Characterization of antimicrobial peptides toward the development of novel antibiotics

Pharmaceuticals

Volumn 6, Issue 8, 2013, Pages 1055-1081

  Aoki, Wataru ^a,b,c   Ueda, Mitsuyoshi ^b  

^a JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Activity regulation; Antibiotic; Antimicrobial peptide; Drug delivery

Indexed keywords

ADEPANTIN 1; ANTIBIOTIC AGENT; APIDAECIN; BETA DEFENSIN; BUFORIN II; CLAVANIN A; DROSOCIN; GRAMICIDIN S; LACTOFERRICIN; LASIOGLOSSIN III; MAGAININ 2; MELITTIN; ONCOCIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN AAP2; PROTEIN HBD1; PROTEIN HBD2; PROTEIN HBD3; PROTEIN HBD4; PROTEIN HNP1; PROTEIN HNP2; PROTEIN HNP3; PROTEIN HNP4; PROTEIN M8G2; PROTEIN R5L; PROTEIN RTD1; PROTEINASE ACTIVATED ADENOSINE PHOSPHATE; PYRRHOCORICIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; DRUG DEGRADATION; DRUG DESIGN; DRUG EFFICACY; DRUG MANUFACTURE; DRUG MECHANISM; DRUG METABOLISM; DRUG RESEARCH; DRUG SAFETY; DRUG SOLUBILITY; DRUG STRUCTURE; EPITHELIUM CELL; GRAM NEGATIVE BACTERIUM; GROUP A STREPTOCOCCAL INFECTION; HEMOLYSIS; HOSPITAL INFECTION; HUMAN; HYDROPHOBICITY; INNATE IMMUNITY; LARGE SCALE PRODUCTION; LEUKOCYTE FUNCTION; MEMBRANE DAMAGE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR INTERACTION; MOLECULARLY TARGETED THERAPY; MULTIDRUG RESISTANCE; NEUTROPHIL; NONHUMAN; PATIENT COMPLIANCE; PHAGOCYTOSIS; QUALITY OF LIFE; REVIEW; STRUCTURE ACTIVITY RELATION; SURFACE CHARGE;

EID: 84882808925     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph6081055     Document Type: Review

References (169)

1. Demain, A.L.; Sanchez, S. Microbial drug discovery: 80 years of progress. J. Antibiot. 2009, 62, 5-16.
2. Schatz, A.; Bugie, E.; Waksman, S.A. Streptomycin, a substance exhibiting antibiotic activity against gram-positive and gram-negative bacteria. Exp. Biol. Med. 1944, 55, 66-69.
3. Lopez, A.D.; Mathers, C.D.; Ezzati, M.; Jamison, D.T.; Murray, C.J. Global and regional burden of disease and risk factors, 2001: Systematic analysis of population health data. Lancet 2006, 367, 1747-1757.
4. Morris, S.; Bai, G.H.; Suffys, P.; Portillo-Gomez, L.; Fairchok, M.; Rouse, D. Molecular mechanisms of multiple drug resistance in clinical isolates of Mycobacterium tuberculosis. J. Infect. Dis. 1995, 171, 954-960.
5. Cohen, M.L. Epidemiology of drug resistance: Implications for a post-antimicrobial era. Science 1992, 257, 1050-1055.
6. Aloush, V.; Navon-Venezia, S.; Seigman-Igra, Y.; Cabili, S.; Carmeli, Y. Multidrug-resistant Pseudomonas aeruginosa: Risk factors and clinical impact. Antimicrob. Agents Chemother. 2006, 50, 43-48.
7. Hiramatsu, K.; Aritaka, N.; Hanaki, H.; Kawasaki, S.; Hosoda, Y.; Hori, S.; Fukuchi, Y.; Kobayashi, I. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 1997, 350, 1670-1673.
8. Manchanda, V.; Sanchaita, S.; Singh, N. Multidrug resistant Acinetobacter. J. Glob. Infect. Dis. 2010, 2, 291-304.
9. Lee, M.; Lee, J.; Carroll, M.W.; Choi, H.; Min, S.; Song, T.; Via, L.E.; Goldfeder, L.C.; Kang, E.; Jin, B.; et al. Linezolid for treatment of chronic extensively drug-resistant tuberculosis. N. Engl. J. Med. 2012, 367, 1508-1518.
10. Ament, P.W.; Jamshed, N.; Horne, J.P. Linezolid: Its role in the treatment of gram-positive, drug-resistant bacterial infections. Am. Fam. Physician 2002, 65, 663-670.
11. Colca, J.R.; McDonald, W.G.; Waldon, D.J.; Thomasco, L.M.; Gadwood, R.C.; Lund, E.T.; Cavey, G.S.; Mathews, W.R.; Adams, L.D.; Cecil, E.T.; et al. Cross-linking in the living cell locates the site of action of oxazolidinone antibiotics. J. Biol. Chem. 2003, 278, 21972-21979.
12. Sanchez Garcia, M.; de la Torre, M.A.; Morales, G.; Pelaez, B.; Tolon, M.J.; Domingo, S.; Candel, F.J.; Andrade, R.; Arribi, A.; Garcia, N.; et al. Clinical outbreak of linezolid-resistant Staphylococcus aureus in an intensive care unit. JAMA 2010, 303, 2260-2264.
