Wieprecht, T. Structural features of helical antimicrobial peptides: Their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta, 1999, 1462(1-2), 71-87.
17. Paredes-Gamero, E. J.; Martins, M. N.; Cappabianco, F. A.; Ide, J. S.; Miranda, A. Characterization of dual effects induced by antimicrobial peptides: regulated cell death or membrane disruption. Biochim. Biophys. Acta, 2012, 1820(7), 1062-1072.
18. Brown, K. L.; Hancock, R. E. Cationic host defense (antimicrobial) peptides. Curr. Opin. Immunol., 2006, 18(1), 24-30.
19. Lohner, K. New strategies for novel antibiotics: peptides targeting bacterial cell membranes. Gen. Physiol. Biophys., 2009, 28(2), 105-116.
20. Ding, L.; Yang, L.; Weiss, T. M.; Waring, A. J.; Lehrer, R. I.; Huang, H. W. Interaction of antimicrobial peptides with lipopolysaccharides. Biochemistry, 2003, 42(42), 12251-12259.
21. Domingues, M. M.; Inacio, R. G.; Raimundo, J. M.; Martins, M.; Castanho, M. A.; Santos, N. C. Biophysical characterization of polymyxin B interaction with LPS aggregates and membrane model systems. Biopolymers, 2012, 98(4), 338-344.
22. Gogoladze, G.; Grigolava, M.; Vishnepolsky, B.; Chubinidze, M.; Duroux, P.; Lefranc, M. P.; Pirtskhalava, M. DBAASP: database of antimicrobial activity and structure of peptides. FEMS Microbiol. Lett., 2014, 357(1), 63-68.
23. Novkovic, M.; Simunic, J.; Bojovic, V.; Tossi, A.; Juretic, D. DADP: The database of anuran defense peptides. Bioinformatics, 2012, 28(10), 1406-1407.
24. Wang, G.; Li, X.; Wang, Z. APD2: The updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res., 2009, 37(Database issue), D933-D937.
25. Matsuzaki, K.; Murase, O.; Fujii, N.; Miyajima, K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry, 1996, 35(35), 11361-11368.
26. Saviello, M. R.; Malfi, S.; Campiglia, P.; Cavalli, A.; Grieco, P.; Novellino, E.; Carotenuto, A. New Insight into the Mechanism of Action of the Temporin Antimicrobial Peptides. Biochemistry, 2010, 49(7), 1477-1485.
27. Eisenberg, D.; Terwilliger, T. C.; Tsui, F. Structural studies of bee melittin. Biophys. J., 1980, 32(1), 252-4.
28. Irudayam, S. J.; Berkowitz, M. L. Influence of the arrangement and secondary structure of melittin peptides on the formation and stability of toroidal pores. Biochim. Biophys. Acta, 2011, 1808(9), 2258-66.
29. Dennison, S. R.; Wallace, J.; Harris, F.; Phoenix, D. A. Amphiphilic alpha-helical antimicrobial peptides and their structure/function relationships. Protein Pept. Lett., 2005, 12(1), 31-39.
30. Takahashi, D.; Shukla, S. K.; Prakash, O.; Zhang, G. Structural determinants of host defense peptides for antimicrobial activity and target cell selectivity. Biochimie, 2010, 92(9), 1236-1241.
31. Tang, M.; Hong, M. Structure and mechanism of beta-hairpin antimicrobial peptides in lipid bilayers from solid-state NMR spectroscopy. Mol. Biosyst., 2009, 5(4), 317-322.
32. Lehrer, R. I. Primate defensins. Nat. Rev. Microbiol., 2004, 2(9), 727-738.
33. Xu, T.; Levitz, S. M.; Diamond, R. D.; Oppenheim, F. G. Anticandidal activity of major human salivary histatins. Infect Immun., 1991, 59(8), 2549-2554.
34. Chan, D. I.; Prenner, E. J.; Vogel, H. J. Tryptophan-and argininerich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta, 2006, 1758(9), 1184-1202.
35. Rokitskaya, T. I.; Kolodkin, N. I.; Kotova, E. A.; Antonenko, Y. N. Indolicidin action on membrane permeability: carrier mechanism versus pore formation. Biochim. Biophys. Acta, 2011, 1808(1), 91-97.
