BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Antimicrobial Peptides (AMPs): Peptide Structure and Mode of Action

  • Park, Yoon-Kyung (Research Center for Proteineous Materials, Chosun University) ;
  • Hahm, Kyung-Soo (Research Center for Proteineous Materials, Chosun University)
  • Published : 2005.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Antimicrobial peptides (AMPs) have been isolated and characterized from tissues and organisms representing virtually every kingdom and phylum. Their amino acid composition, amphipathicity, cationic charge, and size allow them to attach to and insert into membrane bilayers to form pores by 'barrel-stave', 'carpet' or 'toroidal-pore' mechanisms. Although these models are helpful for defining mechanisms of AMP activity, their relevance to resolving how peptides damage and kill microorganisms still needs to be clarified. Moreover, many AMPs employ sophisticated and dynamic mechanisms of action to carry out their likely roles in antimicrobial host defense. Recently, it has been speculated that transmembrane pore formation is not the only mechanism of microbial killing by AMPs. In fact, several observations suggest that translocated AMPs can alter cytoplasmic membrane septum formation, reduce cell-wall, nucleic acid, and protein synthesis, and inhibit enzymatic activity. In this review, we present the structures of several AMPs as well as models of how AMPs induce pore formation. AMPs have received special attention as a possible alternative way to combat antibiotic-resistant bacterial strains. It may be possible to design synthetic AMPs with enhanced activity for microbial cells, especially those with antibiotic resistance, as well as synergistic effects with conventional antibiotic agents that lack cytotoxic or hemolytic activity.

Keywords

References

  1. Baker, M. A., Maloy, W. L., Zasloff, M. and Jacob, L. S. (1993) Anticancer efficacy of magainin 2 and analogue peptides. Cancer Res. 53, 3052-3057
  2. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solidstate NMR spectroscopy. Biochim. Biophys. Acta 1462, 157-183 https://doi.org/10.1016/S0005-2736(99)00205-9
  3. Bessalle, R., Kapitkovsky, A., Gorea, A., Shalit, I. and Fridkin, M. (1990) All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett 274, 151-155 https://doi.org/10.1016/0014-5793(90)81351-N
  4. Boman, H. G. (1995) Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13, 61-92 https://doi.org/10.1146/annurev.iy.13.040195.000425
  5. Brogden, K. A., Ackermann, M. and Huttner, K. M. (1997) Small, anionic, and charge-neutralizing propeptide fragments of zymogens are antimicrobial. Antimicrob. Agents Chem. 41, 1615-1617
  6. Brogden, K. A., Ackermann, M. and Huttner, K. M. (1998) Detection of anionic antimicrobial peptides in ovine bronchoalveolar lavage fluid and respiratory epithelium. Infect. Immun. 66, 5948-5954
  7. Brotz, H., Bierbaum, G., Leopold, K., Reynolds, P. E. and Sahl, H. G. (1998) The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents Chemother. 42, 154-160
  8. Cantor, R. S. (2002) Size distribution of barrel-stave aggregates of membrane peptides: influence of the bilayer lateral pressure profile. Biophys. J. 82, 2520-2525 https://doi.org/10.1016/S0006-3495(02)75595-1
  9. Dathe, M., Nikolenko, H., Meyer, J., Beyermann, M. and Bienert, M. (2001) Optimization of the antimicrobial activity of magainin peptides by modification of charge. FEBS Lett. 501, 146-150 https://doi.org/10.1016/S0014-5793(01)02648-5
