Strand length-dependent antimicrobial activity and membrane-active mechanism of arginine- and valine-rich β-hairpin-like antimicrobial peptides

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 6, 2012, Pages 2994-3003

  Dong, Na ^a   Ma, Qingquan ^a   Shan, Anshan ^a   Lv, Yinfeng ^a   Hu, Wanning ^a   Gu, Yao ^a   Li, Yuzhi ^b  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOLYTE; ARGININE; MELITTIN; POLYPEPTIDE ANTIBIOTIC AGENT; TRYPTOPHAN; UNCLASSIFIED DRUG; VALINE; VR1 PEPTIDE; VR2 PEPTIDE; VR3 PEPTIDE; VR4 PEPTIDE; VR5 PEPTIDE; VRW3 PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIAL COUNT; BACTERIAL INFECTION; BACTERICIDAL ACTIVITY; BETA SHEET; CELL MEMBRANE; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG POTENCY; DRUG SCREENING; DRUG SYNTHESIS; DRUG TARGETING; ESCHERICHIA COLI; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VIVO STUDY; LIPID VESICLE; MALE; MAMMAL CELL; MEMBRANE DEPOLARIZATION; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; OUTER MEMBRANE; PERITONEUM; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; STAPHYLOCOCCUS EPIDERMIDIS; STRUCTURE ACTIVITY RELATION; SURVIVAL RATE;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ARGININE; CELLS, CULTURED; HEMOLYSIS; HUMANS; MALE; MICE; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; STRUCTURE-ACTIVITY RELATIONSHIP; VALINE;

EID: 84861123585     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.06327-11     Document Type: Article

References (47)