36. Brogden, K. A.; Ackermann, M. R.; McCray, P. B. Jr.; Huttner, K. M. Differences in the concentrations of small, anionic, antimicrobial peptides in bronchoalveolar lavage fluid and in respiratory epithelia of patients with and without cystic fibrosis. Infect Immun., 1999, 67(8), 4256-4259.
37. Lai, R.; Liu, H.; Hui Lee, W.; Zhang, Y. An anionic antimicrobial peptide from toad Bombina maxima. Biochem. Biophys. Res. Commun., 2002, 295(4), 796-799.
38. Schittek, B.; Hipfel, R.; Sauer, B.; Bauer, J.; Kalbacher, H.; Stevanovic, S.; Schirle, M.; Schroeder, K.; Blin, N.; Meier, F.; Rassner, G.; Garbe, C. Dermcidin: A novel human antibiotic peptide secreted by sweat glands. Nat. Immunol., 2001, 2(12), 1133-1137.
39. Gennaro, R.; Zanetti, M. Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers, 2000, 55(1), 31-49.
40. Bechinger, B. Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J. Membr. Biol., 1997, 156(3), 197-211.
41. Park, C.; Lee, D. G. Melittin induces apoptotic features in Candida albicans. Biochem. Biophys. Res. Commun., 2010, 394(1), 170-172.
42. 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. USA, 1987, 84(15), 5449-5453.
43. Travis, S. M.; Anderson, N. N.; Forsyth, W. R.; Espiritu, C.; Conway, B. D.; Greenberg, E. P.; McCray, P. B. Jr.; Lehrer, R. I.; Welsh, M. J.; Tack, B. F. Bactericidal activity of mammalian cathelicidin-derived peptides. Infect. Immun., 2000, 68(5), 2748-2755.
44. Ostberg, N.; Kaznessis, Y. Protegrin structure-activity relationships: using homology models of synthetic sequences to determine structural characteristics important for activity. Peptides, 2005, 26(2), 197-206.
45. Ganz, T. Immunology. Versatile defensins. Science, 2002, 298(5595), 977-979.
46. Jenssen, H.; Hamill, P.; Hancock, R. E. Peptide antimicrobial agents. Clin. Microbiol. Rev., 2006, 19(3), 491-511.
47. Selsted, M. E.; Novotny, M. J.; Morris, W. L.; Tang, Y. Q.; Smith, W.; Cullor, J. S. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem., 1992, 267(7), 4292-4295.
48. Ladokhin, A. S.; Selsted, M. E.; White, S. H. CD spectra of indolicidin antimicrobial peptides suggest turns, not polyproline helix. Biochemistry, 1999, 38(38), 12313-12319.
49. Rozek, A.; Friedrich, C. L.; Hancock, R. E. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry, 2000, 39(51), 15765-15774.
50. Boman, H. G.; Faye, I.; Gudmundsson, G. H.; Lee, J. Y.; Lidholm, D. A. Cell-free immunity in Cecropia. A model system for antibacterial proteins. Eur. J. Biochem. 1991, 201(1), 23-31.
51. Vermeer, L. S.; Lan, Y.; Abbate, V.; Ruh, E.; Bui, T. T.; Wilkinson, L. J.; Kanno, T.; Jumagulova, E.; Kozlowska, J.; Patel, J.; McIntyre, C. A.; Yam, W. C.; Siu, G.; Atkinson, R. A.; Lam, J. K. W.; Bansal, S. S.; Drake, A. F.; Mitchell, G. H.; Mason, A. J. Conformational flexibility determines selectivity and antibacterial, antiplasmodial, and anticancer potency of cationic-helical peptides. J. Biol. Chem., 2012, 287(41), 34120-34133.
52. Park, C. B.; Kim, H. S.; 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., 1998, 244(1), 253-257.
53. Yang, S. T.; Lee, J. Y.; Kim, H. J.; Eu, Y. J.; Shin, S. Y.; Hahm, K. S.; Kim, J. I. Contribution of a central proline in model amphipathic alpha-helical peptides to self-association, interaction with phospholipids, and antimicrobial mode of action. FEBS J., 2006, 273(17), 4040-4054.
54. Papo, N.; Shai, Y. Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides, 2003, 24(11), 1693-1703.
55. Wieprecht, T.; Dathe, M.; Epand, R. M.; Beyermann, M.; Krause, E.; Maloy, W. L.; MacDonald, D. L.; Bienert, M. Influence of the angle subtended by the positively charged helix face on the membrane activity of amphipathic, antibacterial peptides. Biochemistry, 1997, 36(42), 12869-12880.
