Discovery of an ultra-short linear antibacterial tetrapeptide with anti-MRSA activity from a structure-activity relationship study

European Journal of Medicinal Chemistry

Volumn 105, Issue , 2015, Pages 138-144

  Lau, Qiu Ying ^a   Ng, Fui Mee ^a   Cheong, Jin Wei Darryl ^a   Yap, Yi Yong Alvin ^a   Tan, Yoke Yan Fion ^a   Jureen, Roland ^b   Hill, Jeffrey ^a   Chia, Cheng San Brian ^a  

^a Agency for Science   (Singapore)

^b NATIONAL UNIVERSITY HOSPITAL   (Singapore)

Author keywords

Antibacterial peptide; Antimicrobial peptide; MRSA; Skin infection; SSTI

Indexed keywords

ANTIBIOTIC AGENT; CLINDAMYCIN; HEXAPEPTIDE; LINEZOLID; OMIGANAN; PEXIGANAN; TETRAPEPTIDE; TRITON X 100; VANCOMYCIN; ANTIINFECTIVE AGENT; OLIGOPEPTIDE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; DRUG POTENCY; HEMOLYSIS; HUMAN; HUMAN CELL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; STRUCTURE ACTIVITY RELATION; CHEMISTRY; CONFORMATION; DOSE RESPONSE; DRUG DEVELOPMENT; DRUG EFFECTS; ERYTHROCYTE; METABOLISM; SYNTHESIS;

ANTI-BACTERIAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DISCOVERY; ERYTHROCYTES; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CONFORMATION; OLIGOPEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84944720736     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2015.10.015     Document Type: Article

References (61)