13. Seo, M.D.; Won, H.S.; Kim, J.H.; Mishig-Ochir, T.; Lee, B.J. Antimicrobial peptides for therapeutic applications: A review. Molecules 2012, 17, 12276-12286.
14. Kosciuczuk, E.M.; Lisowski, P.; Jarczak, J.; Strzalkowska, N.; Jozwik, A.; Horbanczuk, J.; Krzyzewski, J.; Zwierzchowski, L.; Bagnicka, E. Cathelicidins: Family of antimicrobial peptides. A review. Mol. Biol. Rep. 2012, 39, 10957-10970.
15. 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, 5449-5453.
16. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389-395.
17. Soravia, E.; Martini, G.; Zasloff, M. Antimicrobial properties of peptides from Xenopus granular gland secretions. FEBS Lett. 1988, 228, 337-340.
18. Giuliani, A.; Pirri, G.; Nicoletto, S.F. Antimicrobial peptides: An overview of a promising class of therapeutics. Cent. Eur. J. Biol. 2007, 2, 1-33.
19. Yount, N.Y.; Yeaman, M.R. Structural congruence among membrane-active host defense polypeptides of diverse phylogeny. Biochim. Biophys. Acta 2006, 1758, 1373-1386.
20. Brogden, K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250.
21. Park, S.C.; Park, Y.; Hahm, K.S. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int. J. Mol. Sci. 2011, 12, 5971-5992.
22. Wakabayashi, H.; Hiratani, T.; Uchida, K.; Yamaguch, H. Antifungal spectrum and fungicidal mechanism of an N-terminal peptide of bovine lactoferrin. J. Infect. Chemother. 1996, 1, 185-189.
23. Yamauchi, K.; Tomita, M.; Giehl, T.J.; Ellison, R.T., 3rd. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun. 1993, 61, 719-728.
24. Mygind, P.H.; Fischer, R.L.; Schnorr, K.M.; Hansen, M.T.; Sonksen, C.P.; Ludvigsen, S.; Raventos, D.; Buskov, S.; Christensen, B.; de Maria, L.; et al. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 2005, 437, 975-980.
25. Helmerhorst, E.J.; Reijnders, I.M.; vant Hof, W.; Veerman, E.C.; Nieuw Amerongen, A.V. A critical comparison of the hemolytic and fungicidal activities of cationic antimicrobial peptides. FEBS Lett. 1999, 449, 105-110.
26. Aoki, W.; Kuroda, K.; Ueda, M. Next generation of antimicrobial peptides as molecular targeted medicines. J. Biosci. Bioeng. 2012, 114, 365-370.
27. Jenssen, H.; Aspmo, S.I. Serum stability of peptides. Methods Mol. Biol. 2008, 494, 177-186.
28. Bals, R.; Goldman, M.J.; Wilson, J.M. Mouse beta-defensin 1 is a salt-sensitive antimicrobial peptide present in epithelia of the lung and urogenital tract. Infect. Immun. 1998, 66, 1225-1232.
29. 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, 71-87.
30. Matsuzaki, K.; Sugishita, K.; Fujii, N.; Miyajima, K. Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2. Biochemistry 1995, 34, 3423-3429.
31. Ganz, T. Defensins and host defense. Science 1999, 286, 420-421.
32. Bellamy, W. Antifungal properties of lactoferricin B, a peptide derived from the N-terminal region of bovine lactoferrin. Lett. Appl. Microbiol. 1994, 18, 230-233.
33. Gifford, J.L.; Hunter, H.N.; Vogel, H.J. Lactoferricin: A lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol. Life Sci. 2005, 62, 2588-2598.
34. Nibbering, P.H.; Ravensbergen, E.; Welling, M.M.; van Berkel, L.A.; van Berkel, P.H.; Pauwels, E.K.; Nuijens, J.H. Human lactoferrin and peptides derived from its N terminus are highly effective against infections with antibiotic-resistant bacteria. Infect. Immun. 2001, 69, 1469-1476.
35. Dijkshoorn, L.; Brouwer, C.P.; Bogaards, S.J.; Nemec, A.; van den Broek, P.J.; Nibbering, P.H. The synthetic N-terminal peptide of human lactoferrin, hLF(1-11), is highly effective against experimental infection caused by multidrug-resistant Acinetobacter. baumannii. Antimicrob. Agents Chemother. 2004, 48, 4919-4921.
36. Bellamy, W.; Wakabayashi, H.; Takase, M.; Kawase, K.; Shimamura, S.; Tomita, M. Killing of Candida albicans by lactoferricin B, a potent antimicrobial peptide derived from the N-terminal region of bovine lactoferrin. Med. Microbiol. Immunol. 1993, 182, 97-105.
37. Bellamy, W.; Takase, M.; Wakabayashi, H.; Kawase, K.; Tomita, M. Antibacterial spectrum of lactoferricin B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin. J. Appl. Bacteriol. 1992, 73, 472-479.
38. Bechinger, B. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1999, 1462, 157-183.
39. Mani, R.; Cady, S.D.; Tang, M.; Waring, A.J.; Lehrer, R.I.; Hong, M. Membrane-dependent oligomeric structure and pore formation of a beta-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc. Natl. Acad. Sci. USA 2006, 103, 16242-16247.