56. Galdiero, S.; Falanga, A.; Cantisani, M.; Vitiello, M.; Morelli, G.; Galdiero, M. Peptide-lipid interactions: experiments and applications. Int. J. Mol. Sci., 2013, 14(9), 18758-18789.
57. Galdiero, S.; Russo, L.; Falanga, A.; Cantisani, M.; Vitiello, M.; Fattorusso, R.; Malgieri, G.; Galdiero, M.; Isernia, C. Structure and orientation of the gH625-644 membrane interacting region of herpes simplex virus type 1 in a membrane mimetic system. Biochemistry, 2012, 51(14), 3121-3128.
58. Falanga, A.; Tarallo, R.; Vitiello, G.; Vitiello, M.; Perillo, E.; Cantisani, M.; D'Errico, G.; Galdiero, M.; Galdiero, S. Biophysical characterization and membrane interaction of the two fusion loops of glycoprotein B from herpes simplex type I virus. PLoS One, 2012, 7(2), e32186.
59. Galdiero, S.; Falanga, A.; Vitiello, M.; Raiola, L.; Russo, L.; Pedone, C.; Isernia, C.; Galdiero, M. The presence of a single Nterminal histidine residue enhances the fusogenic properties of a Membranotropic peptide derived from herpes simplex virus type 1 glycoprotein H. J. Biol., Chem., 2010, 285(22), 17123-17136.
60. Falanga, A.; Cantisani, M.; Pedone, C.; Galdiero, S. Membrane fusion and fission: enveloped viruses. Protein Pept. Lett., 2009, 16(7), 751-759.
61. Galdiero, S. Editorial: Developments in membrane fusion. Protein Pept. Lett., 2009, 16(7), 711.
62. Galdiero, S.; Falanga, A.; Vitiello, M.; Raiola, L.; Fattorusso, R.; Browne, H.; Pedone, C.; Isernia, C.; Galdiero, M. Analysis of a membrane interacting region of herpes simplex virus type 1 glycoprotein H. J. Biol. Chem., 2008, 283(44), 29993-30009.
63. Joanne, P.; Nicolas, P.; El Amri, C. Antimicrobial peptides and viral fusion peptides: how different they are? Protein Pept. Lett., 2009, 16(7), 743-750.
64. Matsuzaki, K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta, 1998, 1376(3), 391-400.
65. Haney, E. F.; Hunter, H. N.; Matsuzaki, K.; Vogel, H. J. Solution NMR studies of amphibian antimicrobial peptides: linking structure to function Biochim. Biophys. Acta, 2009, 1788(8), 1639-1655.
66. Syvitski, R. T.; Burton, I.; Mattatall, N. R.; Douglas, S. E.; Jakeman, D. L. Structural characterization of the antimicrobial peptide pleurocidin from winter flounder. Biochemistry, 2005, 44(19), 7282-7293.
67. Mangoni, M. L. Temporins, anti-infective peptides with expanding properties. Cell Mol. Life Sci., 2006, 63(9), 1060-1069.
68. Mangoni, M. L.; Carotenuto, A.; Auriemma, L.; Saviello, M. R.; Campiglia, P.; Gomez-Monterrey, I.; Malfi, S.; Marcellini, L.; Barra, D.; Novellino, E.; Grieco, P. Structure-activity relationship, conformational and biological studies of temporin L analogues. J. Med. Chem., 2011, 54(5), 1298-1307.
69. Becucci, L.; Papini, M.; Mullen, D.; Scaloni, A.; Veglia, G.; Guidelli, R. Probing membrane permeabilization by the antimicrobial peptide distinctin in mercury-supported biomimetic membranes. Biochim. Biophys. Acta, 2011, 1808(11), 2745-52.
70. Verardi, R.; Traaseth, N. J.; Shi, L.; Porcelli, F.; Monfregola, L.; De Luca, S.; Amodeo, P.; Veglia, G.; Scaloni, A. Probing membrane topology of the antimicrobial peptide distinctin by solidstate NMR spectroscopy in zwitterionic and charged lipid bilayers. Biochim. Biophys. Acta, 2011, 1808(1), 34-40.