1. H.W. Boucher, G.H. Talbot, J.S. Bradley, J.E. Edwards, D. Gilbert, L.B. Rice, M. Scheld, B. Spellberg, J. Bartlett, Bad bugs, no drugs: no ESKAPE! an update from the infectious diseases society of America, Clin. Infect. Dis. 48 (2009) 1-12.
2. M.Z. David, R.S. Daum, Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic, Clin. Microbiol. Rev. 23 (2010) 616-687.
3. M.S. Dryden, Complicated skin and soft tissue infection, J. Antimicrob. Chemother. 65 (Suppl. 3) (2010) iii35-iii44.
4. G.J. Moran, A. Krishnadasan, R.J. Gorwitz, G.E. Fosheim, L.K. McDougal, R.B. Carey, D.A. Talan, Methicillin-resistant S. aureus infections among patients in the emergency department, N. Engl. J. Med. 355 (2006) 666-674.
5. I.M. Gould, Costs of hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) and its control, Int. J. Antimicrob. Agents 28 (2006) 379-384.
6. B.Y. Lee, A. Singh, M.Z. David, S.M. Bartsch, R.B. Slayton, S.S. Huang, S.M. Zimmer, M.A. Potter, C.M. Macal, D.S. Lauderdale, L.G. Miller, R.S. Daum, The economic burden of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA), Clin. Microbiol. Infect. 19 (2013) 528-536.
7. www.cdc.gov/drugresistance/threat-report-2013/.
8. R.E.W. Hancock, Cationic antimicrobial peptides: towards clinical applications, Exp. Opin. Investig. Drugs 9 (2000) 1723-1729.
9. R.E.W. Hancock, H. Sahl, Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies, Nat. Biotechnol. 24 (2006) 1551-1557.
10. A.K. Marr, W.J. Gooderham, R.E.W. Hancock, Antibacterial peptides for therapeutic use: obstacles and realistic outlook, Curr. Opin. Pharmacol. 6 (2006) 468- 472.
11. L. Zhang, T.J. Falla, Antimicrobial peptides: therapeutic potential, Expert Opin. Pharmacother. 7 (2006) 653-663.
12. N.K. Brogden, K.A. Brogden, Will new generations of modified antimicrobial peptides improve their potential as pharmaceuticals? Int. J. Antimicrob. Agents 38 (2011) 217-225.
13. A.T.Y. Yeung, S.L. Gellatly, R.E.W. Hancock, Multifunctional cationic host defence peptides and their clinical applications, Cell Mol. Life Sci. 68 (2011) 2161- 2176.
14. C.D. Fjell, J.A. Hiss, R.E.W. Hancock, G. Schneider, Designing antimicrobial peptides: form follows function, Nat. Rev. Drug. Discov. 11 (2012) 37-51.
15. M. Zasloff, Antimicrobial peptides of multicellular organisms, Nature 415 (2002) 389-395.
16. Y. Shai, Mode of action of membrane active antimicrobial peptides, Biopolym. Pept. Sci. 66 (2002) 236-248.
17. H.G. Boman, Antibacterial peptides: basic facts and emerging concepts, J. Intern. Med. 254 (2003) 197-215.
18. M.R. Yeaman, N.Y. Yount, Mechanisms of antimicrobial peptide action and resistance, Pharmacol. Rev. 55 (2003) 27-55.
19. M.N. Melo, R. Ferre, M.A.R.B. Castanho, Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations, Nat. Rev. Microbiol. 7 (2009) 245-250.
20. W.C. Wimley, Describing the mechanism of antimicrobial peptide action with the interfacial activity model, ACS Chem. Biol. 5 (2010) 905-917.
21. K.A. Brogden, Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 (2005) 238-250.
22. Y. Ge, D.L. MacDonald, K.J. Holroyd, C. Thornsberry, H. Wexler, M. Zasloff, In vitro antibacterial properties of Pexiganan, an analog of Magainin, Antimicrob. Agents Chemother. 43 (1999) 782-788.
23. R.K. Flamm, P.R. Rhomberg, K.M. Simpson, D.J. Farrell, H.S. Sader, R.N. Jones, In vitro spectrum of pexiganan activity when tested against pathogens from diabetic foot infections and with selected resistance mechanisms, Antimicrob. Agents Chemother. 59 (2015) 1751-1754.
24. E. Rubinchik, D. Dugourd, T. Algara, C. Pasetka, H.D. Friedland, Antimicrobial and antifungal activities of a novel cationic antimicrobial peptide, omiganan, in experimental skin colonisation models, J. Antimicrob. Agents 34 (2009) 457-461.