  10. Falla, T. J., Karunaratne, D. N. and Hancock, R. E. W. (1996) Mode of action of the antimicrobial peptide indolicidin. J. Biol. Chem. 271, 19298-19303 https://doi.org/10.1074/jbc.271.32.19298
  11. Fehlbaum, P., Bulet, P., Chernysh, S., Briand, J. P., Roussel, J. P., Letellier, L., Hetru, C. and Hoffmann, J. A. (1996) Structure– activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc. Natl. Acad. Sci. USA 93, 1221-1225
  12. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K. and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membranepermeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276, 5836-5840 https://doi.org/10.1074/jbc.M007540200
  13. Friedrich, C. L., Moyles, D., Beveridge, T. J. and Hancock, R. E. W. (2000) Antibacterial action of structurally diverse cationic peptides on Gram-positive bacteria. Antimicrob. Agents Chemother. 44, 2086-2092 https://doi.org/10.1128/AAC.44.8.2086-2092.2000
  14. Friedrich, C. L., Rozek, A., Patrzykat, A. and Hancock, R. E. W. (2001) Structure and mechanism of action of an indolicidin peptide derivative with improved activity against Gram-positive bacteria. J. Biol. Chem. 276, 24015-24022 https://doi.org/10.1074/jbc.M009691200
  15. Gallo, R. L., Ono, M., Povsic, T., Page, C., Eriksson, E., Klagsbrun, M. and Bernfield, M. (1994) Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc. Natl. Acad. Sci. USA 91, 11035- 11039
  16. Ganz, T. and Lehrer, R. I. (1998) Antimicrobial peptides of vertebrates. Curr. Opin. Immunol. 10, 41-44 https://doi.org/10.1016/S0952-7915(98)80029-0
  17. Gennaro, R. and Zanetti, M. (2000) Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers 55, 31-49 https://doi.org/10.1002/1097-0282(2000)55:1<31::AID-BIP40>3.0.CO;2-9
  18. Gesell, J., Zasloff, M. and Opella, S. J. (1997) Two-dimensional 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an alpha-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J. Biomol. NMR 9, 127-135 https://doi.org/10.1023/A:1018698002314
  19. Giacometti, A., Cirioni, O., Barchiesi, F., Del Prete, M. S. and Scalise, G.. (1999) Antimicrobial activity of polycationic peptides. Peptides 20, 1265-1273 https://doi.org/10.1016/S0196-9781(99)00131-X
  20. Gibson, B. W., Tang, D. Z., Mandrell, R., Kelly, M. and Spindel, E. R. (1991) Bombinin-like peptides with antimicrobial activity from skin secretions of the Asian toad, Bombina orientalis. J. Biol. Chem. 266, 23103-23111
  21. Hancock, R. E. W. and Lehrer, R. (1998) Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16, 82-88 https://doi.org/10.1016/S0167-7799(97)01156-6
  22. Hirakura, Y., Kobayashi, S. and Matsuzaki, K. (2002) Specific interactions of the antimicrobial peptide cyclic beta-sheet tachyplesin I with lipopolysaccharides. Biochim. Biophys. Acta 1562, 32-36 https://doi.org/10.1016/S0005-2736(02)00358-9
  23. Jakob, S., Robert, B. S. and Alister W. D. (2005) Evolution of innate immune systems. Biochem. Mol. Biol. Edu. 33, 177-183 https://doi.org/10.1002/bmb.2005.494033032466
  24. Johansson, J., Gudmundsson, G. H., Rottenberg, M. E., Berndt, K. D. and Agerberth, B. (1998) Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem. 273, 3718-3724 https://doi.org/10.1074/jbc.273.6.3718
  25. Juretic, D., Chen, H. C., Brown, J. H., Morell, J. L., Hendler, R. W. and Westerhoff, H. V. (1989) Magainin 2 amide and analogues. Antimicrobial activity, membrane depolarization and susceptibility to proteolysis. FEBS Lett. 249, 219-223 https://doi.org/10.1016/0014-5793(89)80627-1