71. de Vos, W. M.; Mulders, J. W.; Siezen, R. J.; Hugenholtz, J.; Kuipers, O. P. Properties of nisin Z and distribution of its gene, nisZ, in Lactococcus lactis. Appl. Environ. Microbiol., 1993, 59(1), 213-218.
72. Twomey, D.; Ross, R. P.; Ryan, M.; Meaney, B.; Hill, C. Lantibiotics produced by lactic acid bacteria: structure, function and applications. Antonie Van Leeuwenhoek, 2002, 82(1-4), 165-185.
73. Steiner, H.; Hultmark, D.; Engstrom, A.; Bennich, H.; Boman, H. G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292: 246-248. 1981. J. Immunol., 2009, 182(11), 6635-6637.
74. Bechinger, B.; Zasloff, M.; Opella, S. J. Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Protein Sci., 1993, 2(12), 2077-2084.
75. Romeo, D.; Skerlavaj, B.; Bolognesi, M.; Gennaro, R. Structure and bactericidal activity of an antibiotic dodecapeptide purified from bovine neutrophils. J. Biol. Chem., 1988, 263(20), 9573-9575.
76. Selsted, M. E.; Harwig, S. S.; Ganz, T.; Schilling, J. W.; Lehrer, R. I. Primary structures of three human neutrophil defensins. J. Clin. Invest., 1985, 76(4), 1436-1439.
77. Jarczak, J.; Kosciuczuk, E. M.; Lisowski, P.; Strzalkowska, N.; Jozwik, A.; Horbanczuk, J.; Krzyzewski, J.; Zwierzchowski, L.; Bagnicka, E. Defensins: natural component of human innate immunity. Hum. Immunol., 2013, 74(9), 1069-1079.
78. Luque-Ortega, J. R.; van't Hof, W.; Veerman, E. C.; Saugar, J. M.; Rivas, L. Human antimicrobial peptide histatin 5 is a cellpenetrating peptide targeting mitochondrial ATP synthesis in Leishmania. FASEB J., 2008, 22(6), 1817-1828.
79. Tsai, H.; Bobek, L. A. Human salivary histatins: promising antifungal therapeutic agents. Crit. Rev. Oral Biol. Med., 1998, 9(4), 480-497.
80. Huo, L.; Zhang, K.; Ling, J.; Peng, Z.; Huang, X.; Liu, H.; Gu, L. Antimicrobial and DNA-binding activities of the peptide fragments of human lactoferrin and histatin 5 against Streptococcus mutans. Arch. Oral Biol., 2011, 56(9), 869-876.
81. Brogden, K. A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3), 238-250.
82. Galdiero, S.; Falanga, A.; Morelli, G.; Galdiero, M. gH625: A milestone in understanding the many roles of membranotropic peptides. Biochim. Biophys. Acta, 2015, 1848, 16-25.
83. Galdiero, S.; Falanga, A.; Vitiello, M.; Grieco, P.; Caraglia, M.; Morelli, G.; Galdiero, M. Exploitation of viral properties for intracellular delivery. J. Pept. Sci., 2014, 20(7), 468-478.
84. Galdiero, S.; Vitiello, M.; Falanga, A.; Cantisani, M.; Incoronato, N.; Galdiero, M. Intracellular delivery: exploiting viral membranotropic peptides. Curr. Drug Metab., 2012, 13(1), 93-104.
85. Splith, K.; Neundorf, I. Antimicrobial peptides with cellpenetrating peptide properties and vice versa. Eur. Biophys. J., 2011, 40(4), 387-397.
86. Valiante, S.; Falanga, A.; Cigliano, L.; Iachetta, G.; Busiello, R. A.; La Marca, V.; Galdiero, M.; Lombardi, A.; Galdiero, S. The peptide gH625 enters into neuron and astrocyte cell lines and crosses the Blood Brain Barrier in rats. Int. J. Nanomed., 2015, 10, 1885-1898.
87. Subbalakshmi, C.; Sitaram, N. Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett., 1998, 160(1), 91-96.
88. Gennaro, R.; Zanetti, M.; Benincasa, M.; Podda, E.; Miani, M. Prorich antimicrobial peptides from animals: structure, biological functions and mechanism of action. Curr. Pharm. Des., 2002, 8(9), 763-778.
89. Boman, H. G.; Agerberth, B.; Boman, A. Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun., 1993, 61(7), 2978-2984.
