Art-175 is a highly efficient antibacterial against multidrug-resistant strains and persisters of Pseudomonas aeruginosa

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 7, 2014, Pages 3774-3784

  Briers, Yves ^a   Walmagh, Maarten ^a   Grymonprez, Barbara ^a   Biebl, Manfred ^b   Pirnay, Jean Paul ^c   Defraine, Valerie ^a   Michiels, Jan ^a   Cenens, William ^a   Aertsen, Abram ^a   Miller, Stefan ^b   Lavigne, Rob ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Lisando GmbH   (Germany)

^c QUEEN ASTRID MILITARY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ART 085; ART 175; CIPROFLOXACIN; PEPTIDOGLYCAN; UNCLASSIFIED DRUG; ART-175; CATHELICIDIN; HYBRID PROTEIN; PROTEINASE; RECOMBINANT PROTEIN;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; CROSS RESISTANCE; GENE MUTATION; MICROSCOPY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; ANIMAL; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOLECULAR CLONING; MOUSE; PSEUDOMONAS INFECTION;

ANIMALS; ANTI-BACTERIAL AGENTS; CATHELICIDINS; CELL SURVIVAL; CLONING, MOLECULAR; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENDOPEPTIDASES; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; PEPTIDOGLYCAN; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS;

EID: 84903206252     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02668-14     Document Type: Article

References (50)

