Intracellular targeting mechanisms by antimicrobial peptides

Antimicrobial Agents and Chemotherapy

Volumn 61, Issue 4, 2017, Pages

  Le, Cheng Foh ^a   Fang, Chee Mun ^a   Sekaran, Shamala Devi ^b  

^a UNIVERSITY OF NOTTINGHAM MALAYSIA CAMPUS   (Malaysia)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Antibiotic resistance; Antimicrobial peptides; Intracellular targeting; Membrane lysis; Novel antibiotics

Indexed keywords

LIPOPOLYSACCHARIDE; POLYPEPTIDE ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE;

ANTIBACTERIAL ACTIVITY; BACTERIAL CELL WALL; BACTERIAL MEMBRANE; CELL DEATH; CELL DIVISION; CYTOPLASM; DRUG MECHANISM; NONHUMAN; NUCLEIC ACID SYNTHESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SYNTHESIS; SHORT SURVEY; CELL MEMBRANE; CELL WALL; DRUG EFFECTS; METABOLISM; MICROBIAL SENSITIVITY TEST;

ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CELL WALL; MICROBIAL SENSITIVITY TESTS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING;

EID: 85016761318     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02340-16     Document Type: Short Survey

References (179)

1. Brogden KA. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238-250. https://doi.org/10.1038/nrmicro1098.
2. Hancock REW, Chapple DS. 1999. Peptide antibiotics. Antimicrob Agents Chemother 43:1317-1323.
3. Nicolas P, Mor A. 1995. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu Rev Microbiol 49:277-304. https://doi.org/10.1146/annurev.mi.49.100195.001425.
4. Oren Z, Shai Y. 1998. Mode of action of linear amphipathic alpha-helical antimicrobial peptides. Biopolymers 47:451-463.
5. Hancock RE. 1997. Peptide antibiotics. Lancet 349:418-422. https://doi.org/10.1016/S0140-6736(97)80051-7.
6. Hancock RE. 2001. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect Dis 1:156-164. https://doi.org/10.1016/S1473-3099(01)00092-5.
7. Shah P, Hsiao FS, Ho YH, Chen CS. 2016. The proteome targets of intracellular targeting antimicrobial peptides. Proteomics 16:1225-1237. https://doi.org/10.1002/pmic.201500380.
8. Di Nardo A, Vitiello A, Gallo RL. 2003. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J Immunol 170:2274-2278. https://doi.org/10.4049/jimmunol.170.5.2274.
9. Rosenberger CM, Gallo RL, Finlay BB. 2004. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc Natl Acad Sci U S A 101:2422-2427. https://doi.org/10.1073/pnas.0304455101.
10. Turner J, Cho Y, Dinh NN, Waring AJ, Lehrer RI. 1998. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob Agents Chemother 42:2206-2214.
11. Lee HY, Andalibi A, Webster P, Moon SK, Teufert K, Kang SH, Li JD, Nagura M, Ganz T, Lim DJ. 2004. Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect Dis 4:12. https://doi.org/10.1186/1471-2334-4-12.
12. Zasloff M. 2002. Innate immunity, antimicrobial peptides, and protection of the oral cavity. Lancet 360:1116-1117. https://doi.org/10.1016/S0140-6736(02)11239-6.
13. Schonwetter BS, Stolzenberg ED, Zasloff MA. 1995. Epithelial antibiotics induced at sites of inflammation. Science 267:1645-1648. https://doi.org/10.1126/science.7886453.
14. Shai Y. 2002. Mode of action of membrane active antimicrobial peptides. Biopolymers 66:236-248. https://doi.org/10.1002/bip.10260.
15. Yeaman MR, Yount NY. 2003. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55:27-55. https://doi.org/10.1124/pr.55.1.2.
16. Hale JD, Hancock RE. 2007. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev Anti Infect Ther 5:951-959. https://doi.org/10.1586/14787210.5.6.951.
17. Sengupta D, Leontiadou H, Mark AE, Marrink SJ. 2008. Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim Biophys Acta 1778:2308-2317. https://doi.org/10.1016/j.bbamem.2008.06.007.
18. Yang L, Harroun TA, Heller WT, Weiss TM, Huang HW. 1998. Neutron off-plane scattering of aligned membranes. I. Method of measurement. Biophys J 75:641-645.
19. Yoneyama F, Imura Y, Ohno K, Zendo T, Nakayama J, Matsuzaki K, Sonomoto K. 2009. Peptide-lipid huge toroidal pore, a new antimicrobial mechanism mediated by a lactococcal bacteriocin, lacticin Q. Antimicrob Agents Chemother 53:3211-3217. https://doi.org/10.1128/AAC.00209-09.
20. Yang L, Harroun TA, Weiss TM, Ding L, Huang HW. 2001. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys J 81:1475-1485.
21. Gazit E, Boman A, Boman HG, Shai Y. 1995. Interaction of the mammalian antibacterial peptide cecropin P1 with phospholipid vesicles. Biochemistry 34:11479-11488. https://doi.org/10.1021/bi00036a021.
22. Nguyen LT, Haney EF, Vogel HJ. 2011. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol 29:464-472. https://doi.org/10.1016/j.tibtech.2011.05.001.
23. Madani F, Lindberg S, Langel U, Futaki S, Graslund A. 2011. Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011:414729.
24. Jones AT. 2007. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 11:670-684. https://doi.org/10.1111/j.1582-4934.2007.00062.x.