90. Gryllos, I.; Tran-Winkler, H. J.; Cheng, M. F.; Chung, H.; Bolcome, R. 3rd; Lu, W.; Lehrer, R. I.; Wessels, M. R. Induction of group A Streptococcus virulence by a human antimicrobial peptide. Proc. Natl. Acad. Sci. U. S. A., 2008, 105(43), 16755-16760.
91. Aggarwal, K.; Silverman, N. Positive and negative regulation of the Drosophila immune response. BMB Rep., 2008, 41(4), 267-277
92. 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, 1999 1462(1-2), 55-70.
93. Pouny, Y.; Rapaport, D.; Mor, A.; Nicolas, P.; Shai, Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry, 1992, 31(49), 12416-12423.
94. Kouzayha, A.; Nasir, M. N.; Buchet, R.; Wattraint, O.; Sarazin, C.; Besson, F. Conformational and interfacial analyses of K3A18K3 and alamethicin in model membranes. J. Phys. Chem. B., 2009, 113(19), 7012-7019.
95. Ladokhin, A. S.; White, S. H. 'Detergent-like' permeabilization of anionic lipid vesicles by melittin. Biochim. Biophys. Acta, 2001, 1514(2), 253-260.
96. Dagan, A.; Efron, L.; Gaidukov, L.; Mor, A.; Ginsburg, H. In vitro antiplasmodium effects of dermaseptin S4 derivatives. Antimicrob. Agents Chemother., 2002, 46(4), 1059-1066.
97. Lee, I. H.; Cho, Y.; Lehrer, R. I. Effects of pH and salinity on the antimicrobial properties of clavanins. Infect Immun., 1997, 65(7), 2898-2903.
98. Rotem, S.; Mor, A. Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta, 2009, 1788(8), 1582-1592.
99. Bradshaw, J. Cationic antimicrobial peptides: issues for potential clinical use. BioDrugs, 2003, 17(4), 233-240.
100. Hancock, R. E. W.; Brown, K. L.; Mookherjee, N. Host defence peptides from invertebrates-emerging antimicrobial strategies. Immunobiology, 2006, 211(4), 315-322.
101. Danial, M.; van Dulmen, T. H.; Aleksandrowicz, J.; Potgens, A. J.; Klok, H. A. Site-specific PEGylation of HR2 peptides: effects of PEG conjugation position and chain length on HIV-1 membrane fusion inhibition and proteolytic degradation. Bioconjug. Chem., 2012, 23(8), 1648-1660.
102. Papo, N.; Oren, Z.; Pag, U.; Sahl, H. G.; Shai, Y. The consequence of sequence alteration of an amphipathic alpha-helical antimicrobial peptide and its diastereomers. J. Biol. Chem., 2002, 277(37), 33913-33921.
103. Hicks, R. P.; Bhonsle, J. B.; Venugopal, D.; Koser, B. W.; Magill, A. J. De novo design of selective antibiotic peptides by incorporation of unnatural amino acids. J. Med. Chem., 2007, 50(13), 3026-3036.
104. Park, Y.; Hahm, K. S. Novel short AMP: design and activity study. Protein Pept. Lett., 2012, 19(6), 652-656.
105. Kang, S. J.; Won, H. S.; Choi, W. S.; Lee, B. J. De novo generation of antimicrobial LK peptides with a single tryptophan at the critical amphipathic interface. J. Pept. Sci., 2009, 15(9), 583-588.
106. Brandelli, A. Nanostructures as promising tools for delivery of antimicrobial peptides. Mini Rev. Med. Chem., 2012, 12(8), 731-741.
107. Tam, J. P.; Lu, Y. A.; Yang, J. L. Antimicrobial dendrimeric peptides. Eur. J. Biochem., 2002, 269(3), 923-932.
108. Juretic, D.; Vukicevic, D.; Ilic, N.; Antcheva, N.; Tossi, A. Computational design of highly selective antimicrobial peptides. J. Chem. Inf. Model, 2009, 49(12), 2873-2882.
109. Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers, 2000, 55(1), 4-30.
110. Rydlo, T.; Rotem, S.; Mor, A. Antibacterial properties of dermaseptin S4 derivatives under extreme incubation conditions. Antimicrob. Agents Chemother., 2006, 50(2), 490-497.
111. Kustanovich, I.; Shalev, D. E.; Mikhlin, M.; Gaidukov, L.; Mor, A. Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives. J. Biol. Chem., 2002, 277(19), 16941-16951.
