Engineering of a linear inactive analog of human β-defensin 4 to generate peptides with potent antimicrobial activity

Journal of Peptide Science

Volumn 21, Issue 6, 2015, Pages 501-511

  Sharma, Himanshu ^a   Mathew, Basil ^a   Nagaraj, Ramakrishnan ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

antimicrobial activity; d amino acids; defensins; microbial membranes; myristoylation; salt sensitivity

Indexed keywords

2 AMINO 2 METHYLPROPIONIC ACID; ARGININE; BETA DEFENSIN 4; CYSTEINE; DEXTRO ARGININE; MYRISTIC ACID; ANTIINFECTIVE AGENT; BETA DEFENSIN; DEFB4A PROTEIN, HUMAN; PEPTIDE;

AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIAL TRANSLOCATION; CANDIDA ALBICANS; CELL DEATH; CELL PERMEABILIZATION; CYTOPLASM; DRUG DESIGN; DRUG POTENCY; DRUG SYNTHESIS; ESCHERICHIA COLI; HYDROPHOBICITY; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; ZETA POTENTIAL; BIOMEDICAL ENGINEERING; CHEMISTRY; DRUG EFFECTS; GRAM NEGATIVE BACTERIUM; HUMAN; METABOLISM;

BACTERIA (MICROORGANISMS); CANDIDA ALBICANS;

AMINOISOBUTYRIC ACIDS; ANTI-INFECTIVE AGENTS; ARGININE; BETA-DEFENSINS; BIOMEDICAL ENGINEERING; CANDIDA ALBICANS; GRAM-NEGATIVE BACTERIA; HUMANS; MYRISTIC ACID; PEPTIDES;

EID: 84929584010     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.2770     Document Type: Article

References (46)