40. Hwang, P.M.; Zhou, N.; Shan, X.; Arrowsmith, C.H.; Vogel, H.J. Three-dimensional solution structure of lactoferricin B, an antimicrobial peptide derived from bovine lactoferrin. Biochemistry 1998, 37, 4288-4298.
41. Hunter, H.N.; Demcoe, A.R.; Jenssen, H.; Gutteberg, T.J.; Vogel, H.J. Human lactoferricin is partially folded in aqueous solution and is better stabilized in a membrane mimetic solvent. Antimicrob. Agents Chemother. 2005, 49, 3387-3395.
42. Jing, W.; Svendsen, J.S.; Vogel, H.J. Comparison of NMR structures and model-membrane interactions of 15-residue antimicrobial peptides derived from bovine lactoferricin. Biochem. Cell Biol. 2006, 84, 312-326.
43. Strom, M.B.; Haug, B.E.; Rekdal, O.; Skar, M.L.; Stensen, W.; Svendsen, J.S. Important structural features of 15-residue lactoferricin derivatives and methods for improvement of antimicrobial activity. Biochem. Cell Biol. 2002, 80, 65-74.
44. Nguyen, L.T.; Haney, E.F.; Vogel, H.J. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 2011, 29, 464-472.
45. 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, 253-257.
46. Uyterhoeven, E.T.; Butler, C.H.; Ko, D.; Elmore, D.E. Investigating the nucleic acid interactions and antimicrobial mechanism of buforin II. FEBS Lett. 2008, 582, 1715-1718.
47. Otvos, L., Jr.; O, I.; Rogers, M.E.; Consolvo, P.J.; Condie, B.A.; Lovas, S.; Bulet, P.; Blaszczyk-Thurin, M. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 2000, 39, 14150-14159.
48. Rosenfeld, Y.; Papo, N.; Shai, Y. Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem. 2006, 281, 1636-1643.
49. Steinstraesser, L.; Koehler, T.; Jacobsen, F.; Daigeler, A.; Goertz, O.; Langer, S.; Kesting, M.; Steinau, H.; Eriksson, E.; Hirsch, T. Host defense peptides in wound healing. Mol. Med. 2008, 14, 528-537.
50. Mader, J.S.; Hoskin, D.W. Cationic antimicrobial peptides as novel cytotoxic agents for cancer treatment. Expet. Opin. Invest. Drugs 2006, 15, 933-946.
51. Quinn, K.; Henriques, M.; Parker, T.; Slutsky, A.S.; Zhang, H. Human neutrophil peptides: A novel potential mediator of inflammatory cardiovascular diseases. Am. J. Physiol. Heart C 2008, 295, 1817-1824.
52. Jenssen, H.; Hamill, P.; Hancock, R.E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 2006, 19, 491-511.
53. Peschel, A.; Sahl, H.G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 2006, 4, 529-536.
54. Nizet, V. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 2006, 8, 11-26.
55. Peschel, A.; Collins, L.V. Staphylococcal resistance to antimicrobial peptides of mammalian and bacterial origin. Peptides 2001, 22, 1651-1659.
56. Peschel, A. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 2002, 10, 179-186.
57. 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, 18692-18700.
58. 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, 157-168.
59. Jin, T.; Bokarewa, M.; Foster, T.; Mitchell, J.; Higgins, J.; Tarkowski, A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 2004, 172, 1169-1176.
60. Sperandio, B.; Regnault, B.; Guo, J.; Zhang, Z.; Stanley, S.L., Jr.; Sansonetti, P.J.; Pedron, T. Virulent Shigella flexneri subverts the host innate immune response through manipulation of antimicrobial peptide gene expression. J. Exp. Med. 2008, 205, 1121-1132.
61. Eilers, B.; Mayer-Scholl, A.; Walker, T.; Tang, C.; Weinrauch, Y.; Zychlinsky, A. Neutrophil antimicrobial proteins enhance Shigella flexneri adhesion and invasion. Cell. Microbiol. 2010, 12, 1134-1143.
62. Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D.S.; Weinrauch, Y.; Zychlinsky, A. Neutrophil extracellular traps kill bacteria. Science 2004, 303, 1532-1535.
63. Amulic, B.; Cazalet, C.; Hayes, G.L.; Metzler, K.D.; Zychlinsky, A. Neutrophil function: From mechanisms to disease. Annu. Rev. Immunol. 2012, 30, 459-489.
64. Malmsten, M.; Kasetty, G.; Pasupuleti, M.; Alenfall, J.; Schmidtchen, A. Highly selective end-tagged antimicrobial peptides derived from PRELP. PLoS One 2011, 6, e16400.
65. Maloy, W.L.; Kari, U.P. Structure-activity studies on magainins and other host defense peptides. Biopolymers 1995, 37, 105-122.
66. Strandberg, E.; Tiltak, D.; Ieronimo, M.; Kanithasen, N.; Wadhwani, P.; Ulrich, A.S. Influence of C-terminal amidation on the antimicrobial and hemolytic activities of cationic alpha-helical peptides. Pure Appl. Chem. 2007, 79, 717-728.
67. Dennison, S.R.; Phoenix, D.A. Influence of C-terminal amidation on the efficacy of modelin-5. Biochemistry 2011, 50, 1514-1523.