25. R.N. Murugan, B. Jacob, E.-H. Kim, M. Ahn, H. Sohn, J.-H. Seo, C. Cheong, J.- K. Hyun, K.S. Lee, S.Y. Shin, J.K. Bamg, Non hemolytic short peptidomimetics as a new class of potent and broad-spectrum antimicrobial agents, Bioorg. Med. Chem. Lett. 23 (2013) 4633-4636.
26. Q.Y. Lau, X.Y. Choo, Z.X. Lim, X.N. Kong, F.M. Ng, M.J.Y. Ang, J. Hill, C.S.B. Chia, A head-to-head comparison of the antimicrobial activities of 30 ultra-short antimicrobial peptides against Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans, Int. J. Pept. Res. Ther. 21 (2015) 21-28.
27. B. Limbago, G.E. Fosheim, V. Schoonover, C.E. Crane, J. Nadle, S. Petit, D. Heltzel, S.M. Ray, L.H. Harrison, R. Lynfield, G. Dumyati, J.M. Townes, W. Schaffner, Y. Mu, S.K. Fridkin, Characterization of methicillin- resistant Staphylococcus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis, J. Clin. Microbiol. 47 (2009) 1344-1351.
28. C. Liu, A. Bayer, S.E. Cosgrove, R.S. Daum, S.K. Fridkin, R.J. Gorwitz, S.L. Kaplan, A.W. Karchmer, D.P. Levine, B.E. Murray, M.J. Rybak, D.A. Talan, H.F. Chambers, Clinical practice guidelines by the infectious diseases society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children, Clin. Infect. Dis. 52 (2011) 1-38.
29. F.R. Deleo, M. Otto, B.N. Kreiswirth, H.F. Chambers, Community-associated meticillin-resistant Staphylococcus aureus, Lancet 375 (2010) 1557-1568.
30. M.D. King, B.J. Humphrey, Y.F. Wang, E.V. Kourbatova, S.M. Ray, H.M. Blumberg, Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections, Ann. Intern. Med. 144 (2006) 309-317.
31. M. Otto, Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus, Annu. Rev. Microbiol. 64 (2010) 143-162.
32. A.D. Kennedy, F.R. DeLeo, Epidemiology and virulence of community-associated MRSA, Clin. Microbiol. Newsl. 31 (2009) 153-160.
33. K. Zhang, J. McClure, S. Elsayed, J. Tan, J.M. Conly, Coexistence of panton- Valentine leukocidin-positive and -negative community-associated methicillin- resistant Staphylococcus aureus USA400 sibling strains in a large Canadian health-care region, J. Infect. Dis. 197 (2008) 195-204.
34. T.L. Smith, M.L. Pearson, K.R. Wilcox, C. Cruz, M.V. Lancaster, B. Robinson-Dunn, F.C. Tenover, M.J. Zervos, J.D. Band, E. White, W.R. Jarvis, Emergence of vancomycin resistance in Staphylococcus aureus. Glycopeptide-intermediate Staphylococcus aureus, N. Engl. J. Med. 340 (1999) 493-501.
35. Clinical and Laboratory Standards Institute, approved standard - ninth edition. Document M07-A9, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, vol. 32, CLSI, Wayne, PA, 2012. No. 2.
36. www.fda.gov/ohrms/dockets/98fr/2002d-0389-gdl0002.pdf.
37. D. Gonzalez, C. Melloni, R. Yogev, B.B. Poindexter, S.R. Mendley, P. Delmore, J.E. Sullivan, J. Autmizguine, A. Lewandowski, B. Harper, K.M. Watt, K.C. Lewis, E.V. Capparelli, D.K. Benjamin, M. Cohen-Wolkowiez, Use of opportunistic clinical data and a population pharmacokinetic model to support dosing of clindamycin for premature infants to adolescents, Clin. Pharmacol. Ther. 96 (2014) 429-437.
38. W. Zhao, T. Róg, A.A. Gurtovenko, I. Vattulainen, M. Karttunen, Role of phosphatidylglycerols in the stability of bacterial membranes, Biochimie 90 (2008) 930-938.
39. M. Tang, A.J. Waring, 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.
40. J.A. Killian, G. von Heijne, How proteins adapt to a membrane-water interface, Trends Biochem. Sci. 25 (2000) 429-434.
41. D.I. Chan, E.J. Prenner, H.J. Vogel, Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action, Biochim. Biophys. Acta 1758 (2006) 1184-1202.
42. X. Bi, C. Wang, W. Dong, W. Zhu, D. Shang, Antimicrobial properties and interaction of two Trp-substituted cationic antimicrobial peptides with a lipid bilayer, J. Antibiot. 67 (2014) 361-368.
