A proposed integrated approach for the preclinical evaluation of phage therapy in Pseudomonas infections

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Danis Wlodarczyk, Katarzyna ^a,b   Vandenheuvel, Dieter ^b   Jang, Ho Bin ^b   Briers, Yves ^b,c   Olszak, Tomasz ^a   Arabski, Michal ^d   Wasik, Slawomir ^e   Drabik, Marcin ^e   Higgins, Gerard ^f,g   Tyrrell, Jean ^g   Harvey, Brian J ^g   Noben, Jean Paul ^h   Lavigne, Rob ^b   Drulis Kawa, Zuzanna ^a  

^a UNIVERSITY OF WROC AW   (Poland)

^b LABORATORY OF GENE TECHNOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d JAN KOCHANOWSKI UNIVERSITY   (Poland)

^e JAN KOCHANOWSKI UNIVERSITY   (Poland)

^f NATIONAL CHILDREN S RESEARCH CENTRE   (Ireland)

^g BEAUMONT HOSPITAL   (Ireland)

^h HASSELT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GENTAMICIN; VIRAL PROTEIN;

ANIMAL; BACTERIAL LOAD; BIOFILM; CELL LINE; CHEMISTRY; CLASSIFICATION; CYSTIC FIBROSIS; DISEASE MODEL; EPITHELIUM CELL; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOTH; MUTATION; PATHOGENICITY; PATHOLOGY; PH; PHAGE THERAPY; PROCEDURES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; PSEUDOMONAS PHAGE; VIROLOGY;

ANIMALS; BACTERIAL LOAD; BIOFILMS; CELL LINE; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GENTAMICINS; HUMANS; HYDROGEN-ION CONCENTRATION; MOTHS; MUTATION; PHAGE THERAPY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PSEUDOMONAS PHAGES; VIRAL PROTEINS;

EID: 84974815720     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28115     Document Type: Article

References (69)

