Cell specificity, anti-inflammatory activity, and plausible bactericidal mechanism of designed Trp-rich model antimicrobial peptides

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 5, 2009, Pages 1193-1203

  Park, Ka Hyon ^a   Nan, Yong Hai ^a   Park, Yoonkyung ^a,b   Kim, Jae Il ^c   Park, Il Seon ^a,d   Hahm, Kyung Soo ^a,d   Shin, Song Yub ^a,d  

^a Chosun University   (South Korea)

^b Chosun University   (South Korea)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

^d Chosun University College of Medicine   (South Korea)

Author keywords

Anti inflammatory activity; Bactericidal mechanism; Cell specificity; Trp rich model antimicrobial peptide

Indexed keywords

ANTIINFECTIVE AGENT; ANTIINFLAMMATORY AGENT; ARGININE; ARGINYLARGINYLTRYPTOPHYLARGINYLARGINYLTRYPTOPHYLARGINYLARGINYL TRYPTOPHYLARGINYLARGININAMIDE; ARGINYLLEUCYLTRYPTOPHYLARGINYLARGINYLTRYPTOPHYLARGINYLARGINYL TRYPTOPHYLARGINYLARGININAMIDE; ARGINYLLEUCYLTRYPTOPHYLARGINYLARGINYLTRYPTOPHYLARGINYLARGINYL TRYPTOPHYLLEUCYLARGININAMIDE; ARGINYLLEUCYLTRYPTOPHYLARGINYLARGINYLTRYPTOPHYLARGINYLARGINYL TRYPTOPHYLLYSYLARGININAMIDE; BUFORIN 2; DNA; INDOLICIDIN; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOLEUCYLLEUCYLPROLYLTRYPTOPHYLLYSYLTRYPTOPHYLPROLYLTRYPTOPHYL TRYPTOPHYLPROLYLTRYPTOPHYLARGINYLARGININAMIDE; LEUCINE; LIPOPOLYSACCHARIDE; LIPOSOME; LYSINE; LYSYLLEUCYLTRYPTOPHYLLEUCYLLEUCYLTRYPTOPHYLLEUCYLLYSYLTRYPTOPHYLL EUCYLLEUCINAMIDE; LYSYLLEUCYLTRYPTOPHYLLYSYLLEUCYLTRYPTOPHYLLEUCYLLYSYLTRYPTOPHYLL EUCYLLYSINAMIDE; LYSYLLEUCYLTRYPTOPHYLLYSYLLEUCYLTRYPTOPHYLLEUCYLLYSYLTRYPTOPHYLLEUCYLL EUCINAMIDE; LYSYLLEUCYLTRYPTOPHYLLYSYLLEUCYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLL EUCYLLYSINAMIDE; LYSYLLEUCYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLL EUCYLLYSINAMIDE; LYSYLLEUCYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLLYSYLLY SINAMIDE; LYSYLLYSYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLLYSYLLYSYLTRYPTOPHYLLYSYLLY SINAMIDE; MESSENGER RNA; NITRIC OXIDE; POLYPEPTIDE ANTIBIOTIC AGENT; RNA; TRYPSIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERICIDAL ACTIVITY; CELL MEMBRANE; CELL SPECIFICITY; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DNA SYNTHESIS; DRUG ACCUMULATION; DRUG BINDING; DRUG MECHANISM; DRUG PENETRATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; RNA INTERFERENCE; RNA SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; DNA; DRUG DESIGN; HEMOLYSIS; HUMANS; LIPOPOLYSACCHARIDES; LIPOSOMES; MACROPHAGES; MICE; MICROBIAL SENSITIVITY TESTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OLIGOPEPTIDES; RNA, MESSENGER; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 65249175757     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.02.020     Document Type: Article

References (51)