43. G. Fimland, V.G. Eijsink, J. Nissen-Meyer, Mutational analysis of the role of tryptophan residues in an antimicrobial peptide, Biochemistry 41 (2002) 9508- 9515.
44. D.J. Schibli, R.F. Epand, H.J. Vogel, R.M. Epand, Tryptophan rich antimicrobial peptides: comparative properties and membrane interactions, Biochem. Cell Biol. 80 (2002) 667-677.
45. F.N. Petersen, M.O. Jensen, C.H. Nielsen, Interfacial tryptophan residues: a role for the cation-pi effect? Biophys. J. 89 (2005) 3985-3996.
46. B. Deslouches, J.D. Steckbeck, J.K. Craigo, Y. Doi, T.A. Mietzner, R.C. Montelaro, Rational design of engineered cationic antimicrobial peptides consisting exclusively of arginine and tryptophan and their activity against multidrug-resistant pathogens, Antimicrob. Agents Chemother. 57 (2013) 2511-2521.
47. B.E. Haug, M.L. Skar, J.S. Svendsen, Bulky aromatic amino acids increase the antibacterial activity of 15-residue bovine lactoferricin derivatives, J. Pept. Sci. 7 (2001) 425-432.
48. B.E. Haug, W. Stensen, T. Stiberg, J.S. Svendsen, Bulky nonproteinogenic amino acids permit the design of very small and effective cationic antibacterial peptides, J. Med. Chem. 47 (2004) 4159-4162.
49. M.B. Strøm, B.E. Haug, M.L. Skar, W. Stensen, T. Stiberg, J.S. Svendsen, The pharmacophore of short cationic antibacterial peptides, J. Med. Chem. 46 (2003) 1567-1570.
50. D. Avrahami, Y. Shai, A new group of antifungal and antibacterial lipopeptides derived from non-membrane active peptides conjugated to palmitic acid, J. Biol. Chem. 279 (2004) 12277-12286.
51. A. Makovitzki, D. Avrahami, Y. Shai, Ultrashort antibacterial and antifungal lipopeptides, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 15997-16002.
52. A. Makovitzki, J. Baram, Y. Shai, Antimicrobial lipopolypeptides composed of palmitoyl di- and tricationic peptides: in vitro and in vivo activities, self- assembly to nanostructures, and a plausible mode of action, Biochemistry 47 (2008) 10630-10636.
53. B. Findlay, G.G. Zhanel, F. Schweizer, Investigating the antimicrobial peptide 'window of activity' using cationic lipopeptides with hydrocarbon and fluorinated tails, Int. J. Antimicrob. Agents 40 (2012) 36-42.
54. H. Mohanram, S. Bhattacharjya, β-Boomerang antimicrobial and antiendotoxic peptides: lipidation and disulfide bond effects on activity and structure, Pharmaceuticals 7 (2014) 482-501.
55. P.C. Appelbaum, Reduced glycopeptide susceptibility in methicillin-resistant Staphylococcus aureus (MRSA), Int. J. Antimicrob. Agents 30 (2007) 398-408.
56. C. Tsoulas, D. Nathwani, Review of meta-analyses of vancomycin compared with new treatments for gram-positive skin and soft-tissue infections: are we any clearer? Int. J. Antimicrob. Agents 46 (2015) 1-7.
57. G.A. Pankey, L.D. Sabath, Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of gram-positive bacterial infections, Clin. Infect. Dis. 38 (2004) 864-870.
58. P.M. Small, H.F. Chambers, Vancomycin for Staphylococcus aureus endocarditis in intravenous drug users, Antimicrob. Agents Chemother. 34 (1990) 1227- 1231.
59. B.T. Tsuji, T. Brown, R. Parasrampuria, D.A. Brazeau, A. Forrest, P.A. Kelchlin, P.N. Holden, C.A. Peloquin, D. Hanna, J.B. Bulitta, Front-loaded linezolid regimens result in increased killing and suppression of the accessory gene regulator system of Staphylococcus aureus, Antimicrob. Agents Chemother. 56 (2012) 3712-3719.
60. W.F. DeGrado, G.F. Musso, M. Lieber, E.T. Kaiser, F.J. Kézdy, Kinetics and mechanism of hemolysis induced by melittin and by a synthetic melittin analogue, Biophys. J. 37 (1982) 329-338.
61. C.L. Ho, Y.L. Lin, W.C. Chen, L.L. Hwang, H.M. Yu, K.T. Wang, Structural requirements for the edema-inducing and hemolytic activities of mastoparan B isolated from the hornet (Vespa basalis) venom, Toxicon 34 (1996) 1027-1035.