Evaluation of strategies for improving proteolytic resistance of antimicrobial peptides by using variants of EFK17, an internal segment of LL-37

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 2, 2009, Pages 593-602

  Strömstedt, Adam A ^a   Pasupuleti, Mukesh ^b   Schmidtchen, Artur ^b   Malmsten, Martin ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOLYSIN; BACTERIAL ENZYME; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; EFK 17; ELASTASE; GLUTAMYLPHENYLALANYLLYSYLARGINYLISOLEUCYLVALYLGLUTAMINYLARGINYLISOLEUCYLLYSYLASPARTYLPHENYLALANYLLEUCYLARGINYLASPARAGINYLLEUCYLVALINE; LEUKOCYTE ELASTASE; LIPOSOME; PROTEINASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACETYLATION; AMIDATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIMICROBIAL ACTIVITY; ARTICLE; CYTOTOXICITY; DRUG ADSORPTION; DRUG POTENCY; ENANTIOMER; ENZYME DEGRADATION; IONIC STRENGTH; LIPID MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN VARIANT; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

ACETYLATION; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BUFFERS; CIRCULAR DICHROISM; DRUG RESISTANCE, BACTERIAL; LIPIDS; LIPOSOMES; MEMBRANE LIPIDS; PEPTIDE HYDROLASES; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STEREOISOMERISM;

EID: 59749089160     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00477-08     Document Type: Article

References (68)

1. Andrushchenko, V. V., H. J. Vogel, and E. J. Prenner. 2007. Interactions of tryptophan-rich cathelicidin antimicrobial peptides with model membranes studied by differential scanning calorimetry. Biochim. Biophys. Acta 1768:2447-2458.
2. Belas, R., J. Manos, and R. Suvanasuthi. 2004. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect. Immun. 72:5159-5167.
3. Bessalle, R., A. Kapitkovsky, A. Gorea, I. Shalit, and M. Fridkin. 1990. All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett. 274:151-155.
4. Bjoorklind, A., and H. Jornvall. 1974. Substrate specificity of three different extracellular proteolytic enzymes from Staphylococcus aureus. Biochim. Biophys. Acta 370:524-529.
5. Butterfield, S. M., P. R. Patel, and M. L. Waters. 2002. Contribution of aromatic interactions to alpha-helix stability. J. Am. Chem. Soc. 124:9751-9755.
6. Chan, D. I., E. J. Prenner, and H. J. Vogel. 2006. Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta 1758:1184-1202.
7. Chen, R. F., and J. R. Knutson. 1988. Mechanism of fluorescence concentration quenching of carboxyfluorescein in liposomes: energy transfer to nonfluorescent dimers. Anal. Biochem. 172:61-77.
8. Ciornei, C. D., T. Sigurdardottir, A. Schmidtchen, and M. Bodelsson. 2005. Antimicrobial and chemoattractant activity, lipopolysaccharide neutralization, cytotoxicity, and inhibition by serum of analogs of human cathelicidin LL-37. Antimicrob. Agents Chemother. 49:2845-2850.
9. De Feijter, J. A., J. Benjamins, and F. A. Veer. 1978. Ellipsometry as a tool to study the adsorption behavior of synthetic and biopolymers at the airwater interface. Biopolymers 17:1759-1772.
10. de Kreij, A., G. Venema, and B. van den Burg. 2000. Substrate specificity in the highly heterogeneous M4 peptidase family is determined by a small subset of amino acids. J. Biol. Chem. 275:31115-31120.
11. Dougherty, D. A. 1996. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271:163-168.
12. Drapeau, G. R., Y. Boily, and J. Houmard. 1972. Purification and properties of an extracellular protease of Staphylococcus aureus. J. Biol. Chem. 247:6720-6726.
13. Durr, U. H., U. S. Sudheendra, and A. Ramamoorthy. 2006. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758:1408-1425.