1. Spellberg B, Guidos R, Gilbert D, Bradley J, Boucher HW, Scheld WM, Bartlett JG, Edwards J, Jr, Infectious Diseases Society of America. 2008. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clin. Infect. Dis. 46:155-164. http://dx.doi.org/10.1086/524891. (Pubitemid 351269151)
2. Xu ZQ, Flavin MT, Flavin J. 2014. Combating multidrug-resistant Gram-negative bacterial infections. Expert Opin. Invest. Drugs 23:163-182. http://dx.doi.org/10.1517/13543784.2014.848853.
3. Silver LL. 2011. Challenges of antibacterial discovery. Clin. Microbiol. Rev. 24:71-109. http://dx.doi.org/10.1128/CMR.00030-10.
4. Lancaster JW, Matthews SJ. 2012. Fidaxomicin: the newest addition to the armamentarium against Clostridium difficile infections. Clin. Ther. 34:1-13. http://dx.doi.org/10.1016/j.clinthera.2011.12.003.
5. Centers for Disease Control and Prevention (CDC). 2013. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/drugresistance/threat-report-2013/ pdf/ar-threats-2013-508.pdf.
6. European Parliament. 2011. Resolution of 27 October 2011 on the public health threat of antimicrobial resistance. European Union, Strasbourg, France. http://www.europarl.europa.eu/sides/getDoc.do?pubRef=-//EP//TEXT+TA+P7-TA-2011- 0473+0+DOC+XML+V0//EN.
7. Delcour AH. 2009. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta 1794:808-816. http://dx.doi.org/10.1016/j.bbapap.2008.11. 005.
8. Lewis K. 2010. Persister cells. Annu. Rev. Microbiol. 64:357-372. http://dx.doi.org/10.1146/annurev.micro.112408.134306.
9. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL. 2007. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 6:29-40. http://dx.doi.org/10.1038/nrd2201. (Pubitemid 46020284)
10. Hancock RE, Sahl HG. 2006. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24:1551-1557. http://dx.doi.org/10.1038/nbt1267. (Pubitemid 44967479)
11. Parisien A, Allain B, Zhang J, Mandeville R, Lan CQ. 2008. Novel alternatives to antibiotics: bacteriophages, cell wall hydrolases and antimicrobial peptides. J. Appl. Microbiol. 104:1-13. http://dx.doi.org/10.1111/ j.1365-2672.2007.03498.x. (Pubitemid 350265294)
12. Nelson DC, Schmelcher M, Rodriguez-Rubio L, Klumpp J, Pritchard DG, Dong S, Donovan DM. 2012. Endolysins as antimicrobials. Adv. Virus Res. 83:299-365. http://dx.doi.org/10.1016/B978-0-12-394438-2.00007-4.
13. Baltzer SA, Brown MH. 2011. Antimicrobial peptides: promising alternatives to conventional antibiotics. J. Mol. Microbiol. Biotechnol. 20: 228-235. http://dx.doi.org/10.1159/000331009.
14. Hancock RE. 1997. Peptide antibiotics. Lancet 349:418-422. http://dx.doi.org/10.1016/S0140-6736(97)80051-7. (Pubitemid 27077684)
15. Dawson RM, Liu CQ. 2009. Cathelicidin peptide SMAP-29: comprehensive review of its properties and potential as a novel class of antibiotics. Drug Dev. Res. 70:481-498. http://dx.doi.org/10.1002/ddr.20329.
16. Young R, Wang I, RoofWD. 2000. Phages will out: strategies of host cell lysis. Trends Microbiol. 8:120-128. http://dx.doi.org/10.1016/S0966-842X(00) 01705-4. (Pubitemid 30155487)
17. Callewaert L, Walmagh M, Michiels CW, Lavigne R. 2011. Food applications of bacterial cell wall hydrolases. Curr. Opin. Biotechnol. 22:164-171. http://dx.doi.org/10.1016/j.copbio.2010.10.012.
18. Schmelcher M, Donovan DM, Loessner MJ. 2012. Bacteriophage endolysins as novel antimicrobials. Future Microbiol. 7:1147-1171. http://dx.doi.org/10.2217/ fmb.12.97.
19. Pastagia M, Schuch R, Fischetti VA, Huang DB. 2013. Lysins: the arrival of pathogen-directed anti-infectives. J. Med. Microbiol. 62(Pt 10):1506-1516. http://dx.doi.org/10.1099/jmm.0.061028-0.
20. Loeffler JM, Nelson D, Fischetti VA. 2001. Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294:2170-2172. http://dx.doi.org/10.1126/science.1066869. (Pubitemid 33150674)
21. Schuch R, Nelson D, Fischetti VA. 2002. A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418:884-889. http://dx.doi.org/10. 1038/nature01026. (Pubitemid 34966308)
22. Pastagia M, Euler C, Chahales P, Fuentes-Duculan J, Krueger JG, Fischetti VA. 2011. A novel chimeric lysin shows superiority to mupirocin for skin decolonization of methicillin-resistant and -sensitive Staphylococcus aureus strains. Antimicrob. Agents Chemother. 55:738-744. http://dx.doi.org/10.1128/ AAC.00890-10.
23. Briers Y, Walmagh M, Lavigne R. 2011. Use of bacteriophage endolysin EL188 and outer membrane permeabilizers against Pseudomonas aeruginosa. J. Appl. Microbiol. 110:778-785. http://dx.doi.org/10.1111/j.1365-2672.2010.04931.x.
24. Skerlavaj B, Benincasa M, Risso A, Zanetti M, Gennaro R. 1999. SMAP-29: a potent antibacterial and antifungal peptide from sheep leukocytes. FEBS Lett. 46:58-62. (Pubitemid 30001718)
25. Briers Y, Volckaert G, Cornelissen A, Lagaert S, Michiels CW, Hertveldt K, Lavigne R. 2007. Muralytic activity and modular structure of the endolysins of Pseudomonas aeruginosa bacteriophages phiKZ and EL. Mol. Microbiol. 65:1334-1344. http://dx.doi.org/10.1111/j.1365-2958.2007.05870.x. (Pubitemid 47262831)
26. Tack BF, Sawai MV, Kearney WR, Robertson AD, Sherman MA, Wang W, Hong T, Boo LM, Wu H, Waring AJ, Lehrer RI. 2002. SMAP-29 has two LPS-binding sites and a central hinge. Eur. J. Biochem. 269:1181-1189. http://dx.doi.org/10.1046/j. 0014-2956.2002.02751.x. (Pubitemid 34175377)
27. Briers Y, Schmelcher M, Loessner MJ, Hendrix J, Engelborghs Y, Volckaert G, Lavigne R. 2009. The high-affinity peptidoglycan binding domain of Pseudomonas phage endolysin KZ144. Biochem. Biophys. Res. Commun. 383:187-191. http://dx.doi.org/10.1016/j.bbrc.2009.03.161.