1. Ganz T,. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 2003; 3: 710-720.
2. Lehrer RI,. Primate defensins. Nat. Rev. Microbiol. 2004; 2: 727-738.
3. Selsted ME, Ouellette AJ,. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 2005; 6: 551-557.
4. Lehrer RI, Ganz T,. Defensins of vertebrate animals. Curr. Opin. Immunol. 2002; 14: 96-102.
5. Schneider JJ, Unholzer A, Schaller M, Schafer-Korting M, Korting HC,. Human defensins. J. Mol. Med. (Berl) 2005; 83: 587-595.
6. Pazgier M, Hoover DM, Yang D, Lu W, Lubkowski J,. Human beta-defensins. Cell. Mol. Life Sci. 2006; 63: 1294-1313.
7. Goldman MJ, Anderson GM, Stolzenberg ED, Kari UP, Zasloff M, Wilson JM,. Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 1997; 88: 553-560.
8. Bals R, Wang X, Wu Z, Freeman T, Bafna V, Zasloff M, Wilson JM,. Human beta-defensin 2 is a salt-sensitive peptide antibiotic expressed in human lung. J. Clin. Invest. 1998; 102: 874-880.
9. Tomita T, Hitomi S, Nagase T, Matsui H, Matsuse T, Kimura S, Ouchi Y,. Effect of ions on antibacterial activity of human beta defensin 2. Microbiol. Immunol. 2000; 44: 749-754.
10. Hoover DM, Wu Z, Tucker K, Lu W, Lubkowski J,. Antimicrobial characterization of human beta-defensin 3 derivatives. Antimicrob. Agents Chemother. 2003; 47: 2804-2809.
11. Wu Z, Hoover DM, Yang D, Boulegue C, Santamaria F, Oppenheim JJ, Lubkowski J, Lu W,. Engineering disulfide bridges to dissect antimicrobial and chemotactic activities of human beta-defensin 3. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 8880-8885.
12. Maemoto A, Qu X, Rosengren KJ, Tanabe H, Henschen-Edman A, Craik DJ, Ouellette AJ,. Functional analysis of the alpha-defensin disulfide array in mouse cryptdin-4. J. Biol. Chem. 2004; 279: 44188-44196.
13. Kluver E, Schulz-Maronde S, Scheid S, Meyer B, Forssmann WG, Adermann K,. Structure-activity relation of human beta-defensin 3: influence of disulfide bonds and cysteine substitution on antimicrobial activity and cytotoxicity. Biochemistry 2005; 44: 9804-9816.
14. Taylor K, McCullough B, Clarke DJ, Langley RJ, Pechenick T, Hill A, Campopiano DJ, Barran PE, Dorin JR, Govan JR,. Covalent dimer species of beta-defensin Defr1 display potent antimicrobial activity against multidrug-resistant bacterial pathogens. Antimicrob. Agents Chemother. 2007; 51: 1719-1724.
15. Varkey J, Nagaraj R,. Antibacterial activity of human neutrophil defensin HNP-1 analogs without cysteines. Antimicrob. Agents Chemother. 2005; 49: 4561-4566.
16. Sharma H, Nagaraj R,. Antimicrobial activity of human beta-defensin 4 analogs: insights into the role of disulfide linkages in modulating activity. Peptides 2012; 38: 255-265.
17. Nagaraj R, Balaram P,. Alamethicin, a transmembrane channel. Acc. Chem. Res. 1981; 14: 356-362.
18. Karle IL, Balaram P,. Structural characteristics of alpha-helical peptide molecules containing Aib residues. Biochemistry 1990; 29: 6747-6756.
19. Zou G, de Leeuw E, Li C, Pazgier M, Zeng P, Lu WY, Lubkowski J, Lu W,. Toward understanding the cationicity of defensins. Arg and Lys versus their noncoded analogs. J. Biol. Chem. 2007; 282: 19653-19665.
20. Schmidt NW, Mishra A, Lai GH, Davis M, Sanders LK, Tran D, Garcia A, Tai KP, McCray PB, Ouellette AJ, Selsted ME, Wong GC,. Criterion for amino acid composition of defensins and antimicrobial peptides based on geometry of membrane destabilization. J. Am. Chem. Soc. 2011; 133: 6720-6727.
21. Schmidt NW, Tai KP, Kamdar K, Mishra A, Lai GH, Zhao K, Ouellette AJ, Wong GC,. Arginine in alpha-defensins: differential effects on bactericidal activity correspond to geometry of membrane curvature generation and peptide-lipid phase behavior. J. Biol. Chem. 2012; 287: 21866-21872.
22. Atherton E, Sheppard RC,. Solid Phase Peptide Synthesis: A Practical Approach, IRL Press: Oxford, 1989.
23. Beekman NJ, Schaaper WM, Tesser GI, Dalsgaard K, Kamstrup S, Langeveld JP, Boshuizen RS, Meloen RH,. Synthetic peptide vaccines: palmitoylation of peptide antigens by a thioester bond increases immunogenicity. J. Pept. Res. 1997; 50: 357-364.
24. Weber PJ, Bader JE, Folkers G, Beck-Sickinger AG,. A fast and inexpensive method for N-terminal fluorescein-labeling of peptides. Bioorg. Med. Chem. Lett. 1998; 8: 597-600.
25. Domingues MM, Santiago PS, Castanho MA, Santos NC,. What can light scattering spectroscopy do for membrane-active peptide studies? J. Pept. Sci. 2008; 14: 394-400.26.
26. Ishitsuka R, Yamaji-Hasegawa A, Makino A, Hirabayashi Y, Kobayashi T,. A lipid-specific toxin reveals heterogeneity of sphingomyelin-containing membranes. Biophys. J. 2004; 86: 296-307.
27. Fishov I, Woldringh CL,. Visualization of membrane domains in Escherichia coli. Mol. Microbiol. 1999; 32: 1166-1172.
28. Roth BL, Poot M, Yue ST, Millard PJ,. Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl. Environ. Microbiol. 1997; 63: 2421-2431.
29. Pham W, Kircher MF, Weissleder R, Tung CH,. Enhancing membrane permeability by fatty acylation of oligoarginine peptides. Chem. Bio. Chem. 2004; 5: 1148-1151.
30. Nelson AR, Borland L, Allbritton NL, Sims CE,. Myristoyl-based transport of peptides into living cells. Biochemistry 2007; 46: 14771-14781.
31. Wilson WW, Wade MM, Holman SC, Champlin FR,. Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J. Microbiol. Methods 2001; 43: 153-164.
32. Fan HY, Nazari M, Raval G, Khan Z, Patel H, Heerklotz H,. Utilizing zeta potential measurements to study the effective charge, membrane partitioning, and membrane permeation of the lipopeptide surfactin. Biochim. Biophys. Acta 1838; 2014: 2306-2312.
33. Alves CS, Melo MN, Franquelim HG, Ferre R, Planas M, Feliu L, Bardají E, Kowalczyk W, Andreu D, Santos NC, Fernandes MX, Castanho MA,. Escherichia coli cell surface perturbation and disruption induced by antimicrobial peptides BP100 and pepR. J. Biol. Chem. 2010; 285: 27536-27544.
34. Ghoul M, Pommepuy M, Moillo-Batt A, Cormier M,. Effect of carbonyl cyanide m-chlorophenylhydrazone on Escherichia coli halotolerance. Appl. Environ. Microbiol. 1989; 55: 1040-1043.
35. Kinoshita N, Unemoto T, Kobayashi H,. Proton motive force is not obligatory for growth of Escherichia coli. J. Bacteriol. 1984; 160: 1074-1077.
36. Ohyama T, Mugikura S, Nishikawa M, Igarashi K, Kobayashi H,. Osmotic adaptation of Escherichia coli with a negligible proton motive force in the presence of carbonyl cyanide m-chlorophenylhydrazone. J. Bacteriol. 1992; 174: 2922-2928.
37. Efe JA, Botelho RJ, Emr SD,. The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology. Curr. Opin. Cell Biol. 2005; 17: 402-408.
38. Woody RW,. Circular dichroism. Methods Enzymol. 1995; 246: 34-71.
39. Olli S, Rangaraj N, Nagaraj R,. Effect of selectively introducing arginine and D-amino acids on the antimicrobial activity and salt sensitivity in analogs of human Beta-defensins. PLoS One 2013; 8: e77031.
40. Scudiero O, Galdiero S, Cantisani M, Di Noto R, Vitiello M, Galdiero M, Naclerio G, Cassiman JJ, Pedone C, Castaldo G, Salvatore F,. Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob. Agents Chemother. 2010; 54: 2312-2322.
41. Jung S, Mysliwy J, Spudy B, Lorenzen I, Reiss K, Gelhaus C, Podschun R, Leippe M, Grötzinger J,. Antimicrob. Agents Chemother. 2011; 55: 954-960.
42. Wieprecht T, Dathe M, Krause E, Beyermann M, Maloy WL, MacDonald DL, Bienert M,. Modulation of membrane activity of amphipathic, antibacterial peptides by slight modifications of the hydrophobic moment. FEBS Lett. 1997; 417: 135-140.
43. Sitaram N, Nagaraj R,. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim. Biophys. Acta 1999; 1462: 29-54.
44. Tossi A, Sandri L, Giangaspero A,. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 2000; 55: 4-30.
45. Saberwal G, Nagaraj R,. Cell-lytic and antibacterial peptides that act by perturbing the barrier function of membranes: facets of their conformational features, structure-function correlations and membrane-perturbing abilities. Biochim. Biophys. Acta 1994; 1197: 109-131.
46. Shai Y,. Mode of action of membrane active antimicrobial peptides. Biopolymers 2002; 66: 236-248.