112. Houston, M. E. Jr.; Kondejewski, L. H.; Karunaratne, D. N.; Gough, M.; Fidai, S.; Hodges, R. S.; Hancock, R. E. Influence of preformed alpha-helix and alpha-helix induction on the activity of cationic antimicrobial peptides. J. Pept. Res., 1998, 52(2), 81-88.
113. Giangaspero, A.; Sandri, L.; Tossi, A. Amphipathic alpha helical antimicrobial peptides. Eur. J. Biochem., 2001, 268(21), 5589-5600.
114. Ladokhin, A. S.; White, S. H. Folding of amphipathic-helices on membranes: energetics of helix formation by melittin. J. Mol. Biol., 1999, 285(4), 1363-1369.
115. Dempsey, C. E.; Hawrani, A.; Howe, R. A.; Walsh, T. R. Amphipathic antimicrobial peptides-from biophysics to therapeutics? Protein Pept. Lett. 2010, 17(11), 1334-1344.
116. Matsuzaki, K. Control of cell selectivity of antimicrobial peptides. Biochim. Biophys. Acta, 2009, 1788(8), 1687-1692.
117. Bhargava, K.; Feix, J. B. Membrane binding, structure, and localization of cecropin-mellitin hybrid peptides: A site-directed spin-labeling study. Biophys. J., 2004, 86(1 I), 329-336.
118. Turner, J.; Cho, Y.; Dinh, N. N.; Waring, A. J.; Lehrer, R. I. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother., 1998, 42(9), 2206-14.
119. Scudiero, O.; Galdiero, S.; Cantisani, M.; Di Noto, R.; Vitiello, M.; Galdiero, M.; Naclerio, G.; Cassiman, J. J.; Pedone, C.; Castaldo, G.; Salvatore, F. Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob. Agents Chemother., 2010, 54(6), 2312-2322.
120. Matsuzaki, K.; Nakamura, A.; Murase, O.; Sugishita, K.-i.; Fujii, N.; Miyajima, K. Modulation of magainin 2 lipid bilayer interactions by peptide charge. Biochemistry, 1997, 36, (8), 2104-2111.
121. Osapay, K.; Tran, D.; Ladokhin, A. S.; White, S. H.; Henschen, A. H.; Selsted, M. E. Formation and characterization of a single Trp-Trp cross-link in indolicidin that confers protease stability without altering antimicrobial activity. J. Biol. Chem., 2000, 275(16), 12017-12022.
122. Grieco, P.; Luca, V.; Auriemma, L.; Carotenuto, A.; Saviello, M. R.; Campiglia, P.; Barra, D.; Novellino, E.; Mangoni, M. L. Alanine scanning analysis and structure-function relationships of the frog-skin antimicrobial peptide temporin-1Ta. J. Pept. Sci., 2011, 17(5), 358-365.
123. Subramanian, S.; Ross, N. W.; MacKinnon, S. L. Myxinidin, a novel antimicrobial peptide from the epidermal mucus of hagfish, Myxine glutinosa L. Mar. Biotechnol. (NY) 2009, 11(6), 748-757.
124. Cantisani, M.; Finamore, E.; Mignogna, E.; Falanga, A.; Nicoletti, G. F.; Pedone, C.; Morelli, G.; Leone, M.; Galdiero, M.; Galdiero, S. Structural insights into and activity analysis of the antimicrobial peptide myxinidin. Antimicrob. Agents Chemother., 2014, 58 (9), 5280-5290.
125. Cantisani, M.; Leone, M.; Mignogna, E.; Kampanaraki, K.; Falanga, A.; Morelli, G.; Galdiero, M.; Galdiero, S. Structureactivity relations of myxinidin, an antibacterial peptide derived from the epidermal mucus of hagfish. Antimicrob. Agents Chemother., 2013, 57 (11), 5665-5673.
126. Scudiero, O.; Galdiero, S.; Nigro, E.; Del Vecchio, L.; Di Noto, R.; Cantisani, M.; Colavita, I.; Galdiero, M.; Cassiman, J. J.; Daniele, A.; Pedone, C.; Salvatore, F. Chimeric beta-defensin analogs, including the novel 3NI analog, display salt-resistant antimicrobial activity and lack toxicity in human epithelial cell lines. Antimicrob. Agents Chemother., 2013, 57(4), 1701-1708.
