Expert Opinion on Three Phage Therapy Related Topics: Bacterial Phage Resistance, Phage Training and Prophages in Bacterial Production Strains

. 2018 Apr 05 ; 10 (4) : . [epub] 20180405

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu kongresy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29621199

Phage therapy is increasingly put forward as a "new" potential tool in the fight against antibiotic resistant infections. During the "Centennial Celebration of Bacteriophage Research" conference in Tbilisi, Georgia on 26-29 June 2017, an international group of phage researchers committed to elaborate an expert opinion on three contentious phage therapy related issues that are hampering clinical progress in the field of phage therapy. This paper explores and discusses bacterial phage resistance, phage training and the presence of prophages in bacterial production strains while reviewing relevant research findings and experiences. Our purpose is to inform phage therapy stakeholders such as policy makers, officials of the competent authorities for medicines, phage researchers and phage producers, and members of the pharmaceutical industry. This brief also points out potential avenues for future phage therapy research and development as it specifically addresses those overarching questions that currently call for attention whenever phages go into purification processes for application.

Autonomous Department of Microorganisms' Biology Faculty of Agriculture and Biology Warsaw University of Life Sciences SGGW 02 787 Warsaw Poland

Bacteriophage Laboratory Hirszfeld Institute of Immunology and Experimental Therapy Polish Academy of Sciences 53 114 Wroclaw Poland

Centre of Excellence in Biological Interactions Department of Biological and Environmental Science Nanoscience Center University of Jyväskylä Survontie 9C FI 40014 Jyväskylä Finland

Chemical Engineering Department Loughborough University Leicestershire LE11 3TU UK

Department of Clinical Immunology Transplantation Institute Medical University of Warsaw 02 006 Warsaw Poland

Department of Experimental Biology Faculty of Science Masaryk University 60000 Brno Czech Republic

Department of Fundamental Microbiology University of Lausanne 1015 Lausanne Switzerland

Department of Microbiology Institut Pasteur 75015 Paris France

Department of Microorganisms Leibniz Institute DSMZ German Collection of Microorganisms and Cell Cultures 38100 Braunschweig Germany

Department of Pharmaceutical and Pharmacological Sciences KU Leuven 3000 Leuven Belgium

Eliava Institute of Bacteriophage Microbiology and Virology Gotua Street 3 0160 Tbilisi Georgia

Faculty of Dental Medicine The Hebrew University of Jerusalem Jerusalem 9112001 Israel

Institute of Biochemistry and Biophysics Polish Academy of Sciences 00 901 Warsaw Poland

Laboratory for Bacteriology Research Faculty Medicine and Health Sciences Ghent University 9000 Ghent Belgium

Laboratory for Molecular and Cellular Technology Queen Astrid Military Hospital 1120 Brussels Belgium

Laboratory of Gene Technology Department of Biosystems 3000 Leuven Belgium

MB Pharma 120 00 Prague 2 Vinohrady Czech Republic

University of Turin 10124 Turin Italy

Zobrazit více v PubMed

Koskella B., Brockhurst M.A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 2014;38:916–931. doi: 10.1111/1574-6976.12072. PubMed DOI PMC

Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010;8:317–327. doi: 10.1038/nrmicro2315. PubMed DOI

Maxwell K.L. Phages fight back: Inactivation of the CRISPR-Cas bacterial immune system by anti-CRISPR proteins. PLoS Pathog. 2016;12:e1005282. doi: 10.1371/journal.ppat.1005282. PubMed DOI PMC

Goldfarb T., Sberro H., Weinstock E., Cohen O., Doron S., Yoav Charpak-Amikam Y., Afik S., Ofir G., Sorek R. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J. 2015;34:169–183. doi: 10.15252/embj.201489455. PubMed DOI PMC

Ofir G., Melamed S., Sberro H., Mukamel Z., Silverman S., Yaakov G., Doron S., Sorek R. DISARM is a widespread bacterial defence system with broad anti-phage activities. Nat. Microbiol. 2018;3:90–98. doi: 10.1038/s41564-017-0051-0. PubMed DOI PMC

Hall A.R., de Vos D., Friman V.P., Pirnay J.P., Buckling A. Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in wax moth larvae. Appl. Environ. Microb. 2012;78:5646–5652. doi: 10.1128/AEM.00757-12. PubMed DOI PMC

Friman V.P., Soanes-Brown D., Sierocinski P., Molin S., Johansen H.K., Merabishvili M., Pirnay J.P., de Vos D., Buckling A. Pre-adapting parasitic phages to a pathogen leads to increased pathogen clearance and lowered resistance evolution with Pseudomonas aeruginosa cystic fibrosis bacterial isolates. J. Evolut. Biol. 2016;29:188–198. doi: 10.1111/jeb.12774. PubMed DOI