25. Mayor S, Pagano RE. 2007. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603-612. https://doi.org/10.1038/nrm2216.
26. Peschel A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol 10:179-186. https://doi.org/10.1016/S0966-842X(02)02333-8.
27. Powers JP, Hancock RE. 2003. The relationship between peptide structure and antibacterial activity. Peptides 24:1681-1691. https://doi.org/10.1016/j.peptides.2003.08.023.
28. Edgerton M, Koshlukova SE, Araujo MW, Patel RC, Dong J, Bruenn JA. 2000. Salivary histatin 5 and human neutrophil defensin 1 kill Candida albicans via shared pathways. Antimicrob Agents Chemother 44:3310-3316. https://doi.org/10.1128/AAC.44.12.3310-3316.2000.
29. Park CB, Kim MS, Kim SC. 1996. A novel antimicrobial peptide from Bufo bufo gargarizans. Biochem Biophys Res Commun 218:408-413. https://doi.org/10.1006/bbrc.1996.0071.
30. Park CB, Yi KS, Matsuzaki K, Kim MS, Kim SC. 2000. 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 97:8245-8250. https://doi.org/10.1073/pnas.150518097.
31. Kobayashi S, Takeshima K, Park CB, Kim SC, Matsuzaki K. 2000. Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry 39:8648-8654. https://doi.org/10.1021/bi0004549.
32. Park CB, Kim HS, Kim SC. 1998. 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 244:253-257. https://doi.org/10.1006/bbrc.1998.8159.
33. Birkemo GA, Luders T, Andersen O, Nes IF, Nissen-Meyer J. 2003. Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Biochim Biophys Acta 1646:207-215. https://doi.org/10.1016/S1570-9639(03)00018-9.
34. Hao G, Shi YH, Tang YL, Le GW. 2013. The intracellular mechanism of action on Escherichia coli of BF2-A/C, two analogues of the antimicrobial peptide Buforin 2. J Microbiol 51:200-206. https://doi.org/10.1007/s12275-013-2441-1.
35. Selsted ME, Novotny MJ, Morris WL, Tang YQ, Smith W, Cullor JS. 1992. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J Biol Chem 267:4292-4295.
36. Falla TJ, Karunaratne DN, Hancock RE. 1996. Mode of action of the antimicrobial peptide indolicidin. J Biol Chem 271:19298-19303. https://doi.org/10.1074/jbc.271.32.19298.
37. Schibli DJ, Epand RF, Vogel HJ, Epand RM. 2002. Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions. Biochem Cell Biol 80:667-677. https://doi.org/10.1139/o02-147.
38. Ladokhin AS, Selsted ME, White SH. 1997. Bilayer interactions of indolicidin, a small antimicrobial peptide rich in tryptophan, proline, and basic amino acids. Biophys J 72:794-805. https://doi.org/10.1016/S0006-3495(97)78713-7.
39. Subbalakshmi C, Krishnakumari V, Nagaraj R, Sitaram N. 1996. Requirements for antibacterial and hemolytic activities in the bovine neutrophil derived 13-residue peptide indolicidin. FEBS Lett 395:48-52. https://doi.org/10.1016/0014-5793(96)00996-9.
40. Subbalakshmi C, 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.
41. Marchand C, Krajewski K, Lee HF, Antony S, Johnson AA, Amin R, Roller P, Kvaratskhelia M, Pommier Y. 2006. Covalent binding of the natural antimicrobial peptide indolicidin to DNA abasic sites. Nucleic Acids Res 34:5157-5165. https://doi.org/10.1093/nar/gkl667.
42. Hsu CH, Chen C, Jou ML, Lee AY, Lin YC, Yu YP, Huang WT, Wu SH. 2005. Structural and DNA-binding studies on the bovine antimicrobial peptide, indolicidin: evidence for multiple conformations involved in binding to membranes and DNA. Nucleic Acids Res 33:4053-4064. https://doi.org/10.1093/nar/gki725.
43. Ghosh A, Kar RK, Jana J, Saha A, Jana B, Krishnamoorthy J, Kumar D, Ghosh S, Chatterjee S, Bhunia A. 2014. Indolicidin targets duplex DNA: structural and mechanistic insight through a combination of spectroscopy and microscopy. ChemMedChem 9:2052-2058. https://doi.org/10.1002/cmdc.201402215.
44. 2+-calmodulin. Biochem Biophys Res Commun 309:879-884. https://doi.org/10.1016/j.bbrc.2003.08.095.
45. Sugiarto H, Yu PL. 2007. Mechanisms of action of ostrich beta-defensins against Escherichia coli. FEMS Microbiol Lett 270:195-200. https://doi.org/10.1111/j.1574-6968.2007.00642.x.
46. Anderson RC, Yu PL. 2003. Isolation and characterisation of proline/ arginine-rich cathelicidin peptides from ovine neutrophils. Biochem Biophys Res Commun 312:1139-1146. https://doi.org/10.1016/j.bbrc.2003.11.045.
47. Nakamura T, Furunaka H, Miyata T, Tokunaga F, Muta T, Iwanaga S, Niwa M, Takao T, 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.
48. Yonezawa A, Kuwahara J, Fujii N, 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.
49. Baquero F, Moreno F. 1984. The microcins. FEMS Microbiol Lett 23: 117-124. https://doi.org/10.1111/j.1574-6968.1984.tb01046.x.