14. Fairman, R., K. R. Shoemaker, E. J. York, J. M. Stewart, and R. L. Baldwin. 1989. Further studies of the helix dipole model: effects of a free alpha-NH3+ or alpha-COO- group on helix stability. Proteins 5:1-7.
15. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. USA 96:9459-9464.
16. Giangaspero, A., L. Sandri, and A. Tossi. 2001. Amphipathic alpha helical antimicrobial peptides. Eur. J. Biochem. 268:5589-5600.
17. Greenfield, N., and G. D. Fasman. 1969. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 8:4108-4116.
18. Gudmundsson, G. H., B. Agerberth, J. Odeberg, T. Bergman, B. Olsson, and R. Salcedo. 1996. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur. J. Biochem. 238:325-332.
19. Guina, T., E. C. Yi, H. Wang, M. Hackett, and S. I. Miller. 2000. A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol. 182:4077-4086.
20. Heilborn, J. D., M. F. Nilsson, G. Kratz, G. Weber, O. Sorensen, N. Borregaard, and M. Stahle-Backdahl. 2003. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Investig. Dermatol. 120:379-389.
21. Hong, S. Y., J. E. Oh, and K. H. Lee. 1999. Effect of D-amino acid substitution on the stability, the secondary structure, and the activity of membraneactive peptide. Biochem. Pharmacol. 58:1775-1780.
22. Hornef, M. W., S. Normark, B. Henriques-Normark, and M. Rhen. 2005. Bacterial evasion of innate defense at epithelial linings. Chem. Immunol. Allergy 86:72-98.
23. Kraus, D., and A. Peschel. 2006. Molecular mechanisms of bacterial resistance to antimicrobial peptides. Curr. Top. Microbiol. Immunol. 306:231-250.
24. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Maillere, B., G. Mourier, M. Herve, and A. Menez. 1995. Fine chemical modifications at N- and C-termini enhance peptide presentation to T cells by increasing the lifespan of both free and MHC-complexed peptides. Mol. Immunol. 32:1377-1385.
27. Mecozzi, S., A. P. West, Jr., and D. A. Dougherty. 1996. Cation-pi interactions in aromatics of biological and medicinal interest: electrostatic potential surfaces as a useful qualitative guide. Proc. Natl. Acad. Sci. USA 93:10566-10571.
28. Nell, M. J., G. S. Tjabringa, A. R. Wafelman, R. Verrijk, P. S. Hiemstra, J. W. Drijfhout, and J. J. Grote. 2006. Development of novel LL-37 derived antimicrobial peptides with LPS and LTA neutralizing and antimicrobial activities for therapeutic application. Peptides 27:649-660.
29. Nizet, V. 2006. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 8:11-26.
30. Olson, C. A., E. J. Spek, Z. Shi, A. Vologodskii, and N. R. Kallenbach. 2001. Cooperative helix stabilization by complex Arg-Glu salt bridges. Proteins 44:123-132.
31. Oren, Z., J. C. Lerman, G. H. Gudmundsson, B. Agerberth, and Y. Shai. 1999. Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem. J. 341(3):501-513.
32. Pauchon, V., C. Besson, J. Saulnier, and J. Wallach. 1993. Peptide synthesis catalysed by Pseudomonas aeruginosa elastase. Biotechnol. Appl. Biochem. 17(2):217-221.
33. Powell, M. F., T. Stewart, L. Otvos, Jr., L. Urge, F. C. Gaeta, A. Sette, T. Arrhenius, D. Thomson, K. Soda, and S. M. Colon. 1993. Peptide stability in drug development. II. Effect of single amino acid substitution and glycosylation on peptide reactivity in human serum. Pharm. Res. 10:1268-1273.
34. Reijmar, K., A. Schmidtchen, and M. Malmsten. 2007. Bactericidal and hemolytic properties of mixed LL-37/surfactant systems. J. Drug Del. Sci. Tech. 17:293-297.