Oechslin F., Piccardi P., Mancini S., Gabard J., Moreillon P., Entenza J.M., Resch G., Que Y.-A. Synergistic interaction between phage therapy and antibiotics clears Pseudomonas aeruginosa infection in endocarditis and Reduces Virulence. J. Infect. Dis. 2017;215:703–712. doi: 10.1093/infdis/jiw632. PubMed DOI PMC

Laanto E., Hoikkala V., Ravantti J., Sundberg L.R. Long-term genomic coevolution of host-parasite interaction in the natural environment. Nat. Commun. 2017;8 doi: 10.1038/s41467-017-00158-7. PubMed DOI PMC

Międzybrodzki R., Borysowski J., Weber-Dąbrowska B., Fortuna W., Letkiewicz S., Szufnarowski K., Pawełczyk Z., Rogóż P., Kłak M., Wojtasik E., et al. Clinical aspects of phage therapy. Adv. Virus Res. 2012;83:73–121. PubMed

Appelmans R. Le dosage du bactériophage. C. R. Soc. Biol. Fil. 1921;89:1098.

Roach D.R., Leung C.Y., Henry M., Morello E., Singh D., Di Santo J.P., Weitz J.S., Debarbieux L. Synergy between the host immune system and bacteriophage is essential for successful phage therapy against an acute respiratory pathogen. Cell Host Microbe. 2017;22:38–47. doi: 10.1016/j.chom.2017.06.018. PubMed DOI

Malik D.J., Sokolov I.J., Vinner G.K., Mancuso F., Cinquerrui S., Vladisavljevic G.T., Clokie M.R.J., Stapley A.G.F., Kirpichnikova A. Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Adv. Colloid Interface Sci. 2017;249:100–133. doi: 10.1016/j.cis.2017.05.014. PubMed DOI

Chan B.K., Sistrom M., Wertz J.E., Kortright K.E., Narayan D., Turner P.E. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci. Rep. 2016;6:26717. doi: 10.1038/srep26717. PubMed DOI PMC

Cooper I.R. A review of current methods using bacteriophages in live animals, food and animal products intended for human consumption. J. Microbiol. Meth. 2016;130:38–47. doi: 10.1016/j.mimet.2016.07.027. PubMed DOI

Ormala A.M., Jalasvuori M. Phage therapy: Should bacterial resistance to phages be a concern, even in the long run? Bacteriophage. 2013;3:e24219. doi: 10.4161/bact.24219. PubMed DOI PMC

Davis K.M., Isberg R.R. Defining heterogeneity within bacterial populations via single cell approaches. BioEssays. 2016;38:782–790. doi: 10.1002/bies.201500121. PubMed DOI

Magdanova L.A., Goliasnaia N.V. Heterogeneity as an adaptive trait of the bacterial community. Mikrobiologiia. 2013;82:3–13. PubMed

Veening J.W., Smits W.K., Kuipers O.P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 2008;62:193–210. doi: 10.1146/annurev.micro.62.081307.163002. PubMed DOI

Woodford N., Ellington M.J. The emergence of antibiotic resistance by mutation. Clin. Microbiol. Infect. 2007;13:5–18. doi: 10.1111/j.1469-0691.2006.01492.x. PubMed DOI

Babouee Flury B., Ellington M.J., Hopkins K.L., Turton J.F., Doumith M., Loy R., Staves P., Hinic V., Frei R., Woodford N. Association of novel nonsynonymous single nucleotide polymorphisms in ampD with cephalosporin resistance and phylogenetic variations in ampC, ampR, ompF, and ompC in Enterobacter cloacae isolates that are highly resistant to carbapenems. Antimicrob. Agents Chempother. 2016;60:2383–2390. doi: 10.1128/AAC.02835-15. PubMed DOI PMC

Proctor R.A., Kahl B., von Eiff C., Vaudaux P.E., Lew D.P., Peters G. Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin. Infect. Dis. 1998;27(Suppl. 1):S68–S74. doi: 10.1086/514906. PubMed DOI

Beaumont H.J., Gallie J., Kost C., Ferguson G.C., Rainey P.B. Experimental evolution of bet hedging. Nature. 2009;462:90–93. doi: 10.1038/nature08504. PubMed DOI

Schooley R.T., Biswas B., Gill J.J., Hernandez-Morales A., Lancaster J., Lessor L., Barr J.J., Reed S.L., Rohwer F., Benler S., et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob. Agents Chemother. 2017;61 doi: 10.1128/AAC.00954-17. PubMed DOI PMC