50. Laviña M, Gaggero C, Moreno F. 1990. Microcin H47, a chromosome-encoded microcin antibiotic of Escherichia coli. J Bacteriol 172:6585-6588. https://doi.org/10.1128/jb.172.11.6585-6588.1990.
51. Solbiati JO, Ciaccio M, Farias RN, Salomon RA. 1996. Genetic analysis of plasmid determinants for microcin J25 production and immunity. J Bacteriol 178:3661-3663. https://doi.org/10.1128/jb.178.12.3661-3663.1996.
52. Vizán JL, Hernandez-Chico C, del Castillo I, Moreno F. 1991. The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated by E. coli DNA gyrase. EMBO J 10:467-476.
53. Davagnino J, Herrero M, Furlong D, Moreno F, Kolter R. 1986. The DNA replication inhibitor microcin B17 is a forty-three-amino-acid protein containing sixty percent glycine. Proteins 1:230-238. https://doi.org/10.1002/prot.340010305.
54. Heddle JG, Blance SJ, Zamble DB, Hollfelder F, Miller DA, Wentzell LM, Walsh CT, Maxwell A. 2001. The antibiotic microcin B17 is a DNA gyrase poison: characterisation of the mode of inhibition. J Mol Biol 307:1223-1234. https://doi.org/10.1006/jmbi.2001.4562.
55. Moreno F, San Millan JL, Hernandez-Chico C, Kolter R. 1995. Microcins. Biotechnology 28:307-321.
56. Roy RS, Gehring AM, Milne JC, Belshaw PJ, Walsh CT. 1999. Thiazole and oxazole peptides: biosynthesis and molecular machinery. Nat Prod Rep 16:249-263. https://doi.org/10.1039/a806930a.
57. Parks WM, Bottrill AR, Pierrat OA, Durrant MC, Maxwell A. 2007. The action of the bacterial toxin, microcin B17, on DNA gyrase. Biochimie 89:500-507. https://doi.org/10.1016/j.biochi.2006.12.005.
58. Laviña M, Pugsley AP, Moreno F. 1986. Identification, mapping, cloning and characterization of a gene (sbmA) required for microcin B17 action on Escherichia coli K12. J Gen Microbiol 132:1685-1693.
59. Salomón RA, Farías RN. 1992. Microcin 25, a novel antimicrobial peptide produced by Escherichia coli. J Bacteriol 174:7428-7435. https://doi.org/10.1128/jb.174.22.7428-7435.1992.
60. Bayro MJ, Mukhopadhyay J, Swapna GV, Huang JY, Ma LC, Sineva E, Dawson PE, Montelione GT, Ebright RH. 2003. Structure of antibacterial peptide microcin J25: a 21-residue lariat protoknot. J Am Chem Soc 125:12382-12383. https://doi.org/10.1021/ja036677e.
61. Salomón RA, Farías RN. 1993. The FhuA protein is involved in microcin 25 uptake. J Bacteriol 175:7741-7742. https://doi.org/10.1128/jb.175.23.7741-7742.1993.
62. Salomón RA, Farías RN. 1995. The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J Bacteriol 177:3323-3325. https://doi.org/10.1128/jb.177.11.3323-3325.1995.
63. Yuzenkova J, Delgado M, Nechaev S, Savalia D, Epshtein V, Artsimovitch I, Mooney RA, Landick R, Farias RN, Salomon R, Severinov K. 2002. Mutations of bacterial RNA polymerase leading to resistance to microcin j25. J Biol Chem 277:50867-50875. https://doi.org/10.1074/jbc.M209425200.
64. Mukhopadhyay J, Sineva E, Knight J, Levy RM, Ebright RH. 2004. Antibacterial peptide microcin J25 inhibits transcription by binding within and obstructing the RNA polymerase secondary channel. Mol Cell 14:739-751. https://doi.org/10.1016/j.molcel.2004.06.010.
65. Adelman K, Yuzenkova J, La Porta A, Zenkin N, Lee J, Lis JT, Borukhov S, Wang MD, Severinov K. 2004. Molecular mechanism of transcription inhibition by peptide antibiotic microcin J25. Mol Cell 14:753-762. https://doi.org/10.1016/j.molcel.2004.05.017.
66. Schnapp D, Kemp GD, Smith VJ. 1996. Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 240:532-539. https://doi.org/10.1111/j.1432-1033.1996.0532h.x.
67. Podda E, Benincasa M, Pacor S, Micali F, Mattiuzzo M, Gennaro R, Scocchi M. 2006. Dual mode of action of Bac7, a proline-rich antibacterial peptide. Biochim Biophys Acta 1760:1732-1740. https://doi.org/10.1016/j.bbagen.2006.09.006.
68. Mattiuzzo M, Bandiera A, Gennaro R, Benincasa M, Pacor S, Antcheva N, Scocchi M. 2007. Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides. Mol Microbiol 66:151-163. https://doi.org/10.1111/j.1365-2958.2007.05903.x.
69. Mardirossian M, Grzela R, Giglione C, Meinnel T, Gennaro R, Mergaert P, Scocchi M. 2014. The host antimicrobial peptide Bac71-35 binds to bacterial ribosomal proteins and inhibits protein synthesis. Chem Biol 21:1639-1647. https://doi.org/10.1016/j.chembiol.2014.10.009.
70. Ho YH, Shah P, Chen YW, Chen CS. 2016. Systematic analysis of intracellular-targeting antimicrobial peptides, bactenecin 7, hybrid of pleurocidin and dermaseptin, proline-arginine-rich peptide, and lactoferricin B, by using Escherichia coli proteome microarrays. Mol Cell Proteomics 15:1837-1847. https://doi.org/10.1074/mcp.M115.054999.