1. Blondelle SE, Houghten RA. 1991. Hemolytic and antimicrobial activities of the twenty-four individual omission analogues of melittin. Biochemistry 30:4671-4678.
2. Brogden KA. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Mol. 3:238-250. (Pubitemid 40298223)
3. Chakraborty TK, Rao KS, Kiran MU, Jagadeesh B. 2008. Nucleation of the beta-hairpin structure in a linear hybrid peptide containing alpha-, beta- and gamma-amino acids. Tetrahedron Lett. 49:2228-2231.
4. Chen Y, et al. 2005. Rational design of alpha-helical antimicrobial peptides with enhanced activities and specificity/therapeutic index. J. Biol. Chem. 280:12316-12329.
5. Davey HM, Kell DB, Weichart DH, Kaprelyants AS. 2004. Estimation of microbial viability using flow cytometry. Curr. Protoc. Cytom. 11:11.3.
6. Dempsey CE. 1990. The actions of melittin on membranes. Biochim. Biophys. Acta 1031:143-161.
7. Deslouches B, et al. 2005. De novo generation of cationic antimicrobial peptides: influence of length and tryptophan substitution on antimicrobial activity. Antimicrob. Agents Chemother. 49:316-322. (Pubitemid 40065808)
8. Falla TJ, Karunaratne DN, Hancock REW. 1996. Mode of action of the antimicrobial peptide indolicidin. J. Biol. Chem. 271:19298 -19303.
9. Frecer V, Ho B, Ding JL. 2004. De novo design of potent antimicrobial peptides. Antimicrob. Agents Chemother. 48:3349-3357. (Pubitemid 39129330)
10. Friedrich CL, Rozek A, Patrzykat A, Hancock REW. 2001. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria. J. Biol. Chem. 276:24015-24022.
11. Gottler LM, de la Salud Bea R, Shelburne CE, Ramamoorthy A, Marsh ENG. 2008. Using fluorous amino acids to probe the effects of changing hydrophobicity on the physical and biological properties of the β-hairpin antimicrobial peptide protegrin-1. Biochemistry 47:9243-9250.
12. Hancock REW. 1999. Host defence (cationic) peptides: what is their future clinical potential? Drugs 57:469-473. (Pubitemid 29196915)
13. Haque TS, Little JC, Gellman SH. 1994. 'Mirror-image' reverse turns promote β-hairpin formation. J. Am. Chem. Soc. 116:4105-4106. (Pubitemid 24981013)
14. Helander IM, Nurmiaho-Lassila E-L, Ahvenainen R, Rhoades J, Roller S. 2001. Chitosan disrupts the barrier properties of the outer membrane of gram-negative bacteria, Int. J. Food Microbiol. 71:235-244. (Pubitemid 33123347)
15. Jiang Z, Vasil AI, Gera L, Vasil ML, Hodges RS. 2011. Rational design of α-helical antimicrobial peptides to target gram-negative pathogens, Acinetobacter baumannii and Pseudomonas aeruginosa: utilization of charge, 'specificity determinants,' total hydrophobicity, hydrophobe type and location as design parameters to improve the therapeutic ratio. Chem. Biol. Drug Des. 77:225-240.
16. Jin X, et al. 2010. Apoptosis-inducing activity of the antimicrobial peptide cecropin of Musca domestica in human hepatocellular carcinoma cell line BEL-7402 and the possible mechanism. Acta Biochim. Biophys. Sin. 42:259-265.
17. Jin Y, et al. 2005. Antimicrobial activities and structures of two linear cationic peptide families with various amphipathic β-sheet and α-helical potentials. Antimicrob. Agents Chemother. 49:4957-4964. (Pubitemid 41778906)
18. Juffer AH, Shepherd CM, Vogel HJ. 2001. Protein-membrane electrostatic interactions: application of the Lekner summation technique. J. Chem. Phys. 114:1892-1905. (Pubitemid 32168664)
19. Lee DL, et al. 2004. Effects of single D-amino acid substitutions on disruption of β-sheet structure and hydrophobicity in cyclic 14-residue antimicrobial peptide analogs related to gramicidin S. J. Pept. Res. 63:69-84. (Pubitemid 38333836)
20. Lee KH, et al. 2006. Interactions between the plasma membrane and the antimicrobial peptide HP (2-20) and its analogues derived from Helicobacter pylori. Biochem. J. 394:105-114. (Pubitemid 43259660)
21. Liu LP, Deber CM. 1998. Uncoupling hydrophobicity and helicity in transmembrane segments. J. Biol. Chem. 273:23645-23648.
22. Liu Z, et al. 2007. Length effects in antimicrobial peptides of the (RW)n series. Antimicrob. Agents Chemother. 51:597-603. (Pubitemid 46185278)
23. Ma Q-Q, et al. 2011. Cell selectivity and interaction with model membranes of Val/Arg-rich peptides. J. Pept. Sci. 17:520-526.
24. Mani R, Cady SD, Tang M, AJ-Waring Lehrer RI, Hong M. 2006. Membrane-dependent oligomeric structure and pore formation of a β-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc. Natl. Acad. Sci. U. S. A. 103:16242-16247. (Pubitemid 44715181)
25. Niidome T, Matsuyama N, Kunihara M, Hatakeyama T, Aoyagi H. 2005. Effect of chain length of cationic model peptides on antibacterial activity. Bull. Chem. Soc. Jpn. 78:473-476. (Pubitemid 40487625)
26. Papanastasiou EA, et al. 2009. Role of acetylation and charge in antimicrobial peptides based on human β-defensin-3. APMIS 117:492- 499.
27. 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. (Pubitemid 28419934)
28. Park Y, Kim HJ, Hahm K-S. 2004. Antibacterial synergism of novel antibiotic peptides with chloramphenicol. Biochem. Biophys. Res. Commun. 321:109-115. (Pubitemid 39055612)
29. Piers KL, Brown MH, Hancock REW. 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. (Pubitemid 24304222)
30. Ragothama SR, Awasthi SK, Balaram P. 1998. β-Hairpin nucleation by Pro-Gly β-turns. Comparison of D-Pro-Gly and L-Pro-Gly sequences in an apolar octapeptide. J. Chem. Soc. Perk. 2:137-143. (Pubitemid 128434869)
31. Rodríguez A, Villegas E, Satake H, Possani LD, Corzo G. 2011. Amino acid substitutions in an alpha-helical antimicrobial arachnid peptide affect its chemical properties and biological activity towards pathogenic bacteria but improves its therapeutic index. Amino Acids 40:61- 68.
32. Rost B, Sander C. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55-72. (Pubitemid 24151484)
33. Schmidt NW, et al. 2011. Criterion for amino acid composition of defensins and antimicrobial peptides based on geometry of membrane destabilization. J. Am. Chem. Soc. 133:6720-6727.
34. Sedgwick EG, Bragg PD. 1987. Distinct phases of the fluorescence response of the lipophilic probe N-phenyl-1-naphthylamine in intact cells and membrane vesicles of Escherichia coli. Biochim. Biophys. Acta 894: 499-506.
35. Shenkarev ZO, et al. 2011. Molecular mechanism of action of β-hairpin antimicrobial peptide arenicin: oligomeric structure in DPC micelles and pore formation in planar lipid bilayers. Biochemistry 50:6255-6265.
36. Shepherd CM, Schaus KA, Vogel HJ, Juffer AH. 2001. Molecular dynamics study of peptide-bilayer adsorption. Biophys. J. 80:579-596. (Pubitemid 32128313)
37. Smith CK, Withka JM, Regan L. 1994. A thermodynamic scale for the beta-sheet forming tendencies of the amino acids. Biochemistry 33:5510-5517.
38. Stanger HE, et al. 2001. Length-dependent stability and strand length limits in antiparallel β-sheet secondary structure. Proc. Natl. Acad. Sci. U. S. A. 98:12015-12020. (Pubitemid 32959818)
39. Stanger HE, Gellman SH. 1998. Rules for antiparallel β-sheet design: D-Pro-Gly is superior to L-Asn-Gly for β-hairpin nucleation. J. Am. Chem. Soc. 120:4236-4237.
40. Stark M, Liu L, Deber CM. 2002. Cationic hydrophobic peptides with antimicrobial activity. Antimicrob. Agents Chemother. 46:3585-3590. (Pubitemid 35192930)
41. Syud FA, Espinosa JF, Gellman SH. 1999. NMR-based quantification of β-sheet populations in aqueous solution through use of reference peptides for the folded and unfolded states. J. Am. Chem. Soc. 121:11577-11578. (Pubitemid 30010494)
42. Tang M, Waring AJ, Hong M. 2009. Effects of arginine density on the membrane-bound structure of a cationic antimicrobial peptide from solid-state NMR. Biochim. Biophys. Acta 1788:514-521.
43. Tang M, Hong M. 2009. Structure and mechanism of beta-hairpin antimicrobial peptides in lipid bilayers from solid-state NMR spectroscopy. Mol. Biosyst. 5:317-322.
44. Varkey J, Nagaraj R. 2005. Antibacterial activity of human neutrophil defensin HNP-1 analogs without cysteines. Antimicrob. Agents Chemother. 49:4561-4566. (Pubitemid 41552585)
45. Vogel HJ, et al. 2002. Towards a structure-function analysis of bovine lactoferricin and related tryptophan-and arginine-containing peptides. Biochem. Cell Biol. 80:49-63. (Pubitemid 34194228)
46. 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. (Pubitemid 32783588)
47. Zhu WL, et al. 2006. Design and mechanism of action of a novel bacteriaselective antimicrobial peptide from the cell-penetrating peptide Pep-1. Biochem. Bioph. Res. Co. 349:769-774. (Pubitemid 44344580)