28. Pirnay JP, De Vos D, Cochez C, Bilocq F, Vanderkelen A, Zizi M, Ghysels B, Cornelis P. 2002. Pseudomonas aeruginosa displays an epidemic population structure. Environ. Microbiol. 4:898-911. http://dx.doi.org/10.1046/j.1462-2920. 2002.00321.x. (Pubitemid 36064179)
29. Pirnay JP, De Vos D, Mossialos D, Vanderkelen A, Cornelis P, Zizi M. 2002. Analysis of the Pseudomonas aeruginosa oprD gene from clinical and environmental isolates. Environ. Microbiol. 4:872-882. http://dx.doi.org/10. 1046/j.1462-2920.2002.00281.x. (Pubitemid 36064177)
30. Cenens W, Mebrhatu MT, Makumi A, Ceyssens PJ, Lavigne R, Van Houdt R, Taddei F, Aertsen A. 2013. Expression of a novel P22 ORFan gene reveals the phage carrier state in Salmonella Typhimurium. PLoS Genet. 9:e1003269. http://dx.doi.org/10.1371/journal.pgen.1003269.
31. CLSI. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard - 9th ed. CLSI M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
32. Chen X, Zhang M, Zhou C, Kallenbach NR, Ren D. 2011. Control of bacterial persister cells by Trp/Arg-containing antimicrobial peptides. Appl. Environ. Microbiol. 77:4878-4885. http://dx.doi.org/10.1128/AEM.02440-10.
33. De Groote VN, Verstraeten N, Fauvart M, Kint CI, Verbeeck AM, Beullens S, Cornelis P, Michiels J. 2009. Novel persistence genes in Pseudomonas aeruginosa identified by high-throughput screening. FEMS Microbiol. Lett. 297:73-79. http://dx.doi.org/10.1111/j.1574-6968.2009.01657.x.
34. Schuch R, Lee HM, Schneider BC, Sauve KL, Law C, Khan BK, Rotolo JA, Horiuchi Y, Couto DE, Raz A, Fischetti VA, Huang DB, Nowinski RC, Wittekind M. 2013. Combination therapy with lysin CF-301 and antibiotic is superior to antibiotic alone for treating methicillin-resistant Staphylococcus aureus-induced murine bacteremia. J. Infect. Dis. http://dx.doi.org/10.1093/ infdis/jit637.
35. Anderson RC, Hancock REW, Yu PL. 2004. Antimicrobial activity and bacterial-membrane interaction of ovine-derived cathelicidins. Antimicrob. Agents Chemother. 48:673-676. http://dx.doi.org/10.1128/AAC.48.2.673-676.2004. (Pubitemid 38141743)
36. Schleifer H, Kandler O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407-477.
37. Daly KE, Huang KC, Wingreen NS, Mukhopadhyay R. 2011. Mechanics of membrane bulging during cell-wall disruption in Gram-negative bacteria. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 83:041922. http://dx.doi.org/10.1103/ PhysRevE.83.041922.
38. Briers Y, Cornelissen A, Aertsen A, Hertveldt K, Michiels CW, Volckaert G, Lavigne R. 2008. Analysis of outer membrane permeability of Pseudomonas aeruginosa and bactericidal activity of endolysins KZ144 and EL188 under high hydrostatic pressure. FEMS Microbiol. Lett. 280:113-119. http://dx.doi.org/10. 1111/j.1574-6968.2007.01051.x. (Pubitemid 351207298)
39. Lukacik P, Barnard TJ, Keller PW, Chaturvedi KS, Seddiki N, Fairman JW, Noinaj N, Kirby TL, Henderson JP, Steven AC, Hinnebusch BJ, Buchanan SK. 2012. Structural engineering of a phage lysin that targets Gram-negative pathogens. Proc. Natl. Acad. Sci. U. S. A. 109:9857-9862. http://dx.doi.org/10.1073/pnas. 1203472109.
40. Fischetti VA. 2005. Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol. 13:491-496. http://dx.doi.org/10.1016/j.tim.2005.08.007. (Pubitemid 41317527)
41. Peschel A, Sahl H-G. 2006. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4:529-536. http://dx.doi.org/10.1038/nrmicro1441. (Pubitemid 43905612)
42. Cabot G, Bruchmann S, Mulet X, Zamorano L, Moyà B, Juan C, Haussler S, Oliver A. 2014. Pseudomonas aeruginosa ceftolozanetazobactam resistance development requires multiple mutations leading to overexpression and structural modification of AmpC. Antimicrob. Agents Chemother. http://dx.doi.org/10.1128/AAC.02462-13.
43. Ernst RK, Moskowitz SM, Emerson JC, Kraig GM, Adams KN, Harvey MD, Ramsey B, Speert DP, Burns JL, Miller SI. 2007. Unique lipid A modifications in Pseudomonas aeruginosa isolated from the airways of patients with cystic fibrosis. J. Infect. Dis. 196:1088-1092. http://dx.doi.org/10.1086/521367. (Pubitemid 47580305)
44. Kümmerer K. 2003. Significance of antibiotics in the environment. J. Antimicrob. Chemother. 52: 5-7. http://dx.doi.org/10.1093/jac/dkg293. (Pubitemid 36850076)
45. Fauvart M, De Groote VN, Michiels J. 2011. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J. Med. Microbiol. 60:699-709. http://dx.doi.org/10.1099/jmm.0. 030932-0.
46. Allison KR, Brynildsen MP, Collins J. 2011. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473:216-220. http://dx.doi.org/10.1038/nature10069.
47. Bryk R, Gold B, Venugopal A, Singh J, Samy R, Pupek K, Cao H, Popescu C, Gurney M, Hotha S, Cherian J, Rhee K, Ly L, Converse PJ, Ehrt S, Vandal O, Jiang X, Schneider J, Lin G, Nathan C. 2008. Selective killing of nonreplicating mycobacteria. Cell Host Microbe 3:137-145. http://dx.doi.org/10.1016/j.chom. 2008.02.003. (Pubitemid 351325759)
48. Dworkin J, Shah IM. 2010. Exit from dormancy in microbial organisms. Nat. Rev. Microbiol. 8:890-896. http://dx.doi.org/10.1038/nrmicro2453.
49. Mulcahy LR, Burns JL, Lory S, Lewis K. 2010. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J. Bacteriol. 192:6191-6196. http://dx.doi.org/10.1128/JB. 01651-09.
50. Masschalck B, Michiels CW. 2003. Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria. Crit. Rev. Microbiol. 29:191-214. http://dx.doi.org/10.1080/713610448. (Pubitemid 37204782)