  26. Kawano, K., Yoneya, T., Miyata, T., Yoshikawa, K., Tokunaga, F., Terada, Y. and Iwanaga, S. (1990) Antimicrobial peptide, tachyplesin I, isolated from hemocytes of the horseshoe crab (Tachypleus tridentatus). NMR determination of the beta-sheet structure. J. Biol. Chem. 265, 15365-15367
  27. Kobayashi, S., Chikushi, A., Tougu, S., Imura, Y., Nishida, M., Yano, Y. and Matsuzaki, K. (2004) Membrane translocation mechanism of the antimicrobial peptide buforin 2. Biochemistry 43, 15610-15616 https://doi.org/10.1021/bi048206q
  28. Kragol, G., Lovas, S., Varadi, G., Condie, B. A., Hoffmann, R. and Otvos, Jr. L. (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperoneassisted protein folding. Biochemistry 40, 3016-3026 https://doi.org/10.1021/bi002656a
  29. Laederach, A., Andreotti, A. H. and Fulton, D. B. (2002) Solution and micelle-bound structures of tachyplesin I and its active aromatic linear derivatives. Biochemistry 41, 12359-12368 https://doi.org/10.1021/bi026185z
  30. Lee, D. G., Park, Y., Jin, I., Hahmn, K. S., Lee, H. H., Moon, Y. H., Woo, E. R. (2004) Structure-antiviral activity relationships of cecropin A-maganin 2 hybrid peptide and its analogues. J. Pept. Sci. 10, 298-303 https://doi.org/10.1002/psc.504
  31. Lee, M. T., Chen, F. Y. and Huang, H. W. (2004) Energetics of pore formation induced by membrane active peptides. Biochemistry 43, 3590-3599 https://doi.org/10.1021/bi036153r
  32. Lehrer, R. I., Lichtenstein, A. K. and Ganz, T. (1993) Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu. Rev. Immunol. 11, 105-128 https://doi.org/10.1146/annurev.iy.11.040193.000541
  33. Mandard, N., Sodano, P., Labbe, H., Bonmatin, J. M., Bulet, P., Hetru, C., Ptak, M. and Vovelle, F. (1998) Solution structure of thanatin, a potent bactericidal and fungicidal insect peptide, determined from proton two-dimensional nuclear magnetic resonance data. Eur. J. Biochem. 256, 404-410 https://doi.org/10.1046/j.1432-1327.1998.2560404.x
  34. Matsuzaki, K. (1998) Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1376, 391-400 https://doi.org/10.1016/S0304-4157(98)00014-8
  35. Matsuzaki, K., Murase, O., Fujii, N. and Miyajima, K. (1996) An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35, 11361-11368 https://doi.org/10.1021/bi960016v
  36. Matsuzaki, K., Nakayama, M., Fukui, M., Otaka, A., Funakoshi, S., Fujii, N., Bessho, K. and Miyajima, K. (1993) Role of disulfide linkages in tachyplesin–lipid interactions. Biochemistry 32, 11704-11710 https://doi.org/10.1021/bi00094a029
  37. Matsuzaki, K., Sugishita, K., Harada, M., Fujii, N. and Miyajima, K. (1997) Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of Gram-negative bacteria. Biochim. Biophys. Acta 1327, 119-130 https://doi.org/10.1016/S0005-2736(97)00051-5
  38. Matsuzaki, K., Yoneyama, S., Fujii, N., Miyajima, K., Yamada, K., Kirino, Y. and Anzai, K. (1997) Membrane permeabilization mechanisms of a cyclic antimicrobial peptide, tachyplesin I, and its linear analog. Biochemistry 36, 9799-9806 https://doi.org/10.1021/bi970588v
  39. Murakami, T., Niwa, M., Tokunaga, F., Miyata, T. and Iwanaga, S. (1991) Direct virus inactivation of tachyplesin I and its isopeptides from horseshoe crab hemocytes. Chemotherapy 37, 327-334 https://doi.org/10.1159/000238875
