Investigating the cationic side chains of the antimicrobial peptide tritrpticin: Hydrogen bonding properties govern its membrane-disruptive activities

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 9, 2011, Pages 2297-2303

  Nguyen, Leonard T ^a   De Boer, Leonie ^b   Zaat, Sebastian A J ^b   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Antimicrobial peptide; Arginine; Cathelicidin; Hydrogen bonding; Membrane active peptide; Tritrpticin

Indexed keywords

ARGININE; CATHELICIDIN; CATION; GUANIDINE; LYSINE DERIVATIVE; PHOSPHOLIPID; POLYPEPTIDE ANTIBIOTIC AGENT; TRITRPTICIN; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERICIDAL ACTIVITY; CELL MEMBRANE PERMEABILITY; DRUG DESIGN; HEMOLYSIS; HUMAN; HUMAN CELL; HYDROGEN BOND; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; STRUCTURE ACTIVITY RELATION;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ARGININE; BACILLUS SUBTILIS; CATIONS; ERYTHROCYTES; ESCHERICHIA COLI; GUANIDINE; HEMOLYSIS; HUMANS; HYDROGEN BONDING; LYSINE; MEMBRANES; METHYLATION; OLIGOPEPTIDES; PEPTIDES; SPECTROMETRY, FLUORESCENCE; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS);

EID: 79959936150     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.05.015     Document Type: Article

References (44)