71. Ghiselli R, Giacometti A, Cirioni O, Circo R, Mocchegiani F, Skerlavaj B, D'Amato G, Scalise G, Zanetti M, Saba V. 2003. Neutralization of endotoxin in vitro and in vivo by Bac7(1-35), a proline-rich antibacterial peptide. Shock 19:577-581. https://doi.org/10.1097/01.shk.0000055236.26446.c9.
72. Cole AM, Weis P, Diamond G. 1997. Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J Biol Chem 272:12008-12013. https://doi.org/10.1074/jbc.272.18.12008.
73. Patrzykat A, Friedrich CL, Zhang L, Mendoza V, Hancock RE. 2002. Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob Agents Chemother 46:-614605-12013. https://doi.org/10.1128/AAC.46.3.605-614.2002.
74. Friedrich CL, Rozek A, Patrzykat A, Hancock RE. 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.
75. Durr UH, Sudheendra US, Ramamoorthy A. 2006. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim Biophys Acta 1758:1408-1425. https://doi.org/10.1016/j.bbamem.2006.03.030.
76. Robinson WE, Jr, McDougall B, Tran D, Selsted ME. 1998. Anti-HIV-1 activity of indolicidin, an antimicrobial peptide from neutrophils. J Leukoc Biol 63:94-100.
77. Selsted ME, Tang YQ, Morris WL, McGuire PA, Novotny MJ, Smith W, Henschen AH, Cullor JS. 1993. Purification, primary structures, and antibacterial activities of beta-defensins, a new family of antimicrobial peptides from bovine neutrophils. J Biol Chem 268:6641-6648.
78. van Abel RJ, Tang YQ, Rao VS, Dobbs CH, Tran D, Barany G, Selsted ME. 1995. Synthesis and characterization of indolicidin, a tryptophan-rich antimicrobial peptide from bovine neutrophils. Int J Pept Protein Res 45:401-409.
79. Le C-F, Yusof MYM, Hassan H, Sekaran SD. 2015. In vitro properties of designed antimicrobial peptides that exhibit potent antipneumococcal activity and produces synergism in combination with penicillin. Sci Rep 5:9761. https://doi.org/10.1038/srep09761.
80. Le C-F, Yusof MY, Hassan MA, Lee VS, Isa DM, Sekaran SD. 2015. In vivo efficacy and molecular docking of designed peptide that exhibits potent antipneumococcal activity and synergises in combination with penicillin. Sci Rep 5:11886. https://doi.org/10.1038/srep11886.
81. Le C-F, Gudimella R, Razali R, Manikam R, Sekaran SD. 2016. Transcriptome analysis of Streptococcus pneumoniae treated with the designed antimicrobial peptides, DM3. Sci Rep 6:26828. https://doi.org/10.1038/srep26828.
82. Agerberth B, Lee JY, Bergman T, Carlquist M, Boman HG, Mutt V, Jornvall H. 1991. Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur J Biochem 202:849-854.
83. Shi J, Ross CR, Chengappa MM, Blecha F. 1994. Identification of a proline-arginine-rich antibacterial peptide from neutrophils that is analogous to PR-39, an antibacterial peptide from the small intestine. J Leukoc Biol 56:807-811.
84. Pränting M, Negrea A, Rhen M, Andersson DI. 2008. Mechanism and fitness costs of PR-39 resistance in Salmonella enterica serovar Typhimurium LT2. Antimicrob Agents Chemother 52:2734-2741. https://doi.org/10.1128/AAC.00205-08.
85. Boman HG, Agerberth B, Boman A. 1993. Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun 61:2978-2984.
86. Li WF, Ma GX, Zhou XX. 2006. Apidaecin-type peptides: biodiversity, structure-function relationships and mode of action. Peptides 27:2350-2359. https://doi.org/10.1016/j.peptides.2006.03.016.
87. Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P. 1989. Apidaecins: antibacterial peptides from honeybees. EMBO J 8:2387-2391.
88. Casteels P, Romagnolo J, Castle M, Casteels-Josson K, Erdjument-Bromage H, Tempst P. 1994. Biodiversity of apidaecin-type peptide antibiotics. Prospects of manipulating the antibacterial spectrum and combating acquired resistance. J Biol Chem 269:26107-26115.
89. Casteels-Josson K, Capaci T, Casteels P, Tempst P. 1993. Apidaecin multipeptide precursor structure: a putative mechanism for amplification of the insect antibacterial response. EMBO J 12:1569-1578.
90. Casteels P, Tempst P. 1994. Apidaecin-type peptide antibiotics function through a non-poreforming mechanism involving stereospecificity. Biochem Biophys Res Commun 199:339-345. https://doi.org/10.1006/bbrc.1994.1234.
91. Ho YH, Sung TC, Chen CS. 2012. Lactoferricin B inhibits the phosphorylation of the two-component system response regulators BasR and CreB. Mol Cell Proteomics 11:M111.014720. https://doi.org/10.1074/mcp.M111.014720.
92. Tu YH, Ho YH, Chuang YC, Chen PC, Chen CS. 2011. Identification of lactoferricin B intracellular targets using an Escherichia coli proteome chip. PLoS One 6:e28197. https://doi.org/10.1371/journal.pone.0028197.