127. Onaizi, S. A.; Leong, S. S. Tethering antimicrobial peptides: current status and potential challenges. Biotechnol. Adv., 2011, 29(1), 67-74.
128. Dutta, D.; Cole, N.; Kumar, N.; Willcox, M. D. Broad spectrum antimicrobial activity of melimine covalently bound to contact lenses. Invest. Ophthalmol. Vis. Sci., 2013, 54(1), 175-182.
129. Li, X.; Li, P.; Saravanan, R.; Basu, A.; Mishra, B.; Lim, S. H.; Su, X.; Tambyah, P. A.; Leong, S. S. Antimicrobial functionalization of silicone surfaces with engineered short peptides having broad spectrum antimicrobial and salt-resistant properties. Acta Biomater., 2014, 10(1), 258-266.
130. Holmberg, K. V.; Abdolhosseini, M.; Li, Y.; Chen, X.; Gorr, S. U.; Aparicio, C. Bio-inspired stable antimicrobial peptide coatings for dental applications. Acta Biomater., 2013, 9(9), 8224-8231.
131. Kazemzadeh-Narbat, M.; Lai, B. F.; Ding, C.; Kizhakkedathu, J. N.; Hancock, R. E.; Wang, R. Multilayered coating on titanium for controlled release of antimicrobial peptides for the prevention of implant-associated infections. Biomaterials, 2013, 34(24), 5969-5977.
132. Tarallo, R.; Carberry, T. P.; Falanga, A.; Vitiello, M.; Galdiero, S.; Galdiero, M.; Weck, M. Dendrimers functionalized with membrane-interacting peptides for viral inhibition. Int. J. Nanomed., 2013, 8, 521-534.
133. Pini, A.; Giuliani, A.; Falciani, C.; Runci, Y.; Ricci, C.; Lelli, B.; Malossi, M.; Neri, P.; Rossolini, G. M.; Bracci, L. Antimicrobial activity of novel dendrimeric peptides obtained by phage displayselection and rational modification. Antimicrob. Agents Chemother., 2005, 49(7), 2665-2672.
134. Bruschi, M.; Pirri, G.; Giuliani, A.; Nicoletto, S. F.; Baster, I.; Scorciapino, M. A.; Casu, M.; Rinaldi, A. C. Synthesis, characterization, antimicrobial activity and LPS-interaction properties of SB041, a novel dendrimeric peptide with antimicrobial properties. Peptides, 2010, 31(8), 1459-1467.
135. dos Santos, C. A.; Seckler, M. M.; Ingle, A. P.; Gupta, I.; Galdiero, S.; Galdiero, M.; Gade, A.; Rai, M. Silver nanoparticles: Therapeutical uses, toxicity, and safety issues. J. Pharm. Sci., 2014, 103(7), 1931-1944.
136. Gaikwad, S.; Ingle, A.; Gade, A.; Rai, M.; Falanga, A.; Incoronato, N.; Russo, L.; Galdiero, S.; Galdiero, M. Antiviral activity of mycosynthesized silver nanoparticles against herpes simplex virus and human parainfluenza virus type 3. Int. J. Nanomed., 2013, 8, 4303-4314.
137. Galdiero, S.; Falanga, A.; Vitiello, M.; Cantisani, M.; Marra, V.; Galdiero, M. Silver nanoparticles as potential antiviral agents. Molecules, 2011, 16(10), 8894-8918.
138. Rai, M.; Deshmukh, S. D.; Ingle, A. P.; Gupta, I. R.; Galdiero, M.; Galdiero, S. Metal nanoparticles: The protective nanoshield against virus infection. Crit. Rev. Microbiol., 2014. doi:10. 3109/1040841X. 2013. 879849.
139. Rai, M.; Kon, K.; Ingle, A.; Duran, N.; Galdiero, S.; Galdiero, M. Broad-spectrum bioactivities of silver nanoparticles: The emerging trends and future prospects. Appl. Microbiol. Biotechnol., 2014, 98(5), 1951-1961.
140. Galdiero, S.; Falanga, A.; Cantisani, M.; Ingle, A.; Galdiero, M.; Rai, M. Silver Nanoparticles as Novel Antibacterial and Antiviral Agents. In Handbook of Nanobiomedical Research, 2014, pp. 565-594.