68. Hwang, H.; Hyun, S.; Kim, Y.; Yu, J. Reduction of helical content by insertion of a disulfide bond leads to an antimicrobial peptide with decreased hemolytic activity. Chem. Med. Chem. 2013, 8, 59-62.
69. McInnes, C.; Kondejewski, L.H.; Hodges, R.S.; Sykes, B.D. Development of the structural basis for antimicrobial and hemolytic activities of peptides based on gramicidin S and design of novel analogs using NMR spectroscopy. J. Biol. Chem. 2000, 275, 14287-14294.
70. Kondejewski, L.H.; Farmer, S.W.; Wishart, D.S.; Kay, C.M.; Hancock, R.E.; Hodges, R.S. Modulation of structure and antibacterial and hemolytic activity by ring size in cyclic gramicidin S analogs. J. Biol. Chem. 1996, 271, 25261-25268.
71. Jiang, Z.; Kullberg, B.J.; van der Lee, H.; Vasil, A.I.; Hale, J.D.; Mant, C.T.; Hancock, R.E.; Vasil, M.L.; Netea, M.G.; Hodges, R.S. Effects of hydrophobicity on the antifungal activity of alpha-helical antimicrobial peptides. Chem. Biol. Drug Des. 2008, 72, 483-495.
72. Kreil, G. D-Amino acids in animal peptides. Annu. Rev. Biochem. 1997, 66, 337-345.
73. Yin, L.M.; Lee, S.; Mak, J.S.; Helmy, A.S.; Deber, C.M. Differential binding of L-vs. D-isomers of cationic antimicrobial peptides to the biofilm exopolysaccharide alginate. Protein Pept. Lett. 2013, 20, 843-847.
74. Navon-Venezia, S.; Feder, R.; Gaidukov, L.; Carmeli, Y.; Mor, A. Antibacterial properties of dermaseptin S4 derivatives with in vivo activity. Antimicrob. Agents Chemother. 2002, 46, 689-694.
75. Stromstedt, A.A.; Pasupuleti, M.; Schmidtchen, A.; Malmsten, M. Evaluation of strategies for improving proteolytic resistance of antimicrobial peptides by using variants of EFK17, an internal segment of LL-37. Antimicrob. Agents Chemother. 2009, 53, 593-602.
76. Nguyen, L.T.; Chau, J.K.; Perry, N.A.; de Boer, L.; Zaat, S.A.; Vogel, H.J. Serum stabilities of short tryptophan-and arginine-rich antimicrobial peptide analogs. PLoS One 2010, 5, e12684.
77. Meng, H.; Kumar, K. Antimicrobial activity and protease stability of peptides containing fluorinated amino acids. J. Am. Chem. Soc. 2007, 129, 15615-15622.
78. Berhanu, W.M.; Ibrahim, M.A.; Pillai, G.G.; Oliferenko, A.A.; Khelashvili, L.; Jabeen, F.; Mirza, B.; Ansari, F.L.; Ul-Haq, I.; El-Feky, S.A.; et al. Similarity analysis, synthesis, and bioassay of antibacterial cyclic peptidomimetics. Beilstein. J. Org. Chem. 2012, 8, 1146-1160.
79. Tew, G.N.; Liu, D.; Chen, B.; Doerksen, R.J.; Kaplan, J.; Carroll, P.J.; Klein, M.L.; DeGrado, W.F. De novo design of biomimetic antimicrobial polymers. Proc. Natl. Acad. Sci. USA 2002, 99, 5110-5114.
80. Mensa, B.; Kim, Y.H.; Choi, S.; Scott, R.; Caputo, G.A.; DeGrado, W.F. Antibacterial mechanism of action of arylamide foldamers. Antimicrob. Agents Chemother. 2011, 55, 5043-5053.
81. Choi, S.; Isaacs, A.; Clements, D.; Liu, D.; Kim, H.; Scott, R.W.; Winkler, J.D.; DeGrado, W.F. De novo design and in vivo activity of conformationally restrained antimicrobial arylamide foldamers. Proc. Natl. Acad. Sci. USA 2009, 106, 6968-6973.
82. Tam, J.P.; Lu, Y.A.; Yang, J.L. Correlations of cationic charges with salt sensitivity and microbial specificity of cystine-stabilized beta-strand antimicrobial peptides. J. Biol. Chem. 2002, 277, 50450-50456.
83. Park, I.Y.; Cho, J.H.; Kim, K.S.; Kim, Y.B.; Kim, M.S.; Kim, S.C. Helix stability confers salt resistance upon helical antimicrobial peptides. J. Biol. Chem. 2004, 279, 13896-13901.
84. Yu, H.Y.; Tu, C.H.; Yip, B.S.; Chen, H.L.; Cheng, H.T.; Huang, K.C.; Lo, H.J.; Cheng, J.W. Easy strategy to increase salt resistance of antimicrobial peptides. Antimicrob. Agents Chemother. 2011, 55, 4918-4921.
85. Chu, H.L.; Yu, H.Y.; Yip, B.S.; Chih, Y.H.; Liang, C.W.; Cheng, H.T.; Cheng, J.W. Boosting salt resistance of short antimicrobial peptides. Antimicrob. Agents Chemother. 2013, doi:10.1128/AAC.00252-13.