Stern A., Sorek R. The phage-host arms race: Shaping the evolution of microbes. BioEssays. 2011;33:43–51. doi: 10.1002/bies.201000071. PubMed DOI PMC

Betts A., Kaltz O., Hochberg M.E. Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. Proc. Natl. Acad. Sci. USA. 2014;111:11109–11114. doi: 10.1073/pnas.1406763111. PubMed DOI PMC

De Sordi L., Khanna V., Debarbieux L. The gut microbiota facilitates drifts in the genetic diversity and infectivity of bacterial viruses. Cell Host Microbe. 2017;22:801–808. doi: 10.1016/j.chom.2017.10.010. PubMed DOI

D’Herelle F. On an invisible microbe antagonistic toward dysenteric bacilli: Brief note by Mr. F. D’Herelle, presented by Mr. Roux. 1917. Res. Microbiol. 2007;158:553–554. PubMed

Merabishvili M., Pirnay J.P., de Vos D. Guidelines to compose an ideal bacteriophage cocktail. Methods Mol. Biol. 2018;1693:99–110. doi: 10.1007/978-1-4939-7395-8_9. PubMed DOI

Betts A., Vasse M., Kaltz O., Hochberg M.E. Back to the future: Evolving bacteriophages to increase their effectiveness against the pathogen Pseudomonas aeruginosa PAO1. Evolut. Appl. 2013;6:1054–1063. doi: 10.1111/eva.12085. PubMed DOI PMC

Merabishvili M., Pirnay J.P., de Vos D. Guidelines to compose an ideal bacteriophage cocktail. In: Azaredo J., Sillankorva S., editors. Bacteriophage Therapy: From Lab to Clinical Practice. 1st ed. Volume 1. Humana Press; New York, NY, USA: 2017. pp. 107–108.

Samson J.E., Magadan A.H., Sabri M., Moineau S. Revenge of the phages: Defeating bacterial defences. Nat. Rev. Microbiol. 2013;11:675–687. doi: 10.1038/nrmicro3096. PubMed DOI

Morello E., Saussereau E., Maura D., Huerre M., Touqui L., Debarbieux L. Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: First steps towards treatment and prevention. PLoS ONE. 2011;6:e16963. doi: 10.1371/journal.pone.0016963. PubMed DOI PMC

Clark S.T., Diaz Caballero J., Cheang M., Coburn B., Wang P.W., Donaldson S.L., Zhang Y., Liu M., Keshavjee S., Yau Y.C., et al. Phenotypic diversity within a Pseudomonas aeruginosa population infecting an adult with cystic fibrosis. Sci. Rep. 2015;5:10932. doi: 10.1038/srep10932. PubMed DOI PMC

Pirnay J.P., Blasdel B.G., Bretaudeau L., Buckling A., Chanishvili N., Clark J.R., Corte-Real S., Debarbieux L., Dublanchet A., de Vos D., et al. Quality and safety requirements for sustainable phage therapy products. Pharm. Res. 2015;32:2173–2179. doi: 10.1007/s11095-014-1617-7. PubMed DOI PMC

Expert Round Table on Acceptance and Re-implementation of Bacteriophage Therapy Silk route to the acceptance and re-implementation of bacteriophage therapy. Biotechnol. J. 2016;11:595–600. doi: 10.1002/biot.201600023. PubMed DOI

Cooper C.J., Khan Mirzaei M., Nilsson A.S. Adapting drug approval pathways for bacteriophage-based therapeutics. Front. Microbiol. 2016;7:1209. doi: 10.3389/fmicb.2016.01209. PubMed DOI PMC

Pirnay J.P., Verbeken G., Ceyssens P.-J., Huys I., de Vos D., Ameloot C., Fauconnier A. The magistral phage. Viruses. 2018;10:64. doi: 10.3390/v10020064. PubMed DOI PMC

Manrique P., Bolduc B., Walk S.T., van der Oost J., de Vos W.M., Young M.J. Healthy human gut phageome. Proc. Natl. Acad. Sci. USA. 2016;113:10400–10405. doi: 10.1073/pnas.1601060113. PubMed DOI PMC

Erez Z., Steinberger-Levy I., Shamir M., Doron S., Stokar-Avihail A., Peleg Y., Melamed S., Leavitt A., Savidor A., Albeck S., et al. Communication between viruses guides lysis-lysogeny decisions. Nature. 2017;541:488–493. doi: 10.1038/nature21049. PubMed DOI PMC

Howard-Varona C., Hargreaves K.R., Abedon S.T., Sullivan M.B. Lysogeny in nature: Mechanisms, impact and ecology of temperate phages. ISME J. 2017;11:1511–1520. doi: 10.1038/ismej.2017.16. PubMed DOI PMC