1. Boman H.G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13 (1995) 61-92
2. Lehrer R.I., and Ganz T. Antimicrobial peptides in mammalian and insect host defence. Curr. Opin. Immunol. 11 (1999) 23-27
3. Hancock R., and Diamond G. The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol. 8 (2000) 402-410
4. Brown K.L., and Hancock R.E. Cationic host defense (antimicrobial) peptides. Curr. Opin. Immunol. 18 (2006) 24-30
5. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
6. Hancock R.E., and Patrzykat A. Clinical development of cationic antimicrobial peptides: from natural to novel antibiotics. Curr. Drug Targets Infect. Disord. 2 (2002) 79-83
7. Oren Z., and Shai Y. Mode of action of linear amphipathic α-helical antimicrobial peptides. Biopolymers 47 (1998) 451-463
8. Tossi A., Sandri L., and Giangaspero A. Amphipathic, α-helical antimicrobial peptides. Biopolymers 55 (2000) 4-30
9. Epand R.F., Lehrer R.I., Wang W., Maget-Dana R., Lelievre D., and Epand R.M. Direct comparison of membrane interactions of model peptides composed of only Leu and Lys residues. Biopolymers 71 (2003) 2-16
10. Bven L., Castano S., Dufourcq J., Wieslander A., and Wrblewski H. The antibiotic activity of cationic linear amphipathic peptides: lessons from the action of leucine/lysine copolymers on bacteria of the class Mollicutes. Eur. J. Biochem. 270 (2003) 2207-2217
11. Song Y.M., Yang S.T., Lim S.S., Kim Y., Hahm K.S., Kim J.I., and Shin S.Y. Effects of L- or D-Pro incorporation into hydrophobic or hydrophilic helix face of amphipathic α-helical model peptide on structure and cell selectivity. Biochem. Biophys. Res. Commun. 314 (2004) 615-621
12. Song Y.M., Park Y., Lim S.S., Yang S.T., Woo E.R., Park I.S., Lee J.S., Kim J.I., Hahm K.S., Kim Y., and Shin S.Y. Cell selectivity and mechanism of action of antimicrobial model peptides containing peptoid residues. Biochemistry 44 (2005) 12094-12106
13. Chan D.I., Prenner E.J., and Vogel H.J. Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta 2006 (1758) 1184-1202
14. Schibli D.J., Epand R.F., Vogel H.J., and Epand R.M. Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions. Biochem. Cell Biol. 80 (2002) 667-677
15. Yang S.T., Shin S.Y., Lee C.W., Kim Y.C., Hahm K.S., and Kim J.I. Selective cytotoxicity following Arg-to-Lys substitution in tritrpticin adopting a unique amphipathic turn structure. FEBS Lett. 540 (2003) 229-233
16. Yang S.T., Shin S.Y., Kim Y.C., Kim Y., Hahm K.S., and Kim J.I. Conformation-dependent antibiotic activity of tritrpticin, a cathelicidin-derived antimicrobial peptide. Biochem. Biophys. Res. Commun. 296 (2002) 1044-1050
17. Selsted M.E., Novotny M.J., Morris W.L., Tang Y.Q., Smith W., and Cullor J.S. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267 (1992) 4292-4295
18. Ryge T.S., Doisy X., Ifrah D., Olsen J.E., and Hansen P.R. New indolicidin analogues with potent antibacterial activity. J. Pept. Res. 64 (2004) 171-185
19. Rozek A., Powers J.P., Friedrich C.L., and Hancock R.E. Structure-based design of an indolicidin peptide analogue with increased protease stability. Biochemistry 42 (2003) 14130-14138
20. Friedrich C.L., Rozek A., Patrzykat A., and Hancock R.E. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against Gram-positive bacteria. J. Biol. Chem. 276 (2001) 24015-24022
21. Subbalakshmi C., Bikshapathy E., Sitaram N., and Nagaraj R. Antibacterial and hemolytic activities of single tryptophan analogs of indolicidin. Biochem. Biophys. Res. Commun. 274 (2000) 714-716
22. Alexander C., and Rietschel E.T. Bacterial lipopolysaccharides and innate immunity. J. Endotoxin Res. 7 (2001) 167-202
23. Cohen J. The immunopathogenesis of sepsis. Nature 420 (2002) 885-918
24. Rosenfeld Y., Papo N., and Shai Y. Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem. 281 (2006) 1636-1643
25. Zughaier S.M., Shafer W.M., and Stephens D.S. Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages. Cell Microbiol. 7 (2005) 1251-1262
26. Rosenfeld Y., and Shai Y. Lipopolysaccharide (endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim. Biophys. Acta 1758 (2006) 1513-1522
