What goes around comes around-A comparative study of the influence of chemical modifications on the antimicrobial properties of small cyclic peptides

Pharmaceuticals

Volumn 6, Issue 9, 2013, Pages 1130-1144

  Scheinpflug, Kathi ^a   Nikolenko, Heike ^a   Komarov, Igor V ^b   Rautenbach, Marina ^c   Dathe, Margitta ^a  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Antimicrobial activity; Chemical modification; Cyclic hexapeptides; Mode of action; Permeabilisation

Indexed keywords

ANTIINFECTIVE AGENT; CYCLO ARGINYLARGINYLARGINYLTRYPTOPHAN(ALANINE COUMARIN)TRYPTOPHAN; CYCLO ARGINYLARGINYLARGINYLTRYPTOPHAN(CYSTEINE BROMOHYDROXYCOUMARIN)TRYPTOPHAN; CYCLO ARGINYLARGINYLARGINYLTRYPTOPHAN(DIAMINOPROPIONIC ACID NITROBENZOXADIAZOLE)TRYPTOPHAN; CYCLO ARGINYLARGINYLARGINYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; CYCLO ARGINYLARGINYLARGINYLTRYPTOPHANYLTRYPTOPHANYLLYSINE CARBOXYFLUORESCEIN; CYCLO ARGINYLARGINYLTRYPTOPHANYLTRYPTOPHANYLTRYPTOPHANYLLYSINE CARBOXYFLUORESCEIN; CYCLO ARGINYLLYSYLARGINYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; CYCLO ARGINYLLYSYLLYSYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; CYCLO LYSYLARGINYLLYSYLTRYPTOPHAN(ALANINE COUMARIN)TRYPTOPHAN; CYCLO LYSYLARGINYLLYSYLTRYPTOPHAN(CYSTEINE BROMOHYDROXYCOUMARIN)TRYPTOPHAN; CYCLO LYSYLARGINYLLYSYLTRYPTOPHAN(DIAMINOPROPIONIC ACID NITROBENZOXADIAZOLE)TRYPTOPHAN; CYCLO LYSYLARGINYLLYSYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; CYCLO LYSYLLYSYLARGINYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; CYCLO LYSYLLYSYLLYSYLTRYPTOPHANYLPHENYLALANYLTRYPTOPHAN; KLA 1 PEPTIDE; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; CHEMICAL MODIFICATION; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG STRUCTURE; HUMAN; HUMAN CELL; HYDROPHOBICITY; NONHUMAN; PROTEIN CONFORMATION; STRUCTURE ANALYSIS;

EID: 84884409922     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph6091130     Document Type: Article

References (39)

1. Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24, 1551-1557.
2. Dathe, M.; Wieprecht, T.; Nikolenko, H.; Handel, L.; Maloy, W.L.; MacDonald, D.L.; Beyermann, M.; Bienert, M. Hydrophobicity, hydrophobic moment and angle subtended by charged residues modulate antibacterial and haemolytic activity of amphipathic helical peptides. FEBS Lett. 1997, 403, 208-212.
3. Nicolas, P. Multifunctional host defense peptides: Intracellular-targeting antimicrobial peptides. FEBS J. 2009, 276, 6483-6496.
4. Wimley, W.C. Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem. Biol. 2010, 5, 905-917.
5. Brogden, K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250.
6. Epand, R.M.; Epand, R.F. Bacterial membrane lipids in the action of antimicrobial agents. J. Pept. Sci. 2011, 17, 298-305.
7. Dathe, M.; Nikolenko, H.; Klose, J.; Bienert, M. Cyclization increases the antimicrobial activity and selectivity of arginine- and tryptophan-containing hexapeptides. Biochemistry 2004, 43, 9140-9150.
8. Junkes, C.; Harvey, R.D.; Bruce, K.D.; Dolling, R.; Bagheri, M.; Dathe, M. Cyclic antimicrobial R-, W-rich peptides: The role of peptide structure and E. coli outer and inner membranes in activity and the mode of action. Eur. Biophys. J. 2011, 40, 515-528.
9. Wells, S.; Johnson, I. Fluorescent Labels for Confocal Microscopy. In Three-Dimensional Confocal Microscopy: Volume Investigation of Biological Specimens; Academic Press: London, UK, 1994; pp. 101-129.
10. Lattig-Tunnemann, G.; Prinz, M.; Hoffmann, D.; Behlke, J.; Palm-Apergi, C.; Morano, I.; Herce, H.D.; Cardoso, M.C. Backbone rigidity and static presentation of guanidinium groups increases cellular uptake of arginine-rich cell-penetrating peptides. Nat. Commun. 2011, 2, 453.
11. Oehlke, J.; Scheller, A.; Wiesner, B.; Krause, E.; Beyermann, M.; Klauschenz, E.; Melzig, M.; Bienert, M. Cellular uptake of an alpha-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically. Biochim. Biophys. Acta 1998, 1414, 127-139.
12. Hagen, V.; Kilic, F.; Schaal, J.; Dekowski, B.; Schmidt, R.; Kotzur, N. [8-[Bis(carboxymethyl) aminomethyl]-6-bromo-7-hydroxycoumarin-4-yl]methyl moieties as photoremovable protecting groups for compounds with COOH, NH2, OH, and C=O functions. J. Org. Chem. 2010, 75, 2790-2797.
13. Madani, F.; Abdo, R.; Lindberg, S.; Hirose, H.; Futaki, S.; Langel, U.; Graslund, A. Modeling the endosomal escape of cell-penetrating peptides using a transmembrane pH gradient. Biochim. Biophys. Acta 2013, 1828, 1198-1204.
14. Chan, W.; White, P. Fmoc Solid Phase Peptide Synthesis-A Practical Approach; Oxford University Press: Oxford, UK, 1999; p. 370.
15. Pearson, D.A.; Blanchette, M.; Baker, M.L.; Guindon, C.A. Trialkylsilanes as scavengers for the trifluoroacetic acid deblocking of protecting groups in peptide synthesis. Tetrahedron Lett. 1989, 30, 2739-2742.
16. Ehrlich, A.; Heyne, H.U.; Winter, R.; Beyermann, M.; Haber, H.; Carpino, L.A.; Bienert, M. Cyclization of all-l-pentapeptides by means of 1-hydroxy-7-azabenzotriazole-derived uronium and phosphonium reagents. J. Org. Chem. 1996, 61, 8831-8838.
17. Dathe, M.; Schumann, M.; Wieprecht, T.; Winkler, A.; Beyermann, M.; Krause, E.; Matsuzaki, K.; Murase, O.; Bienert, M. Peptide helicity and membrane surface charge modulate the balance of electrostatic and hydrophobic interactions with lipid bilayers and biological membranes. Biochemistry 1996, 35, 12612-12622.
18. Dathe, M.; Meyer, J.; Beyermann, M.; Maul, B.; Hoischen, C.; Bienert, M. General aspects of peptide selectivity towards lipid bilayers and cell membranes studied by variation of the structural parameters of amphipathic helical model peptides. Biochim. Biophys. Acta 2002, 1558, 171-186.
19. Lindgren, M.; Gallet, X.; Soomets, U.; Hallbrink, M.; Brakenhielm, E.; Pooga, M.; Brasseur, R.; Langel, U. Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjugate Chem. 2000, 11, 619-626.