1. Trautmann, M., Lepper, P. M., Haller, M. Ecology of Pseudomonas aeruginosa in the intensive care unit and the evolving role of water outlets as a reservoir of the organism. Am. J. Infect. Control 33, S41-S49 (2005).
2. Lyczak, J. B., Cannon, C. L., Pier, G. B. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2, 1051-1060 (2000).
3. Schroeder, T. H. et al. Transgenic cystic fibrosis mice exhibit reduced early clearance of Pseudomonas aeruginosa from the respiratory tract. J. Immunol. 166, 7410-7418 (2001).
4. Bragonzi, A. et al. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 180, 138-145 (2009).
5. Breidenstein, E. B. M., de la Fuente-Nunez, C., Hancock, R. E. W. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 19, 419-426 (2011).
6. Poole, K. Pseudomonas aeruginosa: Resistance to the max. Front. Microbiol. 2, 65 (2011).
7. Sulakvelidze, A., Alavidze, Z., Morris Jr. J. G. Bacteriophage therapy minireview. Antimicrob. Agents Chemother. 45, 649-659 (2001).
8. Wright, A., Hawkins, C. H., Anggard, E. E., Harper, D. R. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin. Otolaryngol. 34, 349-357 (2009).
9. Dorotkiewicz-Jach, A., Augustyniak, D., Olszak, T., Drulis-Kawa, Z. Modern therapeutic approaches against Pseudomonas aeruginosa infections. Curr. Med. Chem. 22, 1642-1664 (2015).
10. Debarbieux, L. et al. Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. J. Infect. Dis. 201, 1096-104 (2010).
11. Morello, E. et al. Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: First steps towards treatment and prevention. PLoS One 6, e16963 (2011).
12. Alemayehu, D. et al. Bacteriophages MR299-2 and NH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio 3, e00029-12 (2012).
13. Saussereau, E. et al. Effectiveness of bacteriophages in the sputum of cystic fibrosis patients. Clin. Microbiol. Infect. 20, 0983-0990 (2014).
14. Cullen, L. et al. Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains. Microbiology 161, 1961-1977 (2015).
15. Bayer, A. S. et al. Effects of alginase on the natural history and antibiotic therapy of experimental endocarditis caused by mucoid Pseudomonas aeruginosa. Infect. Immun. 60, 3979-3985 (1992).
16. Alkawash, M. A., Soothill, J. S., Schiller, N. L. Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114, 131-138 (2006).
17. Danis-Wlodarczyk, K. et al. Characterization of the newly isolated lytic Bacteriophages KTN6 and KT28 and their efficacy against Pseudomonas aeruginosa biofilm. PLoS One 10, e0127603 (2015).
18. Olszak, T. et al. In vitro and in vivo antibacterial activity of environmental bacteriophages against Pseudomonas aeruginosa strains from cystic fibrosis patients. Appl. Microbiol. Biotechnol. 99, 6021-6033 (2015).
19. Drulis-Kawa, Z., Majkowska-Skrobek, G., Maciejewska, B., Delattre, A.-S., Lavigne, R. Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Curr. Protein Pept. Sci. 13, 699-722 (2012).
20. Briers, Y. et al. The structural peptidoglycan hydrolase gp181 of bacteriophage phiKZ. Biochem. Biophys. Res. Commun. 374, 747-751 (2008).
21. Miroshnikov, K. A., Faizullina, N. M., Sykilinda, N. N., Mesyanzhinov, V. V. Properties of the endolytic transglycosylase encoded by gene 144 of Pseudomonas aeruginosa bacteriophage phiKZ. Biochem. 71, 300-305 (2006).
22. Golshahi, L., Lynch, K. H., Dennis, J. J., Finlay, W. H. In vitro lung delivery of bacteriophages KS4-M and ? KZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J. Appl. Microbiol. 110, 106-117 (2011).
23. Matinkhoo, S., Lynch, K. H., Dennis, J. J., Finlay, W. H., Vehring, R. Spray-dried respirable powders containing bacteriophages for the treatment of pulmonary infections. J. Pharm. Sci. 100, 5197-205 (2011).
24. Drulis-Kawa, Z., Olszak, T., Danis, K., Majkowska-Skrobek, G., Ackermann, H.-W. A giant Pseudomonas phage from Poland. Arch. Virol. 159, 567-572 (2014).
25. Lavigne, R. et al. Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol. 9, 224 (2009).
26. Krylov, V. N., Dela Cruz, D. M., Hertveldt, K., Ackermann, H.-W. '? KZ-like viruses', a proposed new genus of myovirus bacteriophages. Arch. Virol. 152, 1955-1959 (2007).
27. Krylov, V. N. et al. Pseudomonas bacteriophage ? KZ contains an inner body in its capsid. Can. J. Microbiol. 30, 758-762 (1984).
28. Thomas, J. a et al. Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage ? KZ. Mol. Microbiol. 84, 324-339 (2012).
29. Sokolova, O. S. et al. Genome packaging in EL and Lin68, two giant phiKZ-like bacteriophages of P. aeruginosa. Virology 468-470, 472-478 (2014).
30. Matsui, H. et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95, 1005-1015 (1998).
31. Zabner, J. et al. Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am. J. Physiol.-Lung Cell. Mol. Physiol. 284, L844-L854 (2003).
32. Worlitzsch, D. et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109, 317-325 (2002).
33. Cornelissen, A. et al. Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology 434, 251-256 (2012).