86. Mishra, B.; Basu, A.; Saravanan, R.; Xiang, L.; Yang, L.K.; Leong, S.S.J. Lasioglossin-III: Antimicrobial characterization and feasibility study for immobilization applications. RSC Adv. 2013, 3, 9534-9543.
87. Li, Y. Recombinant production of antimicrobial peptides in Escherichia coli: A review. Protein Expr. Purif. 2011, 80, 260-267.
88. Bogomolovas, J.; Simon, B.; Sattler, M.; Stier, G. Screening of fusion partners for high yield expression and purification of bioactive viscotoxins. Protein Expr. Purif. 2009, 64, 16-23.
89. Butt, T.R.; Edavettal, S.C.; Hall, J.P.; Mattern, M.R. SUMO fusion technology for difficult-to-express proteins. Protein Expr. Purif. 2005, 43, 1-9.
90. Bommarius, B.; Jenssen, H.; Elliott, M.; Kindrachuk, J.; Pasupuleti, M.; Gieren, H.; Jaeger, K.E.; Hancock, R.E.; Kalman, D. Cost-effective expression and purification of antimicrobial and host defense peptides in Escherichia coli. Peptides 2010, 31, 1957-1965.
91. Vidovic, V.; Prongidi-Fix, L.; Bechinger, B.; Werten, S. Production and isotope labeling of antimicrobial peptides in Escherichia coli by means of a novel fusion partner that enables high-yield insoluble expression and fast purification. J. Pept. Sci. 2009, 15, 278-284.
92. Lee, J.H.; Kim, J.H.; Hwang, S.W.; Lee, W.J.; Yoon, H.K.; Lee, H.S.; Hong, S.S. High-level expression of antimicrobial peptide mediated by a fusion partner reinforcing formation of inclusion bodies. Biochem. Biophys. Res. Commun. 2000, 277, 575-580.
93. Kim, J.M.; Jang, S.A.; Yu, B.J.; Sung, B.H.; Cho, J.H.; Kim, S.C. High-level expression of an antimicrobial peptide histonin as a natural form by multimerization and furin-mediated cleavage. Appl. Microbiol. Biotechnol. 2008, 78, 123-130.
94. Lee, J.H.; Minn, I.; Park, C.B.; Kim, S.C. Acidic peptide-mediated expression of the antimicrobial peptide buforin II as tandem repeats in Escherichia coli. Protein Expr. Purif. 1998, 12, 53-60.
95. Kim, H.K.; Chun, D.S.; Kim, J.S.; Yun, C.H.; Lee, J.H.; Hong, S.K.; Kang, D.K. Expression of the cationic antimicrobial peptide lactoferricin fused with the anionic peptide in Escherichia coli. Appl. Microbiol. Biotechnol. 2006, 72, 330-338.
96. Agerberth, B.; Gudmundsson, G.H. Host antimicrobial defence peptides in human disease. Curr. Top. Microbiol. Immunol. 2006, 306, 67-90.
97. Gill, S.R.; Pop, M.; Deboy, R.T.; Eckburg, P.B.; Turnbaugh, P.J.; Samuel, B.S.; Gordon, J.I.; Relman, D.A.; Fraser-Liggett, C.M.; Nelson, K.E. Metagenomic analysis of the human distal gut microbiome. Science 2006, 312, 1355-1359.
98. Dewhirst, F.E.; Chen, T.; Izard, J.; Paster, B.J.; Tanner, A.C.; Yu, W.H.; Lakshmanan, A.; Wade, W.G. The human oral microbiome. J. Bacteriol. 2010, 192, 5002-5017.
99. Turnbaugh, P.J.; Ley, R.E.; Hamady, M.; Fraser-Liggett, C.M.; Knight, R.; Gordon, J.I. The human microbiome project. Nature 2007, 449, 804-810.
100. Goldman, M.J.; Anderson, G.M.; Stolzenberg, E.D.; Kari, U.P.; Zasloff, M.; Wilson, J.M. Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 1997, 88, 553-560.
101. Putsep, K.; Carlsson, G.; Boman, H.G.; Andersson, M. Deficiency of antibacterial peptides in patients with morbus Kostmann: An observation study. Lancet 2002, 360, 1144-1149.
102. Diamond, G.; Beckloff, N.; Ryan, L.K. Host defense peptides in the oral cavity and the lung: Similarities and differences. J. Dent. Res. 2008, 87, 915-927.
103. Mogayzel, P.J., Jr.; Naureckas, E.T.; Robinson, K.A.; Mueller, G.; Hadjiliadis, D.; Hoag, J.B.; Lubsch, L.; Hazle, L.; Sabadosa, K.; Marshall, B. Cystic fibrosis pulmonary guidelines. Chronic medications for maintenance of lung health. Am. J. Respir. Crit. Care Med. 2013, 187, 680-689.
104. Desgranges, S.; Le Prieult, F.; Daly, A.; Lydon, J.; Brennan, M.; Rai, D.K.; Subasinghage, A.P.; Hewage, C.M.; Cryan, S.A.; Greene, C.; et al. In vitro activities of synthetic host defense propeptides processed by neutrophil elastase against cystic fibrosis pathogens. Antimicrob. Agents Chemother. 2011, 55, 2487-2489.