27. Yoshioka M., Fukuishi N., Kubo Y., Yamanobe H., Ohsaki K., Kawasoe Y., Murata M., Ishizumi A., Nishii Y., Matsui N., and Akagi M. Human cathelicidin CAP18/LL-37 changes mast cell function toward innate immunity. Biol. Pharm. Bull. 31 (2008) 212-216
28. Hancock R.E. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1 (2001) 156-164
29. Bowdish D.M., Davidson D.J., Scott M.G., and Hancock R.E. Immunomodulatory activity of small host defense peptides. Antimicrob. Agents Chemother. 49 (2005) 1727-1732
30. Hancock R.E., and Scott M.G. The role of antimicrobial peptides in animal defenses. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8856-8861
31. Nagaoka I., Hirota S., Niyonsaba F., Hirata M., Adachi Y., Tamura H., and Heumann D. Cathelicidin family of antibacterial peptides CAP18 and CAP11 inhibit the expression of TNF-alpha by blocking the binding of LPS to CD14 (+) cells. J. Immunol. 167 (2001) 3329-3338
32. Mao D., and Wallace B.A. Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles. Biochemistry 23 (1984) 2667-2673
33. Shai Y., Bach D., and Yanovsky A. Channel formation properties of synthetic pardaxin and analogues. J. Biol. Chem. 265 (1990) 20202-20209
34. Barlett C.R. Phosphorus assay in column chromatography. J. Biol. Chem. 234 (1959) 466-468
35. Scudiero D.A., Shoemaker R.H., Paull K.D., Monks A., Tierney S., Nofziger T.H., Currens M.J., Seniff D., and Boyd M.R. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res. 48 (1988) 4827-4833
36. 15N]nitrate in biological fluids. Anal. Biochemistry 126 (1982) 131-138
37. Jeon Y.J., Han S.B., Ahn K.S., and Kim H.M. Activation of NF-kappaB/Rel in angelan-stimulated macrophages. Immunopharmacology 43 (1999) 1-9
38. Tack B.F., Sawai M.V., Kearney W.R., Robertson A.D., Sherman M.A., Wang W., Hong T., Boo L.M., Wu H., and Waring A.J. SMAP-29 has two LPS-binding sites and a central hinge. Eur. J. Biochem. 269 (2002) 1181-1189
39. Xiao Y., Dai H., Bommineni Y.R., Soulages J.L., Gong Y.X., Prakash O., and Zhang G. Structure-activity relationships of fowlicidin-1, a cathelicidin antimicrobial peptide in chicken. FEBS J. 273 (2006) 2581-2593
40. Kiyota T., Lee S., and Sugihara G. Design and synthesis of amphiphilic α-helical model peptides with systematically varied hydrophobic-hydrophilic balance and their interaction with lipid- and bio-membranes. Biochemistry 35 (1996) 13196-13204
41. Kim S., Kim S.S., and Lee B.J. Correlation between the activities of α-helical antimicrobial peptides and hydrophobicities represented as RP-HPLC retention times. Peptides 26 (2005) 2050-2056
42. Chen Y., Mant C.T., Farmer S.W., Hancock R.E., Vasil M.L., and Hodges R.S. Rational design of α-helical antimicrobial peptides with enhanced activities and specificity/therapeutic index. J. Biol. Chem. 280 (2005) 12316-12329
43. Zhu W.L., Song Y.M., Park Y., Park K.H., Yang S.T., Kim J.I., Park I.S., Hahm K.S., and Shin S.Y. Substitution of the leucine zipper sequence in melittin with peptoid residues affects self-association, cell selectivity, and mode of action. Biochim. Biophys. Acta 1768 (2007) 1506-1517
44. Hamamoto K., Kida Y., Zhang Y., Shimizu T., and Kuwano K. Antimicrobial activity and stability to proteolysis of small linear cationic peptides with d-amino acid substitutions. Microbiol. Immunol. 46 (2002) 741-749
45. Park C.B., Kim H.S., and Kim S.C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244 (1998) 253-257
46. Shai Y. Mode of action of membrane active antimicrobial peptides. Biopolymers 66 (2002) 236-248
47. Dathe M., and Wieprecht T. Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta 1462 (1999) 71-87
48. Park C.B., Yi K.S., Matsuzaki K., Kim M.S., and Kim S.C. Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8245-8250
49. Tomasinsig L., Skerlavaj B., Papo N., Giabbai B., Shai Y., and Zanetti M. Mechanistic and functional studies of the interaction of a proline-rich antimicrobial peptide with mammalian cells. J. Biol. Chem. 281 (2006) 383-391
50. Cudic M., and Otvos Jr. L. Intracellular targets of antibacterial peptides. Curr. Drug Targets 3 (2002) 101-106
51. Boman H.G., Agerberth B., and Boman A. Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect. Immun. 61 (1993) 2978-2984