  40. Nakamura, T., Furunaka, H., Miyata, T., Tokunaga, F., Muta, T., Iwanaga, S., Niwa, M., Takao, T. and Shimonishi, Y. (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. J. Biol. Chem. 263, 16709-16713
  41. Oren, Z. and Shai, Y. (1998) Mode of action of linear amphipathic $\alpha$-helical antimicrobial peptides. Biopolymers 47, 451-463 https://doi.org/10.1002/(SICI)1097-0282(1998)47:6<451::AID-BIP4>3.0.CO;2-F
  42. Otvos, L. Jr. (2000) Antibacterial peptides isolated from insects. J. Pept. Sci. 6, 497-511 https://doi.org/10.1002/1099-1387(200010)6:10<497::AID-PSC277>3.0.CO;2-W
  43. Otvos, L. Jr. (2002) The short proline-rich antibacterial peptide family. Cell Mol. Life Sci. 59, 1138-1150 https://doi.org/10.1007/s00018-002-8493-8
  44. Park, C. B., Yi, K. S., Matsuzaki, K., Kim, M. S. and Kim, S. C. (2000) Structure-activity analysis of buforin II, a histone H2Aderived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl Acad. Sci. USA 97, 8245-8250
  45. Park, Y., Choi, B. H., Kwak, J. S., Kang, C. W., Lim, H. T., Cheong, H. S. and Hahn, K. S. (2005) Kunitz-type serine protease inhibitor from potato (Solanum tuberosum L cv. jopung). J. Agricul. Food Chem. 53, 6491-6496 https://doi.org/10.1021/jf0505123
  46. Patrzykat, A., Friedrich, C. L., Zhang, L., Mendoza, V. and Hancock, R. E. W. (2002) Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob. Agents Chemother. 46, 605-614 https://doi.org/10.1128/AAC.46.3.605-614.2002
  47. Pouny, Y., Rapaport, D., Mor, A., Nicolas, P. and Shai, Y. (1992) Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31, 12416-12423 https://doi.org/10.1021/bi00164a017
  48. Rao, A. G. (1999) Conformation and antimicrobial activity of linear derivatives of tachyplesin lacking disulfide bonds. Arch. Biochem. Biophys. 361, 127-134 https://doi.org/10.1006/abbi.1998.0962
  49. Rozek, A., Friedrich, C. L. and Hancock, R. E. W. (2000) Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 39, 15765-15774 https://doi.org/10.1021/bi000714m
  50. Schutte, B. C. and McCray, P. B. Jr. (2002) â-defensins in lung host defense. Annu. Rev. Physiol. 64, 709-748 https://doi.org/10.1146/annurev.physiol.64.081501.134340
  51. Selsted, M. E., Novotny, M. J., Morris, W. L., Tang, Y. Q., Smith, W. and Cullorm J. S. (1992) Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267, 4292-4295
  52. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alphahelical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55-70 https://doi.org/10.1016/S0005-2736(99)00200-X
  53. Simmaco, M., Mignogna, G. and Barra, D. (1998) Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47, 435-450 https://doi.org/10.1002/(SICI)1097-0282(1998)47:6<435::AID-BIP3>3.0.CO;2-8
  54. Spaar, A., Munster, C. and Salditt, T. (2004) Conformation of peptides in lipid membranes studied by X-ray grazing incidence scattering. Biophys. J. 87, 396-407 https://doi.org/10.1529/biophysj.104.040667
  55. Subbalakshmi, C. and Sitaram, N. (1998) Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett. 160, 91-96 https://doi.org/10.1111/j.1574-6968.1998.tb12896.x
  56. Tamamura, H., Ikoma, R., Niwa, M., Funakoshi, S., Murakami, T. and Fujii, N. (1993) Antimicrobial activity and conformation of tachyplesin I and its analogs. Chem. Pharm. Bull. (Tokyo) 41, 978-980 https://doi.org/10.1248/cpb.41.978
  57. Tang, Y. Q., Yuan, J., Osapay, G., Osapay, K., Tran, D., Miller, C. J., Ouellette, A. J. and Selsted, M. E. (1999) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated a-defensins. Science 286, 498-502 https://doi.org/10.1126/science.286.5439.498