105. Dale, B.A.; Fredericks, L.P. Antimicrobial peptides in the oral environment: Expression and function in health and disease. Curr. Issues Mol. Biol. 2005, 7, 119-133.
106. Gorr, S.-U. Antimicrobial peptides of the oral cavity. Periodontol. 2000 2009, 51, 152-180.
107. Ganz, T. Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 2003, 3, 710-720.
108. Cole, A.M.; Hong, T.; Boo, L.M.; Nguyen, T.; Zhao, C.; Bristol, G.; Zack, J.A.; Waring, A.J.; Yang, O.O.; Lehrer, R.I. Retrocyclin: A primate peptide that protects cells from infection by T-and M-tropic strains of HIV-1. Proc. Natl. Acad. Sci. USA 2002, 99, 1813-1818.
109. Tang, Y.Q.; Yuan, J.; Osapay, G.; Osapay, K.; Tran, D.; Miller, C.J.; Ouellette, A.J.; Selsted, M.E. A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 1999, 286, 498-502.
110. Ganz, T.; Selsted, M.E.; Szklarek, D.; Harwig, S.S.; Daher, K.; Bainton, D.F.; Lehrer, R.I. Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Invest. 1985, 76, 1427-1435.
111. Ganz, T.; Lehrer, R.I. Defensins. Pharmacol. Ther. 1995, 66, 191-205.
112. Rice, W.G.; Ganz, T.; Kinkade, J.M., Jr.; Selsted, M.E.; Lehrer, R.I.; Parmley, R.T. Defensin-rich dense granules of human neutrophils. Blood 1987, 70, 757-765.
113. Cowland, J.B.; Borregaard, N. The individual regulation of granule protein mRNA levels during neutrophil maturation explains the heterogeneity of neutrophil granules. J. Leukoc. Biol. 1999, 66, 989-995.
114. Yount, N.Y.; Wang, M.S.; Yuan, J.; Banaiee, N.; Ouellette, A.J.; Selsted, M.E. Rat neutrophil defensins. Precursor structures and expression during neutrophilic myelopoiesis. J. Immunol. 1995, 155, 4476-4484.
115. Faurschou, M.; Sorensen, O.E.; Johnsen, A.H.; Askaa, J.; Borregaard, N. Defensin-rich granules of human neutrophils: Characterization of secretory properties. Biochim. Biophys. Acta 2002, 1591, 29-35.
116. Ganz, T. Extracellular release of antimicrobial defensins by human polymorphonuclear leukocytes. Infect. Immun. 1987, 55, 568-571.
117. Ganz, T.; Oren, A.; Lehrer, R.I. Defensins: Microbicidal and cytotoxic peptides of mammalian host defense cells. Med. Microbiol. Immunol. 1992, 181, 99-105.
118. Faurschou, M.; Borregaard, N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 2003, 5, 1317-1327.
119. Sengelov, H.; Kjeldsen, L.; Borregaard, N. Control of exocytosis in early neutrophil activation. J. Immunol. 1993, 150, 1535-1543.
120. Joly, S.; Maze, C.; McCray, P.B., Jr.; Guthmiller, J.M. Human beta-defensins 2 and 3 demonstrate strain-selective activity against oral microorganisms. J. Clin. Microbiol. 2004, 42, 1024-1029.
121. Dale, B.A.; Kimball, J.R.; Krisanaprakornkit, S.; Roberts, F.; Robinovitch, M.; O'Neal, R.; Valore, E.V.; Ganz, T.; Anderson, G.M.; Weinberg, A. Localized antimicrobial peptide expression in human gingiva. J. Periodontal Res. 2001, 36, 285-294.
122. Sawaki, K.; Mizukawa, N.; Yamaai, T.; Fukunaga, J.; Sugahara, T. Immunohistochemical study on expression of alpha-defensin and beta-defensin-2 in human buccal epithelia with candidiasis. Oral Dis. 2002, 8, 37-41.
123. Chung, W.O.; Dale, B.A. Innate immune response of oral and foreskin keratinocytes: Utilization of different signaling pathways by various bacterial species. Infect. Immun. 2004, 72, 352-358.
124. Liu, L.; Roberts, A.A.; Ganz, T. By IL-1 signaling, monocyte-derived cells dramatically enhance the epidermal antimicrobial response to lipopolysaccharide. J. Immunol. 2003, 170, 575-580.
125. Garcia, J.R.; Krause, A.; Schulz, S.; Rodriguez-Jimenez, F.J.; Kluver, E.; Adermann, K.; Forssmann, U.; Frimpong-Boateng, A.; Bals, R.; Forssmann, W.G. Human beta-defensin 4: A novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J. 2001, 15, 1819-1821.
126. Sorensen, O.E.; Cowland, J.B.; Theilgaard-Monch, K.; Liu, L.; Ganz, T.; Borregaard, N. Wound healing and expression of antimicrobial peptides/polypeptides in human keratinocytes, a consequence of common growth factors. J. Immunol. 2003, 170, 5583-5589.
127. Arvola, T.; Laiho, K.; Torkkeli, S.; Mykkanen, H.; Salminen, S.; Maunula, L.; Isolauri, E. Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: A randomized study. Pediatrics 1999, 104, e64.