34. Pirnay, J.-P. et al. Pseudomonas aeruginosa displays an epidemic population structure. Environ. Microbiol. 4, 898-911 (2002).
35. Ceyssens, P.-J. et al. Phenotypic and genotypic variations within a single bacteriophage species. Virol. J. 8, 134 (2011).
36. Allen, L. et al. Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J. Immunol. 174, 3643-3649 (2005).
37. Hassett, D. J., Charniga, L., Bean, K., Ohman, D. E., Cohen, M. S. Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase 60, 328-336 (1992).
38. Dietrich, L. E. P., Price-Whelan, A., Petersen, A., Whiteley, M., Newman, D. K. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61, 1308-1321 (2006).
39. Meyer, J. M., Neely, A., Stintzi, A., Georges, C., Holder, I. A. Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect. Immun. 64, 518-523 (1996).
40. Arabski, M., Wasik, S., Dworecki, K., Kaca, W. Laser interferometric determination of ampicillin and colistin transfer through cellulose biomembrane in the presence of Proteus vulgaris O25 lipopolysaccharide. J. Memb. Sci. 299, 268-275 (2007).
41. Fleiszig, S. M., Zaidi, T. S., Pier, G. B. Pseudomonas aeruginosa invasion of and multiplication within corneal epithelial cells in vitro. Infect Immun 63, 4072-4077 (1995).
42. Fancello, L., Desnues, C., Raoult, D., Rolain, J. M. Bacteriophages and diffusion of genes encoding antimicrobial resistance in cystic fibrosis sputum microbiota. J. Antimicrob. Chemother. 66, 2448-2454 (2011).
43. Miriagou, V. et al. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clin. Microbiol. Infect. 16, 112-122 (2010).
44. Ceyssens, P.-J. et al. The genome and structural proteome of YuA, a new Pseudomonas aeruginosa phage resembling M6. J. Bacteriol. 190, 1429-1435 (2008).
45. Adams, M. H. In Bacteriophages (ed. Adams, M. H.) 27-30 (Interscience Publishers, 1959).
46. Ceyssens, P.-J. et al. Comparative analysis of the widespread and conserved PB1-like viruses infecting Pseudomonas aeruginosa. Environ. Microbiol. 11, 2874-2883 (2009).
47. Besemer, J., Lomsadze, A., Borodovsky, M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 29, 2607-2618 (2001).
48. Lukashin, A. V., Borodovsky, M. GeneMark.hmm: New solutions for gene finding. Nucleic Acids Res. 26, 1107-1115 (1998).
49. Sayers, E. et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 39, D38-D51 (2011).
50. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
51. Soding, J., Biegert, A., Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248 (2005).
52. Finn, R. D., Clements, J., Eddy, S. R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29-W37 (2011).
53. Finn, R. D. et al. Pfam: clans, web tools and services. Nucleic Acids Res. 34, D247-D251 (2006).
54. Mitchell, A. et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213-D221 (2015).
55. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858 (2015).
56. Lowe, T., Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 (1997).
57. Rice, P., Longden, I., Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277 (2000).
58. Naville, M., Ghuillot-Gaudeffroy, A., Marchais, A., Gautheret, D. ARNold: A web tool for the prediction of Rho-independent transcription terminators. RNA Biol. 8, 11-13 (2014).
59. Leplae, R., Lima-Mendez, G., Toussaint, A. ACLAME: A CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 38, D57-D61 (2010).
60. Lima-Mendez, G., Van Helden, J., Toussaint, A., Leplae, R. Reticulate representation of evolutionary and functional relationships between phage genomes. Mol. Biol. Evol. 25, 762-777 (2008).
61. Jang, H. Bin et al. Phylogenomic Network and Comparative Genomics Reveal a Diverged Member of the ? KZ-Related Group, Marine Vibrio Phage ? JM-2012. J. Virol. 87, 12866-12878 (2013).
62. Casjens, S. Prophages and bacterial genomics: What have we learned so far? Mol. Microbiol. 49, 277-300 (2003).
63. Brohee, S., Faust, K., Lima-Mendez, G., Vanderstocken, G., van Helden, J. Network Analysis Tools: from biological networks to clusters and pathways. Nat. Protoc. 3, 1616-1629 (2008).
64. Van den Bossche, A. et al. Systematic Identification of Hypothetical Bacteriophage Proteins Targeting Key Protein Complexes of Pseudomonas aeruginosa. J. Proteome Res. 13, 4446-4456 (2014).
65. Ceyssens, P.-J. et al. Development of Giant Bacteriophage KZ is Independent of the Host Transcription Apparatus. J. Virol. 88, 10501-10510 (2014).
66. Pajunen, M., Kiljunen, S., Skurnik, M. Bacteriophage phi YeO3-12, Specific for Yersinia enterocolitica Serotype O:3, is Related to Coliphages T3 and T7. J. Bacteriol. 182, 5114-5120 (2000).
67. Kutter, E. Phage host range and efficiency of plating. Methods Mol. Biol. 501, 141-149 (2009).
68. Wasik, S., Bryll, A., Drabik, M., Dworecki, K., Slezak, A. Laser interferometric investigation of solute transport through membraneconcentration boundary layer system. J. Biol. Phys. 41, 409-420 (2015).
69. Hoegy, F., Mislin, G. L. A., Schalk, I. J. Pyoverdine and pyochelin measurements. Methods Mol. Biol. 1149, 293-301 (2014).