35. Ringstad, L., E. A. Nordahl, A. Schmidtchen, and M. Malmsten. 2007. Composition effect on peptide interaction with lipids and bacteria: variants of C3a peptide CNY21. Biophys. J. 92:87-98.
36. Ringstad, L., L. Kacprzyk, A. Schmidtchen, and M. Malmsten. 2007. Effects of topology, length, and charge on the activity of a kininogen-derived peptide on lipid membranes and bacteria. Biochim. Biophys. Acta 1768:715-727.
37. Ringstad, L., E. Protopapa, B. Lindholm-Sethson, A. Schmidtchen, A. Nelson, and M. Malmsten. 2008. An electrochemical study into the interaction between complement-derived peptides and DOPC mono- and bilayers. Langmuir 24:208-216.
38. Ringstad, L., A. Schmidtchen, and M. Malmsten. 2006. Effect of peptide length on the interaction between consensus peptides and DOPC/DOPA bilayers. Langmuir 22:5042-5050.
39. Ruissen, A. L., J. Groenink, P. Krijtenberg, E. Walgreen-Weterings, W. van't Hof, E. C. Veerman, and A. V. N. Amerongen. 2003. Internalisation and degradation of histatin 5 by Candida albicans. Biol. Chem. 384:183-190.
40. Sal-Man, N., D. Gerber, I. Bloch, and Y. Shai. 2007. Specificity in transmembrane helix-helix interactions mediated by aromatic residues. J. Biol. Chem. 282:19753-19761.
41. Schellenberger, V., C. W. Turck, L. Hedstrom, and W. J. Rutter. 1993. Mapping the S′ subsites of serine proteases using acyl transfer to mixtures of peptide nucleophiles. Biochemistry 32:4349-4353.
42. Schellenberger, V., C. W. Turck, and W. J. Rutter. 1994. Role of the S′ subsites in serine protease catalysis. Active-site mapping of rat chymotrypsin, rat trypsin, alpha-lytic protease, and cercarial protease from Schistosoma mansoni. Biochemistry 33:4251-4257.
43. Schmidtchen, A., I. M. Frick, E. Andersson, H. Tapper, and L. Bjorck. 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46:157-168.
44. Serrano, L., M. Bycroft, and A. R. Fersht. 1991. Aromatic-aromatic interactions and protein stability. Investigation by double-mutant cycles. J. Mol. Biol. 218:465-475.
45. Shalev, D. E., A. Mor, and I. Kustanovich. 2002. Structural consequences of carboxyamidation of dermaseptin S3. Biochemistry 41:7312-7317.
46. Shi, Z., C. A. Olson, and N. R. Kallenbach. 2002. Cation-pi interaction in model alpha-helical peptides. J. Am. Chem. Soc. 124:3284-3291.
47. Sieprawska-Lupa, M., P. Mydel, K. Krawczyk, K. Wojcik, M. Puklo, B. Lupa, P. Suder, J. Silberring, M. Reed, J. Pohl, W. Shafer, F. McAleese, T. Foster, J. Travis, and J. Potempa. 2004. Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob. Agents Chemother. 48:4673-4679.
48. Sigurdardottir, T., P. Andersson, M. Davoudi, M. Malmsten, A. Schmidtchen, and M. Bodelsson. 2006. In silico identification and biological evaluation of antimicrobial peptides based on human cathelicidin LL-37. Antimicrob. Agents Chemother. 50:2983-2989.
49. Sjogren, H., and S. Ulvenlund. 2005. Comparison of the helix-coil transition of a titrating polypeptide in aqueous solutions and at the air-water interface. Biophys. Chem. 116:11-21.
50. Smith, J. S., and J. M. Scholtz. 1998. Energetics of polar side-chain interactions in helical peptides: salt effects on ion pairs and hydrogen bonds. Biochemistry 37:33-40.