  58. Vizioli, J. and Salzet, M. (2002) Antimicrobial peptides from animals: focus on invertebrates. Trends Pharmacol. Sci. 23, 494-496 https://doi.org/10.1016/S0165-6147(02)02105-3
  59. von Horsten, H. H., Schafer, B. and Kirchhoff, C. (2004) SPAG11/ isoform HE2C, an atypical anionic $\beta$-defensin-like peptide. Peptides 25, 1223-1233 https://doi.org/10.1016/j.peptides.2004.05.016
  60. Wu, M., Maier, E., Benz, R. and Hancock, R. E. W. (1999) Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38, 7235-7242 https://doi.org/10.1021/bi9826299
  61. Yamaguchi, S., Huster, D., Waring, A., Lehrer, R. I., Kearney, W., Tack, B. F. and Hong, M. (2001) Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR spectroscopy. Biophys. J. 81, 2203-2214 https://doi.org/10.1016/S0006-3495(01)75868-7
  62. Yamaguchi, S., Hong, T., Waring, A., Lehrer, R. I. and Hong, M. (2002) Solid-state NMR investigations of peptide-lipid interaction and orientation of a a-sheet antimicrobial peptide, protegrin. Biochemistry 41, 9852-9862 https://doi.org/10.1021/bi0257991
  63. Yang, L., Harroun, T. A., Weiss, T. M., Ding, L. and Huang, H. W. (2001) Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81, 1475-1485 https://doi.org/10.1016/S0006-3495(01)75802-X
  64. Yonezawa, A., Kuwahara, J., Fujii, N. and Sugiura, Y. (1992) Binding of tachyplesin I to DNA revealed by footprinting analysis: significant contribution of secondary structure to DNA binding and implication for biological action. Biochemistry 31, 2998-3004 https://doi.org/10.1021/bi00126a022
  65. Zasloff, M. (1987) 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 84, 5449-5453
  66. Zasloff, M. (2002) AMPs of multicellular organisms. Nature (London) 415, 389-395 https://doi.org/10.1038/415389a
  67. Zasloff, M., Martin, B. and Chen, H. C. (1988) Antimicrobial activity of synthetic magainin peptides and several analogues. Proc. Natl. Acad. Sci. USA 85, 910-913
  68. Zhang, L., Benz, R. and Hancock, R. E. W. (1999) Influence of proline residues on the antibacterial and synergistic activities of alpha-helical peptides. Biochemistry 38, 8102-8111 https://doi.org/10.1021/bi9904104
  69. Zhang, L., Rozek, A. and Hancock, R. E. W. (2001) Interaction of cationic antimicrobial peptides with model membranes. J. Biol. Chem. 276, 35714-35722 https://doi.org/10.1074/jbc.M104925200

Cited by

  1. Balteatide: A Novel Antimicrobial Decapeptide from the Skin Secretion of the Purple-Sided Leaf Frog,Phyllomedusa baltea vol.2014, 2014, https://doi.org/10.1155/2014/176214
  2. Recent progresses of simulations on passive membrane permeations in China vol.42, pp.10, 2016, https://doi.org/10.1080/08927022.2015.1135333
  3. Hylaranins: prototypes of a new class of amphibian antimicrobial peptide from the skin secretion of the oriental broad-folded frog, Hylarana latouchii vol.46, pp.4, 2014, https://doi.org/10.1007/s00726-013-1655-1
  4. Feleucins: Novel Bombinin Precursor-Encoded Nonapeptide Amides from the Skin Secretion ofBombina variegata vol.2014, 2014, https://doi.org/10.1155/2014/671362
  5. Use of refined potato (Solanum tuberosum L. cv. Gogu valley) protein as an alternative to antibiotics in weanling pigs vol.124, pp.1-3, 2009, https://doi.org/10.1016/j.livsci.2008.12.003