Thomas S., Izard J., Walsh E., Batich K., Chongsathidkiet P., Clarke G., Sela D.A., Muller A.J., Mullin J.M., Albert K., et al. The host microbiome regulates and maintains human health: A primer and perspective for non-microbiologists. Cancer Res. 2017;77:1783–1812. doi: 10.1158/0008-5472.CAN-16-2929. PubMed DOI PMC

Blasdel B.G., Ceyssens P.J., Chevallereau A., Debarbieux L., Lavigne R. Comparative transcriptomics reveals a conserved Bacterial Adaptive Phage Response (BAPR) to viral predation. bioRxiv. 2018 doi: 10.1101/248849. DOI

Lwoff A. Lysogeny. Bacteriol. Rev. 1953;17:269–337. PubMed PMC

Nanda A.M., Heyer A., Krämer C., Grünberger A., Kohlheyer D., Frunzke J. Analysis of SOS-induced spontaneous prophage induction in Corynebacterium glutamicum at the single-cell level. J. Bacteriol. 2014;196:180–188. doi: 10.1128/JB.01018-13. PubMed DOI PMC

Colon M.P., Chakraborty D., Pevzner Y., Koudelka G.B. Mechanisms that determine the differential stability of Stx(+) and Stx(−) lysogens. Toxins. 2016;8:96. doi: 10.3390/toxins8040096. PubMed DOI PMC

Łobocka M., Hejnowicz M.S., Dąbrowski K., Izak D., Gozdek A., Głowacka A., Gawor J., Kosakowski J., Gromadka R., Weber-Dąbrowska B., et al. Staphylococcus aureus Strains for the Production of Monoclonal Bacteriophage Preparations Deprived of Contamination with Plasmid DNA. WO 2016/030871 A1. U.S. Patent. 2016 Mar 16;

Fortier L.C., Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence. 2013;4:354–365. doi: 10.4161/viru.24498. PubMed DOI PMC

Colavecchio A., Cadieux B., Lo A., Goodridge L.D. Bacteriophages contribute to the spread of antibiotic resistance genes among foodborne pathogens of the Enterobacteriaceae family—A review. Front. Microbiol. 2017;8:1108. doi: 10.3389/fmicb.2017.01108. PubMed DOI PMC

Feiner R., Argov T., Rabinovich L., Sigal N., Borovok L., Herskovits A.A. A new perspective on lysogeny: Prophages as active regulatory switches of bacteria. Nat. Rev. Microbiol. 2015;13:641–650. doi: 10.1038/nrmicro3527. PubMed DOI

Canchaya C., Desiere F., Mcshan W.M., Ferretti J.J., Parkhill J., Brüssow H. Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology. 2002;302:245–258. doi: 10.1006/viro.2002.1570. PubMed DOI

Touchon M., Bernheim A., Rocha E.P. Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J. 2016;10:2744–2754. doi: 10.1038/ismej.2016.47. PubMed DOI PMC

Maslanova I., Stribna S., Doskar J., Pantucek R. Efficient plasmid transduction to Staphylococcus aureus strains insensitive to the lytic action of transducing phage. FEMS Microbiol. Lett. 2016;363 doi: 10.1093/femsle/fnw211. PubMed DOI

Haaber J., Leisner J.L., Cohn M.T., Catalan-Moreno A., Nielsen J.B., Westh H., Penadés J.R., Ingmer H. Bacterial viruses enable their host to acquire antibiotic resistance genes from neighbouring cells. Nat. Commun. 2016;7:13333. doi: 10.1038/ncomms13333. PubMed DOI PMC

Akhter S., Aziz R.K., Edwards R.A. PhiSpy: A novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res. 2012;40:e126. doi: 10.1093/nar/gks406. PubMed DOI PMC

Arndt D., Grant J.R., Marcu A., Sajed T., Pon A., Liang Y., Wishart D.S. PHASTER: A better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44:W16–W21. doi: 10.1093/nar/gkw387. PubMed DOI PMC

Ceyssens P.J., Minakhin L., Van den Bossche A., Yakunina M., Klimuk E., Blasdel B.G., de Smet J., Noben J.P., Bläsi U., Severinov K., et al. Development of giant bacteriophage φKZ is independent of the host transcription apparatus. J. Virol. 2018;88:10501–10510. doi: 10.1128/JVI.01347-14. PubMed DOI PMC

Łobocka M., Hejnowicz M.S., Gągała U., Weber-Dąbrowska B., Węgrzyn G., Dadlez M. The first step to bacteriophage therapy—How to choose the correct phage. In: Borysowski J., Międzybrodzki R., Górski A., editors. Phage Therapy: Current Research and Applications. Caister Academic Press; Poole, UK: 2004. pp. 23–69.

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