51. Sonesson, A., L. Ringstad, E. A. Nordahl, M. Malmsten, M. Morgelin, and A. Schmidtchen. 2007. Antifungal activity of C3a and C3a-derived peptides against Candida. Biochim. Biophys. Acta 1768:346-353.
52. Sorensen, O., K. Arnljots, J. B. Cowland, D. F. Bainton, and N. Borregaard. 1997. The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils. Blood 90:2796-2803.
53. Stromstedt, A. A., P. Wessman, L. Ringstad, K. Edwards, and M. Malmsten. 2007. Effect of lipid headgroup composition on the interaction between melittin and lipid bilayers. J. Colloid Interface Sci. 311:59-69.
54. Tiberg, F., I. Harwigsson, and M. Malmsten. 2000. Formation of model lipid bilayers at the silica-water interface by co-adsorption with non-ionic dodecyl maltoside surfactant. Eur. Biophys. J. 29:196-203.
55. Tossi, A., L. Sandri, and A. Giangaspero. 2002. New consensus hydropathy scale extended to non-proteinogenic amino acids, p. 416-417. In Peptides 2002: Proceedings of the Twenty-Seventh European Peptide Symposium. Edizioni Ziino, Naples, Italy.
56. Travis, J., J. Potempa, and H. Maeda. 1995. Are bacterial proteinases pathogenic factors? Trends Microbiol. 3:405-407.
57. Travis, S. M., N. N. Anderson, W. R. Forsyth, C. Espiritu, B. D. Conway, E. P. Greenberg, P. B. McCray, Jr., R. I. Lehrer, M. J. Welsh, and B. F. Tack. 2000. Bactericidal activity of mammalian cathelicidin-derived peptides. Infect. Immun. 68:2748-2755.
58. Turner, J., Y. Cho, N.-N. Dinh, A. J. Waring, and R. I. Lehrer. 1998. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42:2206-2214.
59. Vacklin, H. P., F. Tiberg, and R. K. Thomas. 2005. Formation of supported phospholipid bilayers via co-adsorption with beta-D-dodecyl maltoside. Biochim. Biophys. Acta 1668:17-24.
60. Wade, D., A. Boman, B. Wahlin, C. M. Drain, D. Andreu, H. G. Boman, and R. B. Merrifield. 1990. All-D amino acid-containing channel-forming antibiotic peptides. Proc. Natl. Acad. Sci. USA 87:4761-4765.
61. Wang, Y., B. Agerberth, A. Lothgren, A. Almstedt, and J. Johansson. 1998. Apolipoprotein A-I binds and inhibits the human antibacterial/cytotoxic peptide LL-37. J. Biol. Chem. 273:33115-33118.
62. Wiegand, I., K. Hilpert, and R. E. Hancock. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
63. Wieprecht, T., O. Apostolov, M. Beyermann, and J. Seelig. 1999. Thermodynamics of the alpha-helix-coil transition of amphipathic peptides in a membrane environment: implications for the peptide-membrane binding equilibrium. J. Mol. Biol. 294:785-794.
64. Wu, M., and R. E. Hancock. 1999. Interaction of the cyclic antimicrobial cationic peptide bactenecin with the outer and cytoplasmic membrane. J. Biol. Chem. 274:29-35.
65. Yau, W. M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry 37:14713-14718.
66. Zanetti, M., R. Gennaro, and D. Romeo. 1995. Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Lett. 374:1-5.
67. Zelezetsky, I., S. Pacor, U. Pag, N. Papo, Y. Shai, H. G. Sahl, and A. Tossi. 2005. Controlled alteration of the shape and conformational stability of alpha-helical cell-lytic peptides: effect on mode of action and cell specificity. Biochem. J. 390:177-188.
68. Zelezetsky, I., and A. Tossi. 2006. Alpha-helical antimicrobial peptides - using a sequence template to guide structure-activity relationship studies. Biochim. Biophys. Acta 1758:1436-1449.