  6. QSAR analysis of antimicrobial and haemolytic effects of cyclic cationic antimicrobial peptides derived from protegrin-1 vol.14, pp.17, 2006, https://doi.org/10.1016/j.bmc.2006.05.005
  7. Phylloseptin-PBa—A Novel Broad-Spectrum Antimicrobial Peptide from the Skin Secretion of the Peruvian Purple-Sided Leaf Frog (Phyllomedusa Baltea) Which Exhibits Cancer Cell Cytotoxicity vol.7, pp.12, 2015, https://doi.org/10.3390/toxins7124878
  8. Feleucin-BO1: A Novel Antimicrobial Non-Apeptide Amide from the Skin Secretion of the Toad,Bombina orientalis,and Design of a Potent Broad-Spectrum Synthetic Analogue, Feleucin-K3 vol.85, pp.3, 2015, https://doi.org/10.1111/cbdd.12396
  9. Treatment of microbial biofilms in the post-antibiotic era: prophylactic and therapeutic use of antimicrobial peptides and their design by bioinformatics tools vol.70, pp.3, 2014, https://doi.org/10.1111/2049-632X.12151
  10. Insights from Micro-second Atomistic Simulations of Melittin in Thin Lipid Bilayers vol.248, pp.3, 2015, https://doi.org/10.1007/s00232-015-9807-8
  11. Peptides as the next generation of anti-infectives vol.5, pp.3, 2013, https://doi.org/10.4155/fmc.12.213
  12. Display of adenoregulin with a novel Pichia pastoris cell surface display system vol.35, pp.2, 2007, https://doi.org/10.1007/BF02686102
  13. Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus vol.120, pp.2, 2007, https://doi.org/10.1111/j.1365-2567.2006.02493.x
  14. Effects of Surface Charges on the Bactericide Activity of CdTe/ZnS Quantum Dots: A Cell Membrane Disruption Perspective vol.33, pp.9, 2017, https://doi.org/10.1021/acs.langmuir.7b00173
  15. Identification of antimicrobial peptides from teleosts and anurans in expressed sequence tag databases using conserved signal sequences vol.279, pp.5, 2012, https://doi.org/10.1111/j.1742-4658.2011.08463.x
  16. Pore-forming bacterial toxins and antimicrobial peptides as modulators of ADAM function vol.201, pp.4, 2012, https://doi.org/10.1007/s00430-012-0260-3
  17. Characterization of the branched antimicrobial peptide M6 by analyzing its mechanism of action andin vivo toxicity vol.13, pp.6, 2007, https://doi.org/10.1002/psc.858
  18. Metallopeptides - from Drug Discovery to Catalysis vol.57, pp.3A, 2010, https://doi.org/10.1002/jccs.201000043
  19. Evaluation of 99mTc-UBI 29-41 scintigraphy for specific detection of experimental Staphylococcus aureus prosthetic joint infections vol.34, pp.8, 2007, https://doi.org/10.1007/s00259-007-0368-7
  20. Insect proteins as a potential source of antimicrobial peptides in livestock production. A review vol.26, pp.2, 2017, https://doi.org/10.22358/jafs/69998/2017
  21. Phylloseptin-1 (PSN-1) from Phyllomedusa sauvagei skin secretion: A novel broad-spectrum antimicrobial peptide with antibiofilm activity vol.47, pp.11-12, 2010, https://doi.org/10.1016/j.molimm.2010.04.010
  22. Alanine scanning analysis and structure-function relationships of the frog-skin antimicrobial peptide temporin-1Ta vol.17, pp.5, 2011, https://doi.org/10.1002/psc.1350
  23. Antimicrobial properties of a lipid interactive α-helical peptide VP1 against Staphylococcus aureus bacteria vol.129, pp.2-3, 2007, https://doi.org/10.1016/j.bpc.2007.06.007
  24. Effects of synbiotic fermentation products on primary chemoprevention in human colon cells vol.23, pp.7, 2012, https://doi.org/10.1016/j.jnutbio.2011.03.022
  25. Improving the Selectivity of Antimicrobial Peptides from Anuran Skin vol.52, pp.12, 2012, https://doi.org/10.1021/ci300328y