93. Ganz T, Lehrer RI. 1997. Antimicrobial peptides of leukocytes. Curr Opin Hematol 4:53-58. https://doi.org/10.1097/00062752-199704010-00009.
94. Lehrer RI, Barton A, Daher KA, Harwig SS, Ganz T, Selsted ME. 1989. Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity. J Clin Invest 84:553-561.
95. Jenssen H, Hamill P, Hancock RE. 2006. Peptide antimicrobial agents. Clin Microbiol Rev 19:491-511. https://doi.org/10.1128/CMR.00056-05.
96. Ellis RJ. 1990. The molecular chaperone concept. Semin Cell Biol 1:1-9.
97. Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, Agostini F, Tartaglia GG, Hayer-Hartl M, Hartl FU. 2012. DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1:251-264. https://doi.org/10.1016/j.celrep.2011.12.007.
98. Cociancich S, Dupont A, Hegy G, Lanot R, Holder F, Hetru C, Hoffmann JA, Bulet P. 1994. Novel inducible antibacterial peptides from a hemipteran insect, the sap-sucking bug Pyrrhocoris apterus. Biochem J 300:567-575.
99. Miura K, Ueno S, Kamiya K, Kobayashi J, Matsuoka H, Ando K, Chinzei Y. 1996. Cloning of mRNA sequences for two antibacterial peptides in a hemipteran insect, Riptortus clavatus. Zoolog Sci 13:111-117. https://doi.org/10.2108/zsj.13.111.
100. Otvos L, Jr, O I, Rogers ME, Consolvo PJ, Condie BA, Lovas S, Bulet P, Blaszczyk-Thurin M. 2000. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39:14150-14159. https://doi.org/10.1021/bi0012843.
101. Chesnokova LS, Slepenkov SV, Witt SN. 2004. The insect antimicrobial peptide, L-pyrrhocoricin, binds to and stimulates the ATPase activity of both wild-type and lidless DnaK. FEBS Lett 565:65-69. https://doi.org/10.1016/j.febslet.2004.03.075.
102. Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, Otvos L, Jr. 2001. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40:3016-3026. https://doi.org/10.1021/bi002656a.
103. Rahnamaeian M, Cytrynska M, Zdybicka-Barabas A, Dobslaff K, Wiesner J, Twyman RM, Zuchner T, Sadd BM, Regoes RR, Schmid-Hempel P, Vilcinskas A. 2015. Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proc Biol Sci 282:20150293. https://doi.org/10.1098/rspb.2015.0293.
104. 2): a novel antibacterial peptide optimized against Gram-negative human pathogens. J Med Chem 53:5240-5247. https://doi.org/10.1021/jm100378b.
105. Knappe D, Zahn M, Sauer U, Schiffer G, Strater N, Hoffmann R. 2011. Rational design of oncocin derivatives with superior protease stabilities and antibacterial activities based on the high-resolution structure of the oncocin-DnaK complex. Chembiochem 12:874-876. https://doi.org/10.1002/cbic.201000792.
106. Scocchi M, Lüthy C, Decarli P, Mignogna G, Christen P, Gennaro R. 2009. The proline-rich antibacterial peptide Bac7 binds to and inhibits in vitro the molecular chaperone DnaK. Int J Pept Res Ther 15:9.
107. Sorsa T, Suomalainen K, Uitto VJ. 1990. The role of gingival crevicular fluid and salivary interstitial collagenases in human periodontal diseases. Arch Oral Biol 35(Suppl):193S-196S.
108. Troxler RF, Offner GD, Xu T, Vanderspek JC, Oppenheim FG. 1990. Structural relationship between human salivary histatins. J Dent Res 69:2-6. https://doi.org/10.1177/00220345900690010101.
109. Oppenheim FG, Xu T, McMillian FM, Levitz SM, Diamond RD, Offner GD, Troxler RF. 1988. Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J Biol Chem 263:7472-7477.
110. Puri S, Edgerton M. 2014. How does it kill?: understanding the candidacidal mechanism of salivary histatin 5. Eukaryot Cell 13:958-964. https://doi.org/10.1128/EC.00095-14.
111. MacKay BJ, Denepitiya L, Iacono VJ, Krost SB, Pollock JJ. 1984. Growth-inhibitory and bactericidal effects of human parotid salivary histidinerich polypeptides on Streptococcus mutans. Infect Immun 44:695-701.
112. Forssten SD, Bjorklund M, Ouwehand AC. 2010. Streptococcus mutans, caries and simulation models. Nutrients 2:290-298. https://doi.org/10.3390/nu2030290.
113. Gusman H, Travis J, Helmerhorst EJ, Potempa J, Troxler RF, Oppenheim FG. 2001. Salivary histatin 5 is an inhibitor of both host and bacterial enzymes implicated in periodontal disease. Infect Immun 69:1402-1408. https://doi.org/10.1128/IAI.69.3.1402-1408.2001.
114. Gusman H, Grogan J, Kagan HM, Troxler RF, Oppenheim FG. 2001. Salivary histatin 5 is a potent competitive inhibitor of the cysteine proteinase clostripain. FEBS Lett 489:97-100. https://doi.org/10.1016/S0014-5793(01)02077-4.
115. Stevens DL, Bisno AL, Chambers HF, Everett ED, Dellinger P, Goldstein EJ, Gorbach SL, Hirschmann JV, Kaplan EL, Montoya JG, Wade JC. 2005. Practice guidelines for the diagnosis and management of skin and soft-tissue infections. Clin Infect Dis 41:1373-1406. https://doi.org/10.1086/497143.