141. Hankins, J. V.; Madsen, J. A.; Giles, D. K.; Brodbelt, J. S.; Trent, M. S. Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in gram-positive and gramnegative bacteria. Proc. Natl. Acad. Sci. USA, 2012, 109(22), 8722-8727.
142. Strandberg, K. L.; Richards, S. M.; Tamayo, R.; Reeves, L. T.; Gunn, J. S. An altered immune response, but not individual cationic antimicrobial peptides, is associated with the oral attenuation of Ara4N-deficient Salmonella enterica serovar Typhimurium in mice. PLoS One, 2012, 7(11), e49588.
143. Tran, A. X.; Whittimore, J. D.; Wyrick, P. B.; McGrath, S. C.; Cotter, R. J.; Trent, M. S. The lipid A 1-phosphatase of Helicobacter pylori is required for resistance to the antimicrobial peptide polymyxin. J. Bacteriol., 2006, 188(12), 4531-4541.
144. Andra, J.; Goldmann, T.; Ernst, C. M.; Peschel, A.; Gutsmann, T. Multiple peptide resistance factor (MprF)-mediated Resistance of Staphylococcus aureus against antimicrobial peptides coincides with a modulated peptide interaction with artificial membranes comprising lysyl-phosphatidylglycerol. J. Biol. Chem., 2011, 286(21), 18692-18700.
145. Schmidtchen, A.; Frick, I. M.; Andersson, E.; Tapper, H.; Bjorck, L. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol., 2002, 46(1), 157-168.
146. Belas, R.; Manos, J.; Suvanasuthi, R. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect. Immun., 2004, 72(9), 5159-5167.
147. Ge, Y.; MacDonald, D. L.; Holroyd, K. J.; Thornsberry, C.; Wexler, H.; Zasloff, M. In vitro antibacterial properties of pexiganan, an analog of magainin. Antimicrob. Agents Chemother., 1999, 43(4), 782-788.
148. Lamb, H. M.; Wiseman, L. R. Pexiganan acetate. Drugs 1998, 56(6), 1047-1052; discussion 1053-1054.
149. Moore, A. The big and small of drug discovery. Biotech versus pharma: Advantages and drawbacks in drug development. EMBO Rep., 2003, 4(2), 114-117.
150. Bu, H. F.; Wang, X.; Zhu, Y. Q.; Williams, R. Y.; Hsueh, W.; Zheng, X.; Rozenfeld, R. A.; Zuo, X. L.; Tan, X. D. Lysozymemodified probiotic components protect rats against polymicrobial sepsis: role of macrophages and cathelicidin-related innate immunity. J. Immunol., 2006, 177(12), 8767-8776.
151. Yang, Y. H.; Wu, W. K.; Tai, E. K.; Wong, H. P.; Lam, E. K.; So, W. H.; Shin, V. Y.; Cho, C. H. The cationic host defense peptide rCRAMP promotes gastric ulcer healing in rats. J. Pharmacol. Exp. Ther., 2006, 318(2), 547-554.
152. Sader, H. S.; Fedler, K. A.; Rennie, R. P.; Stevens, S.; Jones, R. N. Omiganan pentahydrochloride (MBI 226), a topical 12-amino-acid cationic peptide: spectrum of antimicrobial activity and measurements of bactericidal activity. Antimicrob. Agents Chemother., 2004, 48(8), 3112-3118.
153. Panyutich, A.; Shi, J.; Boutz, P. L.; Zhao, C.; Ganz, T. Porcine polymorphonuclear leukocytes generate extracellular microbicidal activity by elastase-mediated activation of secreted proprotegrins. Infect. Immun., 1997, 65(3), 978-985.
154. Brewer, D.; Hunter, H.; Lajoie, G. NMR studies of the antimicrobial salivary peptides histatin 3 and histatin 5 in aqueous and nonaqueous solutions. Biochem. Cell Biol., 1998, 76(2-3), 247-256.
155. Giroir, B. P.; Quint, P. A.; Barton, P.; Kirsch, E. A.; Kitchen, L.; Goldstein, B.; Nelson, B. J.; Wedel, N. J.; Carroll, S. F.; Scannon, P. J. Preliminary evaluation of recombinant amino-terminal fragment of human bactericidal/permeability-increasing protein in children with severe meningococcal sepsis. Lancet, 1997, 350(9089), 1439-1443.