128. Doron, S.I.; Hibberd, P.L.; Gorbach, S.L. Probiotics for prevention of antibiotic-associated diarrhea. J. Clin. Gastroenterol. 2008, 42, 58-63.
129. Danna, P.L.; Urban, C.; Bellin, E.; Rahal, J.J. Role of Candida in pathogenesis of antibiotic-associated diarrhoea in elderly inpatients. Lancet 1991, 337, 511-514.
130. Giannella, R.A. Antibiotic-associated diarrhea and Clostridium difficile colitis: An update. Rev. Esp. Enferm. Dig. 2001, 93, 535-543.
131. Glukhov, E.; Stark, M.; Burrows, L.L.; Deber, C.M. Basis for selectivity of cationic antimicrobial peptides for bacterial versus mammalian membranes. J. Biol. Chem. 2005, 280, 33960-33967.
132. Umeyama, M.; Kira, A.; Nishimura, K.; Naito, A. Interactions of bovine lactoferricin with acidic phospholipid bilayers and its antimicrobial activity as studied by solid-state NMR. Biochim. Biophys. Acta 2006, 1758, 1523-1528.
133. Katsu, T.; Kuroko, M.; Morikawa, T.; Sanchika, K.; Fujita, Y.; Yamamura, H.; Uda, M. Mechanism of membrane damage induced by the amphipathic peptides gramicidin S and melittin. Biochim. Biophys. Acta 1989, 983, 135-141.
134. Steiner, H.; Hultmark, D.; Engstrom, A.; Bennich, H.; Boman, H.G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 1981, 292, 246-248.
135. Chou, H.T.; Kuo, T.Y.; Chiang, J.C.; Pei, M.J.; Yang, W.T.; Yu, H.C.; Lin, S.B.; Chen, W.J. Design and synthesis of cationic antimicrobial peptides with improved activity and selectivity against Vibrio spp. Int. J. Antimicrob. Agents 2008, 32, 130-138.
136. Juretic, D.; Vukicevic, D.; Petrov, D.; Novkovic, M.; Bojovic, V.; Lucic, B.; Ilic, N.; Tossi, A. Knowledge-based computational methods for identifying or designing novel, non-homologous antimicrobial peptides. Eur. Biophys. J. 2011, 40, 371-385.
137. Juretic, D.; Vukicevic, D.; Ilic, N.; Antcheva, N.; Tossi, A. Computational design of highly selective antimicrobial peptides. J. Chem. Inf. Model. 2009, 49, 2873-2882.
138. Mishra, B.; Wang, G. Ab initio design of potent anti-MRSA peptides based on database filtering technology. J. Am. Chem. Soc. 2012, 134, 12426-12429.
139. Gaynes, R.; Edwards, J.R. Overview of nosocomial infections caused by gram-negative bacilli. Clin. Infect. Dis. 2005, 41, 848-854.
140. Peleg, A.Y.; Hooper, D.C. Hospital-acquired infections due to gram-negative bacteria. N. Engl. J. Med. 2010, 362, 1804-1813.
141. Su, Y.; Waring, A.J.; Ruchala, P.; Hong, M. Structures of beta-hairpin antimicrobial protegrin peptides in lipopolysaccharide membranes: Mechanism of gram selectivity obtained from solid-state nuclear magnetic resonance. Biochemistry 2011, 50, 2072-2083.
142. Muhle, S.A.; Tam, J.P. Design of Gram-negative selective antimicrobial peptides. Biochemistry 2001, 40, 5777-5785.
143. Scott, M.G.; Rosenberger, C.M.; Gold, M.R.; Finlay, B.B.; Hancock, R.E. An alpha-helical cationic antimicrobial peptide selectively modulates macrophage responses to lipopolysaccharide and directly alters macrophage gene expression. J. Immunol. 2000, 165, 3358-3365.
144. Casteels, P.; Ampe, C.; Jacobs, F.; Vaeck, M.; Tempst, P. Apidaecins: Antibacterial peptides from honeybees. EMBO J. 1989, 8, 2387-2391.
145. Bulet, P.; Dimarcq, J.L.; Hetru, C.; Lagueux, M.; Charlet, M.; Hegy, G.; van Dorsselaer, A.; Hoffmann, J.A. A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J. Biol. Chem. 1993, 268, 14893-14897.
146. Knappe, D.; Piantavigna, S.; Hansen, A.; Mechler, A.; Binas, A.; Nolte, O.; Martin, L.L.; Hoffmann, R. Oncocin (VDKPPYLPRPRPPRRIYNR-NH2): A novel antibacterial peptide optimized against gram-negative human pathogens. J. Med. Chem. 2010, 53, 5240-5247.
147. Shamova, O.; Brogden, K.A.; Zhao, C.; Nguyen, T.; Kokryakov, V.N.; Lehrer, R.I. Purification and properties of proline-rich antimicrobial peptides from sheep and goat leukocytes. Infect. Immun. 1999, 67, 4106-4111.
148. He, J.; Yarbrough, D.K.; Kreth, J.; Anderson, M.H.; Shi, W.; Eckert, R. Systematic approach to optimizing specifically targeted antimicrobial peptides against Streptococcus mutans. Antimicrob. Agents Chemother. 2010, 54, 2143-2151.