116. Nishikata M, Kanehira T, Oh H, Tani H, Tazaki M, Kuboki Y. 1991. Salivary histatin as an inhibitor of a protease produced by the oral bacterium Bacteroides gingivalis. Biochem Biophys Res Commun 174:625-630. https://doi.org/10.1016/0006-291X(91)91463-M.
117. Couto MA, Harwig SS, Cullor JS, Hughes JP, Lehrer RI. 1992. eNAP-2, a novel cysteine-rich bactericidal peptide from equine leukocytes. Infect Immun 60:5042-5047.
118. Couto MA, Harwig SS, Lehrer RI. 1993. Selective inhibition of microbial serine proteases by eNAP-2, an antimicrobial peptide from equine neutrophils. Infect Immun 61:2991-2994.
119. Fogaça AC, Almeida IC, Eberlin MN, Tanaka AS, Bulet P, Daffre S. 2006. Ixodidin, a novel antimicrobial peptide from the hemocytes of the cattle tick Boophilus microplus with inhibitory activity against serine proteinases. Peptides 27:667-674. https://doi.org/10.1016/j.peptides.2005.07.013.
120. Lutkenhaus J. 1990. Regulation of cell division in E. coli. Trends Genet 6:22-25. https://doi.org/10.1016/0168-9525(90)90045-8.
121. Ishikawa M, Kubo T, Natori S. 1992. Purification and characterization of a diptericin homologue from Sarcophaga peregrina (flesh fly). Biochem J 287:573-578.
122. Wanniarachchi YA, Kaczmarek P, Wan A, Nolan EM. 2011. Human defensin 5 disulfide array mutants: disulfide bond deletion attenuates antibacterial activity against Staphylococcus aureus. Biochemistry 50:8005-8017. https://doi.org/10.1021/bi201043j.
123. Moser S, Chileveru HR, Tomaras J, Nolan EM. 2014. A bacterial mutant library as a tool to study the attack of a defensin peptide. Chembiochem 15:2684-2688. https://doi.org/10.1002/cbic.201402354.
124. Chileveru HR, Lim SA, Chairatana P, Wommack AJ, Chiang IL, Nolan EM. 2015. Visualizing attack of Escherichia coli by the antimicrobial peptide human defensin 5. Biochemistry 54:1767-1777. https://doi.org/10.1021/bi501483q.
125. Navarre WW, Schneewind O. 1999. Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174-229.
126. Vollmer W, Holtje JV. 2001. Morphogenesis of Escherichia coli. Curr Opin Microbiol 4:625-633. https://doi.org/10.1016/S1369-5274(01)00261-2.
127. Koch AL. 2003. Bacterial wall as target for attack: past, present, and future research. Clin Microbiol Rev 16:673-687. https://doi.org/10.1128/CMR.16.4.673-687.2003.
128. Prasch T, Naumann T, Markert RL, Sattler M, Schubert W, Schaal S, Bauch M, Kogler H, Griesinger C. 1997. Constitution and solution conformation of the antibiotic mersacidin determined by NMR and molecular dynamics. Eur J Biochem 244:501-512. https://doi.org/10.1111/j.1432-1033.1997.00501.x.
129. Brötz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG. 1998. The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 42:154-160.
130. Brötz H, Bierbaum G, Reynolds PE, Sahl HG. 1997. The lantibiotic mersacidin inhibits peptidoglycan biosynthesis at the level of transglycosylation. Eur J Biochem 246:193-199. https://doi.org/10.1111/j.1432-1033.1997.t01-1-00193.x.
131. Chatterjee S, Lad SJ, Phansalkar MS, Rupp RH, Ganguli BN, Fehlhaber HW, Kogler H. 1992. Mersacidin, a new antibiotic from Bacillus. Fermentation, isolation, purification and chemical characterization. J Antibiot (Tokyo) 45:832-838.
132. Hoffmann A, Pag U, Wiedemann I, Sahl HG. 2002. Combination of antibiotic mechanisms in lantibiotics. Farmaco 57:685-691. https://doi.org/10.1016/S0014-827X(02)01208-9.
133. Kruszewska D, Sahl HG, Bierbaum G, Pag U, Hynes SO, Ljungh A. 2004. Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J Antimicrob Chemother 54:648-653. https://doi.org/10.1093/jac/dkh387.
134. de Leeuw E, Li C, Zeng P, Diepeveen-de Buin M, Lu WY, Breukink E, Lu W. 2010. Functional interaction of human neutrophil peptide-1 with the cell wall precursor lipid II. FEBS Lett 584:1543-1548. https://doi.org/10.1016/j.febslet.2010.03.004.
135. Sass V, Schneider T, Wilmes M, Korner C, Tossi A, Novikova N, Shamova O, Sahl HG. 2010. Human beta-defensin 3 inhibits cell wall biosynthesis in stapylococci. Infect Immun 78:2793-2800. https://doi.org/10.1128/IAI.00688-09.
136. Breukink E, de Kruijff B. 2006. Lipid II as a target for antibiotics. Nat Rev Drug Discov 5:321-332. https://doi.org/10.1038/nrd2004.
137. Hsu ST, Breukink E, Tischenko E, Lutters MA, de Kruijff B, Kaptein R, Bonvin AM, van Nuland NA. 2004. The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat Struct Mol Biol 11:963-967. https://doi.org/10.1038/nsmb830.