1. B.N. Ames Assay of inorganic phosphate, total phosphate and phosphatases Methods Enzymol. 8 1966 115 118
2. S.E. Blondelle, and R.A. Houghten Novel antimicrobial compounds identified using synthetic combinatorial library technology Trends Biotechnol. 14 1996 60 65 (Pubitemid 26056343)
3. D.I. Chan, E.J. Prenner, and H.J. Vogel Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action Biochim. Biophys. Acta 1758 2006 1184 1202 (Pubitemid 44444830)
4. M.R. de Planque, B.B. Bonev, J.A. Demmers, D.V. Greathouse, R.E. Koeppe II, and F. Separovic Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions Biochemistry 42 2003 5341 5348 (Pubitemid 36560430)
5. R.M. Epand, and R.F. Epand Lipid domains in bacterial membranes and the action of antimicrobial agents Biochim. Biophys. Acta 1788 2009 289 294
6. R.M. Epand, R.F. Epand, C.J. Arnusch, B. Papahadjopoulos-Sternberg, G. Wang, and Y. Shai Lipid clustering by three homologous arginine-rich antimicrobial peptides is insensitive to amino acid arrangement and induced secondary structure Biochim. Biophys. Acta 1798 2010 1272 1280
7. R. Halevy, A. Rozek, S. Kolusheva, R.E. Hancock, and R. Jelinek Membrane binding and permeation by indolicidin analogs studied by a biomimetic lipid/polydiacetylene vesicle assay Peptides 24 2003 1753 1761 (Pubitemid 38198082)
8. B.E. Haug, W. Stensen, M. Kalaaji, O. Rekdal, and J.S. Svendsen Synthetic antimicrobial peptidomimetics with therapeutic potential J. Med. Chem. 51 2008 4306 4314 (Pubitemid 352032455)
9. J.C. Hsu, and C.M. Yip Molecular dynamics simulations of indolicidin association with model lipid bilayers Biophys. J. 92 2007 L100 L102
10. R.E. Isaacson MBI-226. Micrologix/Fujisawa Curr. Opin. Investig. Drugs 4 2003 999 1003
11. W. Jing, A.R. Demcoe, and H.J. Vogel Conformation of a bactericidal domain of puroindoline a: structure and mechanism of action of a 13-residue antimicrobial peptide J. Bacteriol. 185 2003 4938 4947 (Pubitemid 36962302)
12. J. Krijgsveld, S.A. Zaat, J. Meeldijk, P.A. van Veelen, G. Fang, and B. Poolman Thrombocidins, microbicidal proteins from human blood platelets, are C-terminal deletion products of CXC chemokines J. Biol. Chem. 275 2000 20374 20381 (Pubitemid 30457613)
13. R.I. Lehrer, A. Barton, K.A. Daher, S.S. Harwig, T. Ganz, and M.E. Selsted Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity J. Clin. Invest. 84 1989 553 561 (Pubitemid 19196987)
14. B. Liu, and E. Wilson The antimicrobial activity of CCL28 is dependent on C-terminal positively-charged amino acids Eur. J. Immunol. 40 2010 186 196
15. R.A. Llenado, C.S. Weeks, M.J. Cocco, and A.J. Ouellette Electropositive charge in alpha-defensin bactericidal activity: functional effects of Lys-for-Arg substitutions vary with the peptide primary structure Infect. Immun. 77 2009 5035 5043
16. K. Lohner The role of membrane lipid composition in cell targeting of antimicrobial peptides K. Lohner, Development of Novel Antimicrobial Agents: Emerging Strategies 2001 Horizon Scientific Press Wymondham, UK 149 165
17. D.J. Mandell, I. Chorny, E.S. Groban, S.E. Wong, E. Levine, and C.S. Rapp Strengths of hydrogen bonds involving phosphorylated amino acid side chains J. Am. Chem. Soc. 129 2007 820 827 (Pubitemid 46183932)
18. K. Matsuzaki, O. Murase, N. Fujii, and K. Miyajima An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation Biochemistry 35 1996 11361 11368 (Pubitemid 26299310)
19. J. Mavri, and H.J. Vogel Ion pair formation of phosphorylated amino acids and lysine and arginine side chains: a theoretical study Proteins 24 1996 495 501 (Pubitemid 26122062)
20. M.N. Melo, D. Dugourd, and M.A. Castanho Omiganan pentahydrochloride in the front line of clinical applications of antimicrobial peptides Recent Pat. Antiinfect. Drug Discov. 1 2006 201 207
21. J. Pimthon, R. Willumeit, A. Lendlein, and D. Hofmann Membrane association and selectivity of the antimicrobial peptide NK-2: a molecular dynamics simulation study J. Pept. Sci. 15 2009 654 667
22. T.L. Pukala, M.P. Boland, J.D. Gehman, L. Kuhn-Nentwig, F. Separovic, and J.H. Bowie Solution structure and interaction of cupiennin 1a, a spider venom peptide, with phospholipid bilayers Biochemistry 46 2007 3576 3585 (Pubitemid 46449174)
23. A. Rozek, C.L. Friedrich, and R.E. Hancock Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles Biochemistry 39 2000 15765 15774 (Pubitemid 32040945)
24. T.S. Ryge, X. Doisy, D. Ifrah, J.E. Olsen, and P.R. Hansen New indolicidin analogues with potent antibacterial activity J. Pept. Res. 64 2004 171 185 (Pubitemid 39446659)
25. D.J. Schibli, R.F. Epand, H.J. Vogel, and R.M. Epand Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions Biochem. Cell Biol. 80 2002 667 677 (Pubitemid 36124825)
26. D.J. Schibli, P.M. Hwang, and H.J. Vogel Structure of the antimicrobial peptide tritrpticin bound to micelles: a distinct membrane-bound peptide fold Biochemistry 38 1999 16749 16755
27. D.J. Schibli, L.T. Nguyen, S.D. Kernaghan, O. Rekdal, and H.J. Vogel Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures Biophys. J. 91 2006 4413 4426 (Pubitemid 44904228)
28. D. Seebach, A.K. Beck, and D.J. Bierbaum The world of beta- and gamma-peptides comprised of homologated proteinogenic amino acids and other components Chem. Biodivers. 1 2004 1111 1239
29. M.E. Selsted, M.J. Novotny, W.L. Morris, Y.Q. Tang, W. Smith, and J.S. Cullor Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils J. Biol. Chem. 267 1992 4292 4295
30. K.S. Shashidhara, and S.M. Gaikwad Fluorescence quenching and time-resolved fluorescence studies of alpha-mannosidase from Aspergillus fischeri (NCIM 508) J. Fluoresc. 17 2007 599 605 (Pubitemid 350075675)
31. L.A. Stevens, R.L. Levine, B.R. Gochuico, and J. Moss ADP-ribosylation of human defensin HNP-1 results in the replacement of the modified arginine with the noncoded amino acid ornithine Proc. Natl. Acad. Sci. U. S. A. 106 2009 19796 19800
32. M.B. Strom, O. Rekdal, and J.S. Svendsen Antimicrobial activity of short arginine- and tryptophan-rich peptides J. Pept. Sci. 8 2002 431 437
33. J. Svenson, B.O. Brandsdal, W. Stensen, and J.S. Svendsen Albumin binding of short cationic antimicrobial micropeptides and its influence on the in vitro bactericidal effect J. Med. Chem. 50 2007 3334 3339 (Pubitemid 47065982)
34. D. Takahashi, S.K. Shukla, O. Prakash, and G. Zhang Structural determinants of host defense peptides for antimicrobial activity and target cell selectivity Biochimie 92 2010 1236 1241
35. M. Tang, A.J. Waring, and M. Hong Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR J. Am. Chem. Soc. 129 2007 11438 11446 (Pubitemid 47555563)
36. H.J. Vogel, D.J. Schibli, W. Jing, E.M. Lohmeier-Vogel, R.F. Epand, and R.M. Epand Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides Biochem. Cell Biol. 80 2002 49 63 (Pubitemid 34194228)
37. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848 (Pubitemid 26330634)
38. A.S. Woods, and S. Ferre Amazing stability of the arginine-phosphate electrostatic interaction J. Proteome Res. 4 2005 1397 1402 (Pubitemid 41208697)
39. S.T. Yang, S.Y. Shin, K.S. Hahm, and J.I. Kim Different modes in antibiotic action of tritrpticin analogs, cathelicidin-derived Trp-rich and Pro/Arg-rich peptides Biochim. Biophys. Acta 1758 2006 1580 1586 (Pubitemid 44466702)
40. S.T. Yang, S.Y. Shin, C.W. Lee, Y.C. Kim, K.S. Hahm, and J.I. Kim Selective cytotoxicity following Arg-to-Lys substitution in tritrpticin adopting a unique amphipathic turn structure FEBS Lett. 540 2003 229 233 (Pubitemid 36398062)
41. A. Zairi, F. Tangy, K. Bouassida, and K. Hani Dermaseptins and magainins: antimicrobial peptides from frogs' skin-new sources for a promising spermicides microbicides - a mini review J. Biomed. Biotechnol. 2009 2009 452567
42. M. Zanetti Cathelicidins, multifunctional peptides of the innate immunity J. Leukoc. Biol. 75 2004 39 48 (Pubitemid 38166778)
43. W.L. Zhu, K.S. Hahm, and S.Y. Shin Cathelicidin-derived Trp/Pro-rich antimicrobial peptides with lysine peptoid residue (Nlys): therapeutic index and plausible mode of action J. Pept. Sci. 13 2007 529 535 (Pubitemid 47322352)
44. G. Zou, E. de Leeuw, C. Li, M. Pazgier, C. Li, and P. Zeng Toward understanding the cationicity of defensins. Arg and Lys versus their noncoded analogs J. Biol. Chem. 282 2007 19653 19665 (Pubitemid 47100066)