20. Oehlke, J.; Savoly, B.; Blasig, I.E. Utilization of endothelial cell monolayers of low tightness for estimation of transcellular transport characteristics of hydrophilic compounds. Eur. J. Pharm. Sci. 1994, 2, 365-372.
21. Dansen, T.B.; Pap, E.H.W.; Wanders, R.J.; Wirtz, K.W. Targeted fluorescent probes in peroxisome function. Histochem. J. 2001, 33, 65-69.
22. Junkes, C.; Wessolowski, A.; Farnaud, S.; Evans, R.W.; Good, L.; Bienert, M.; Dathe, M. The interaction of arginine- and tryptophan-rich cyclic hexapeptides with Escherichia coli membranes. J. Pept. Sci. 2008, 14, 535-543.
23. Wessolowski, A.; Bienert, M.; Dathe, M. Antimicrobial activity of arginine- and tryptophan-rich hexapeptides: The effects of aromatic clusters, D-amino acid substitution and cyclization. J. Pept. Res. 2004, 64, 159-169.
24. Dathe, M.; Wieprecht, T. Structural features of helical antimicrobial peptides: Their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta 1999, 1462, 71-87.
25. Kondejewski, L.H.; Jelokhani-Niaraki, M.; Farmer, S.W.; Lix, B.; Kay, C.M.; Sykes, B.D.; Hancock, R.E.; Hodges, R.S. Dissociation of antimicrobial and hemolytic activities in cyclic peptide diastereomers by systematic alterations in amphipathicity. J. Biol. Chem. 1999, 274, 13181-13192.
26. Bagheri, M.; Keller, S.; Dathe, M. Interaction of W-substituted analogs of cyclo-RRRWFW with bacterial lipopolysaccharides: The role of the aromatic cluster in antimicrobial activity. Antimicrob. Agents Chemother. 2011, 55, 788-797.
27. Radchenko, D.S.; Michurin, O.M.; Grygorenko, O.O.; Scheinpflug, K.; Dathe, M.; Komarov, I.V. Confining the χ space of basic natural amino acids: Cyclobutane-derived χ1,χ2-constrained analogues of arginine, lysine and ornithine. Tetrahedron 2013, 69, 505-511.
28. Dennison, S.R.; Wallace, J.; Harris, F.; Phoenix, D.A. Amphiphilic alpha-helical antimicrobial peptides and their structure/function relationships. Protein Pept. Lett. 2005, 12, 31-39.
29. Spathelf, B.M.; Rautenbach, M. Anti-listerial activity and structure-activity relationships of the six major tyrocidines, cyclic decapeptides from Bacillus aneurinolyticus. Bioorg. Med. Chem. 2009, 17, 5541-5548.
30. Marques, M.A.; Citron, D.M.; Wang, C.C. Development of Tyrocidine A analogues with improved antibacterial activity. Bioorg. Med. Chem. 2007, 15, 6667-6677.
31. Appelt, C.; Wessolowski, A.; Soderhall, J.A.; Dathe, M.; Schmieder, P. Structure of the antimicrobial, cationic hexapeptide cyclo(RRWWRF) and its analogues in solution and bound to detergent micelles. Chembiochem 2005, 6, 1654-1662.
32. Woody, R.W. Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins. Eur. Biophys. J. 1994, 23, 253-262.
33. Appelt, C.; Wessolowski, A.; Dathe, M.; Schmieder, P. Structures of cyclic, antimicrobial peptides in a membrane-mimicking environment define requirements for activity. J. Pept. Sci. 2008, 14, 524-527.
34. Scheller, A.; Oehlke, J.; Wiesner, B.; Dathe, M.; Krause, E.; Beyermann, M.; Melzig, M.; Bienert, M. Structural requirements for cellular uptake of alpha-helical amphipathic peptides. J. Pept. Sci. 1999, 5, 185-194.
35. Mercier, R.; Domínguez-Cuevas, P.; Errington, J. Crucial role for membrane fluidity in proliferation of primitive cells. Cell Rep. 2012, 1, 417-423.
36. Epand, R.M.; Epand, R.F. Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim. Biophys. Acta (BBA) Biomembr. 2009, 1788, 289-294.
37. Eun, Y.J.; Zhou, M.; Kiekebusch, D.; Schlimpert, S.; Trivedi, R.R.; Bakshi, S.; Zhong, Z.; Wahlig, T.A.; Thanbichler, M.; Weibel, D.B. Divin: A small molecule inhibitor of bacterial divisome assembly. J. Am. Chem. Soc. 2013, 135, 9768-9776.
38. Thanbichler, M. Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harb. Perspect. Biol. 2010, 2, a000331.
39. Ferullo, D.J.; Cooper, D.L.; Moore, H.R.; Lovett, S.T. Cell cycle synchronization of Escherichia coli using the stringent response, with fluorescence labeling assays for DNA content and replication. Methods 2009, 48, 8-13.