138. Hasper HE, Kramer NE, Smith JL, Hillman JD, Zachariah C, Kuipers OP, de Kruijff B, Breukink E. 2006. An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313:1636-1637. https://doi.org/10.1126/science.1129818.
139. Wescombe PA, Tagg JR. 2003. Purification and characterization of streptin, a type A1 lantibiotic produced by Streptococcus pyogenes. Appl Environ Microbiol 69:2737-2747. https://doi.org/10.1128/AEM.69.5.2737-2747.2003.
140. Stein T, Borchert S, Conrad B, Feesche J, Hofemeister B, Hofemeister J, Entian KD. 2002. Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3. J Bacteriol 184:1703-1711. https://doi.org/10.1128/JB.184.6.1703-1711.2002.
141. McAuliffe O, Ross RP, Hill C. 2001. Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol Rev 25:285-308. https://doi.org/10.1111/j.1574-6976.2001.tb00579.x.
142. Bonelli RR, Schneider T, Sahl HG, Wiedemann I. 2006. Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-ofaction studies. Antimicrob Agents Chemother 50:1449-1457. https://doi.org/10.1128/AAC.50.4.1449-1457.2006.
143. Furmanek B, Kaczorowski T, Bugalski R, Bielawski K, Bohdanowicz J, Podhajska AJ. 1999. Identification, characterization and purification of the lantibiotic staphylococcin T, a natural gallidermin variant. J Appl Microbiol 87:856-866. https://doi.org/10.1046/j.1365-2672.1999.00937.x.
144. Essig A, Hofmann D, Munch D, Gayathri S, Kunzler M, Kallio PT, Sahl HG, Wider G, Schneider T, Aebi M. 2014. Copsin, a novel peptide-based fungal antibiotic interfering with the peptidoglycan synthesis. J Biol Chem 289:34953-34964. https://doi.org/10.1074/jbc.M114.599878.
145. Schneider T, Kruse T, Wimmer R, Wiedemann I, Sass V, Pag U, Jansen A, Nielsen AK, Mygind PH, Raventos DS, Neve S, Ravn B, Bonvin AM, De Maria L, Andersen AS, Gammelgaard LK, Sahl HG, Kristensen HH. 2010. Plectasin, a fungal defensin, targets the bacterial cell wall precursor lipid II. Science 328:1168-1172. https://doi.org/10.1126/science.1185723.
146. Mygind PH, Fischer RL, Schnorr KM, Hansen MT, Sonksen CP, Ludvigsen S, Raventos D, Buskov S, Christensen B, De Maria L, Taboureau O, Yaver D, Elvig-Jorgensen SG, Sorensen MV, Christensen BE, Kjaerulff S, Frimodt-Moller N, Lehrer RI, Zasloff M, Kristensen HH. 2005. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437:975-980. https://doi.org/10.1038/nature04051.
147. Sahl HG, Brandis H. 1981. Production, purification and chemical properties of an antistaphylococcal agent produced by Staphylococcus epidermidis. J Gen Microbiol 127:377-384.
148. Bierbaum G, Sahl HG. 1987. Autolytic system of Staphylococcus simulans 22: influence of cationic peptides on activity of N-acetylmuramoyl-L-alanine amidase. J Bacteriol 169:5452-5458. https://doi.org/10.1128/jb.169.12.5452-5458.1987.
149. Yeaman MR, Puentes SM, Norman DC, Bayer AS. 1992. Partial characterization and staphylocidal activity of thrombin-induced platelet microbicidal protein. Infect Immun 60:1202-1209.
150. Yeaman MR, Norman DC, Bayer AS. 1992. Platelet microbicidal protein enhances antibiotic-induced killing of and postantibiotic effect in Staphylococcus aureus. Antimicrob Agents Chemother 36:1665-1670. https://doi.org/10.1128/AAC.36.8.1665.
151. Yeaman MR, Ibrahim AS, Edwards JE, Jr, Bayer AS, Ghannoum MA. 1993. Thrombin-induced rabbit platelet microbicidal protein is fungicidal in vitro. Antimicrob Agents Chemother 37:546-553. https://doi.org/10.1128/AAC.37.3.546.
152. Yeaman MR, Tang YQ, Shen AJ, Bayer AS, Selsted ME. 1997. Purification and in vitro activities of rabbit platelet microbicidal proteins. Infect Immun 65:1023-1031.
153. Koo SP, Bayer AS, Sahl HG, Proctor RA, Yeaman MR. 1996. Staphylocidal action of thrombin-induced platelet microbicidal protein is not solely dependent on transmembrane potential. Infect Immun 64:1070-1074.
154. Shimoda M, Ohki K, Shimamoto Y, Kohashi O. 1995. Morphology of defensin-treated Staphylococcus aureus. Infect Immun 63:2886-2891.
155. Yeaman MR, Bayer AS, Koo SP, Foss W, Sullam PM. 1998. Platelet microbicidal proteins and neutrophil defensin disrupt the Staphylococcus aureus cytoplasmic membrane by distinct mechanisms of action. J Clin Invest 101:178-187. https://doi.org/10.1172/JCI562.
156. Xiong YQ, Yeaman MR, Bayer AS. 1999. 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 43:1111-1117.
157. Viljanen P, Koski P, Vaara M. 1988. Effect of small cationic leukocyte peptides (defensins) on the permeability barrier of the outer membrane. Infect Immun 56:2324-2329.
158. Raetz CR, Reynolds CM, Trent MS, Bishop RE. 2007. Lipid A modification systems in Gram-negative bacteria. Annu Rev Biochem 76:295-329. https://doi.org/10.1146/annurev.biochem.76.010307.145803.
159. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635-700. https://doi.org/10.1146/annurev.biochem.71.110601.135414.
160. Tracey KJ, Fong Y, Hesse DG, Manogue KR, Lee AT, Kuo GC, Lowry SF, Cerami A. 1987. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature 330: 662-664. https://doi.org/10.1038/330662a0.
161. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher CJ, Jr, Recombinant Human Protein C Worldwide Evaluation in Severe Sepsis (PROWESS) Study Group. 2001. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344:699-709. https://doi.org/10.1056/NEJM200103083441001.
162. Esmon CT. 2000. Regulation of blood coagulation. Biochim Biophys Acta 1477:349-360. https://doi.org/10.1016/S0167-4838(99)00266-6.
163. van Deuren M, Brandtzaeg P, van der Meer JWM. 2000. Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13:144-166. https://doi.org/10.1128/CMR.13.1.144-166.2000.
164. Piers KL, Brown MH, Hancock RE. 1994. Improvement of outer membrane-permeabilizing and lipopolysaccharide-binding activities of an antimicrobial cationic peptide by C-terminal modification. Antimicrob Agents Chemother 38:2311-2316. https://doi.org/10.1128/AAC.38.10.2311.
165. Piers KL, Hancock RE. 1994. The interaction of a recombinant cecropin/melittin hybrid peptide with the outer membrane of Pseudomonas aeruginosa. Mol Microbiol 12:951-958. https://doi.org/10.1111/j.1365-2958.1994.tb01083.x.
166. Gough M, Hancock RE, Kelly NM. 1996. Antiendotoxin activity of cationic peptide antimicrobial agents. Infect Immun 64:4922-4927.
167. Gee K, Kozlowski M, Kumar A. 2003. Tumor necrosis factor-alpha induces functionally active hyaluronan-adhesive CD44 by activating sialidase through p38 mitogen-activated protein kinase in lipopolysaccharide-stimulated human monocytic cells. J Biol Chem 278:37275-37287. https://doi.org/10.1074/jbc.M302309200.
168. Kubo Y, Fukuishi N, Yoshioka M, Kawasoe Y, Iriguchi S, Imajo N, Yasui Y, Matsui N, Akagi M. 2007. Bacterial components regulate the expression of Toll-like receptor 4 on human mast cells. Inflamm Res 56:70-75. https://doi.org/10.1007/s00011-006-6064-4.
169. Mukhopadhyay S, Herre J, Brown GD, Gordon S. 2004. The potential for Toll-like receptors to collaborate with other innate immune receptors. Immunology 112:521-530. https://doi.org/10.1111/j.1365-2567.2004.01941.x.
170. Sun Y, Shang D. 2015. Inhibitory effects of antimicrobial peptides on lipopolysaccharide-induced inflammation. Mediators Inflamm 2015:167572. https://doi.org/10.1155/2015/167572.
171. Frecer V, Ho B, Ding JL. 2000. Interpretation of biological activity data of bacterial endotoxins by simple molecular models of mechanism of action. Eur J Biochem 267:837-852. https://doi.org/10.1046/j.1432-1327.2000.01069.x.
172. Muhle SA, Tam JP. 2001. Design of Gram-negative selective antimicrobial peptides. Biochemistry 40:5777-5785. https://doi.org/10.1021/bi0100384.
173. Maria-Neto S, Candido Ede S, Rodrigues DR, de Sousa DA, da Silva EM, de Moraes LM, Otero-Gonzalez Ade J, Magalhaes BS, Dias SC, Franco OL. 2012. Deciphering the magainin resistance process of Escherichia coli strains in light of the cytosolic proteome. Antimicrob Agents Chemother 56:1714-1724. https://doi.org/10.1128/AAC.05558-11.
174. Jindal HM, Le CF, Mohd Yusof MY, Velayuthan RD, Lee VS, Zain SM, Isa DM, Sekaran SD. 2015. Antimicrobial activity of novel synthetic peptides derived from indolicidin and ranalexin against Streptococcus pneumoniae. PLoS One 10:e0128532. https://doi.org/10.1371/journal.pone.0128532.
175. Lum KY, Tay ST, Le CF, Lee VS, Sabri NH, Velayuthan RD, Hassan H, Sekaran SD. 2015. Activity of novel synthetic peptides against Candida albicans. Sci Rep 5:9657. https://doi.org/10.1038/srep09657.
176. 2+ on its interaction with a biomimetic membrane. Soft Matter 10: 616-626. https://doi.org/10.1039/C3SM52400K.
177. Harris F, Dennison SR, Phoenix DA. 2009. Anionic antimicrobial peptides from eukaryotic organisms. Curr Protein Pept Sci 10:585-606. https://doi.org/10.2174/138920309789630589.
178. Noore J, Noore A, Li B. 2013. Cationic antimicrobial peptide LL-37 is effective against both extra- and intracellular Staphylococcus aureus. Antimicrob Agents Chemother 57:1283-1290. https://doi.org/10.1128/AAC.01650-12.
179. Chen L, Todd R, Kiehlbauch J, Walters M, Kallen A. 2017. Notes from the field: pan-resistant New Delhi-metallo-beta-lactamase-producing Klebsiella pneumoniae-Washoe County, Nevada, 2016. MMWR Morb Mortal Wkly Rep 66:33. https://doi.org/10.15585/mmwr.mm6601a7.