149. Eckert, R.; Qi, F.; Yarbrough, D.K.; He, J.; Anderson, M.H.; Shi, W. Adding selectivity to antimicrobial peptides: Rational design of a multidomain peptide against Pseudomonas spp. Antimicrob. Agents Chemother. 2006, 50, 1480-1488.
150. Banas, J.A. Virulence properties of Streptococcus mutans. Front. Biosci. 2004, 9, 1267-1277.
151. Loesche, W.J. Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 1986, 50, 353-380.
152. Eckert, R.; He, J.; Yarbrough, D.K.; Qi, F.; Anderson, M.H.; Shi, W. Targeted killing of Streptococcus mutans by a pheromone-guided "smart" antimicrobial peptide. Antimicrob. Agents Chemother. 2006, 50, 3651-3657.
153. Li, L.N.; Guo, L.H.; Lux, R.; Eckert, R.; Yarbrough, D.; He, J.; Anderson, M.; Shi, W.Y. Targeted antimicrobial therapy against Streptococcus mutans establishes protective non-cariogenic oral biofilms and reduces subsequent infection. Int. J. Oral Sci. 2010, 2, 66-73.
154. Svensater, G.; Sjogreen, B.; Hamilton, I.R. Multiple stress responses in Streptococcus mutans and the induction of general and stress-specific proteins. Microbiology 2000, 146, 107-117.
155. Lee, I.H.; Zhao, C.; Cho, Y.; Harwig, S.S.; Cooper, E.L.; Lehrer, R.I. Clavanins, alpha-helical antimicrobial peptides from tunicate hemocytes. FEBS Lett. 1997, 400, 158-162.
156. Li, L.; He, J.; Eckert, R.; Yarbrough, D.; Lux, R.; Anderson, M.; Shi, W. Design and characterization of an acid-activated antimicrobial peptide. Chem. Biol. Drug Des. 2009, 75, 127-132.
157. Tsuboi, R.; Matsuda, K.; Ko, I.J.; Ogawa, H. Correlation between culture medium pH, extracellular proteinase activity, and cell growth of Candida albicans in insoluble stratum corneum-supplemented media. Arch. Dermatol. Res. 1989, 281, 342-345.
158. Wegscheid-Gerlach, C.; Gerber, H.D.; Diederich, W.E. Proteases of Plasmodium falciparum as potential drug targets and inhibitors thereof. Curr. Top. Med. Chem. 2010, 10, 346-367.
159. Aoki, W.; Kitahara, N.; Miura, N.; Morisaka, H.; Yamamoto, Y.; Kuroda, K.; Ueda, M. Candida albicans possesses Sap7 as a pepstatin A-insensitive secreted aspartic protease. PLoS One 2012, 7, e32513.
160. Aoki, W.; Kitahara, N.; Miura, N.; Morisaka, H.; Yamamoto, Y.; Kuroda, K.; Ueda, M. Comprehensive characterization of secreted aspartic proteases encoded by a virulence gene family in Candida albicans. J. Biochem. 2011, 150, 431-438.
161. Aoki, W.; Kitahara, N.; Miura, N.; Morisaka, H.; Kuroda, K.; Ueda, M. Design of a novel antimicrobial peptide activated by virulent proteases. Chem. Biol. Drug Des. 2012, 80, 725-733.
162. Aoki, W.; Kitahara, N.; Miura, N.; Morisaka, H.; Kuroda, K.; Ueda, M. Profiling of adhesive properties of the agglutinin-like sequence (ALS) protein family, a virulent attribute ofCandida albicans. FEMS Immunol. Med. Microbiol. 2012, 65, 121-124.
163. Aoki, W.; Ueda, T.; Tatsukami, Y.; Kitahara, N.; Morisaka, H.; Kuroda, K.; Ueda, M. Time-course proteomic profile of Candida albicans during adaptation to a fetal serum. Pathog. Dis. 2013, 67, 67-75.
164. Aoki, W.; Tatsukami, Y.; Kitahara, N.; Matsui, K.; Morisaka, H.; Kuroda, K.; Ueda, M. Elucidation of potentially virulent factors of Candida albicans during serum adaptation by using quantitative time-course proteomics. J. Proteomics 2013, in press.
165. Aoki, W.; Ueda, M. New developments in the pathogenesis of Candida albicans: Characterization of secreted aspartic proteases and profiling of survival mechanism in blood. Candida albicans: Symptoms, Causes and Treatment Options; Nova Science Publishers: New York, NY, USA, 2013, in press.
166. Gottler, L.M.; Ramamoorthy, A. Structure, membrane orientation, mechanism, and function of pexiganan-A highly potent antimicrobial peptide designed from magainin. Biochim. Biophys. Acta 2009, 1788, 1680-1686.
167. Bulmus, V.; Ding, Z.; Long, C.J.; Stayton, P.S.; Hoffman, A.S. Site-specific polymer-streptavidin bioconjugate for pH-controlled binding and triggered release of biotin. Bioconjug. Chem. 2000, 11, 78-83.
168. Kim, J.J.; Park, K. Modulated insulin delivery from glucose-sensitive hydrogel dosage forms. J. Control. Release 2001, 77, 39-47.
169. Fogueri, L.R.; Singh, S. Smart polymers for controlled delivery of proteins and peptides: A review of patents. Recent Pat. Drug Deliv. Formul. 2009, 3, 40-48.