Safety analysis of a Russian phage cocktail: From MetaGenomic analysis to oral application in healthy human subjects

Virology

Volumn 443, Issue 2, 2013, Pages 187-196

  McCallin, Shawna ^a   Alam Sarker, Shafiqul ^b   Barretto, Caroline ^a   Sultana, Shamima ^b   Berger, Bernard ^a   Huq, Sayeda ^b   Krause, Lutz ^a,c   Bibiloni, Rodrigo ^a,d   Schmitt, Bertrand ^a   Reuteler, Gloria ^a   Brüssow, Harald ^a  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

^b INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d RUAKURA RESEARCH CENTRE   (New Zealand)

Author keywords

Bacteriophages; Escherichia coli; Fecal microbiota; Human phage therapy; Metagenomics; Safety

Indexed keywords

MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; PLACEBO;

ABDOMINAL PAIN; ADULT; ALLERGY; ANTIBODY BLOOD LEVEL; ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE T4; BACTERIOPHAGE T7; BIOINFORMATICS; BIOSAFETY; CHILD; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DRUG MEGADOSE; DYSPEPSIA; ELECTRON MICROSCOPY; ESCHERICHIA COLI INFECTION; FECES MICROFLORA; FEMALE; HUMAN; HUMAN EXPERIMENT; LOOSE FECES; LOW DRUG DOSE; MALE; METAGENOMICS; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; OTALGIA; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEUS INFECTION; SCHOOL CHILD; SIDE EFFECT; TOOTH PAIN; URTICARIA;

BACTERIOPHAGES; ESCHERICHIA COLI; FECAL MICROBIOTA; HUMAN PHAGE THERAPY; METAGENOMICS; SAFETY;

ADMINISTRATION, ORAL; BACTERIOPHAGES; BIOLOGICAL THERAPY; ESCHERICHIA COLI INFECTIONS; GRAM-NEGATIVE BACTERIA; HUMANS; METAGENOMICS; MICROSCOPY, ELECTRON, TRANSMISSION; MYOVIRIDAE; PODOVIRIDAE; PROTEUS INFECTIONS; RUSSIA; SIPHOVIRIDAE; TREATMENT OUTCOME;

ESCHERICHIA; ESCHERICHIA COLI; MYOVIRIDAE; PODOVIRIDAE; SIPHOVIRIDAE;

EID: 84880787826     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.05.022     Document Type: Article

References (49)

1. Barondess J.J., Beckwith J. bor gene of phage lambda, involved in serum resistance, encodes a widely conserved outer membrane lipoprotein. J. Bacteriol. 1995, 177:1247-1253.
2. Breitbart M., Salamon P., Andresen B., Mahaffy J.M., Segall A.M., Mead D., Azam F., Rohwer F. Genomic analysis of uncultured marine viral communities. Proc. Nat. Acad. Sci. U.S.A. 2002, 99(22):14250-14255.
3. Brüssow H. Bacteriophage-host interaction: from splendid isolation into a messy reality. Curr. Opin. Microbiol. 2013, in press.
4. Brüssow H. Phage therapy: the Escherichia coli experience. Microbiology 2005, 151:2133-2140.
5. Brüssow H. Control of bacterial diarrhea with phages: coverage and safety issues of bacteriophage therapy. Bacteriophages in the Control of Food- and Waterborne Pathogens 2010, 273-295. ASM Press, Washington DC. P.M. Sarbour, M.W. Griffiths (Eds.).
6. Brüssow H. What is needed for phage therapy to become a reality in Western medicine?. Virology 2012, 434:138-142.
7. Brüssow H., Canchaya C., Hardt W.D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 2004, 68:560-602.
8. Bull J.J., Vimr E.R., Molineux I.J. A tale of tails: Sialidase is key to success in a model of phage therapy against K1-capsulated Escherichia coli. Virology 2010, 398:79-86.
9. Choi S.H., Baumler D.J., Kaspar C.W. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 2000, 66:3911-3916.
10. Comeau A.M., Bertrand C., Letarov A., Tétart F., Krisch H.M. Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 2007, 362:384-396.
11. Denou E., Bruttin A., Barretto C., Ngom-Bru C., Brüssow H., Zuber S. T4 phages against Escherichia coli diarrhea: potentials and problems. Virology 2009, 388:21-23.
12. Häusler T. Viruses vs. Superbugs: A Solution to the Antibiotics Crisis? 2007, Macmillian Press, New York.
13. Huson D.H., Mitra S. Introduction to the analysis of environmental sequences: metagenomics with MEGAN. Methods Mol. Biol. 2012, 856:415-429.
14. King M.R., Vimr R.P., Steenbergen S.M., Spanjaard L., Plunkett G., Blattner F.R., Vimr E.R. Escherichia coli K1-specific bacteriophage CUS-3 distribution and function in phase-variable capsular polysialic acid O acetylation. J. Bacteriol. 2007, 189:6447-6456.
15. Kulikov E., Kropinski A.M., Golomidova A., Lingohr E., Govorun V., Serebryakova M., Prokhorov N., Letarova M., Manykin A, Strotskaya A, Letarov A. Isolation and characterization of a novel indigenous intestinal N4-related coliphage vB_EcoP_G7C. Virology 2012, 426:93-99.
16. Maura D., Morello E., du Merle L., Bomme P., Le Bouguénec C., Debarbieux L. Intestinal colonization by enteroaggregative Escherichia coli supports long-term bacteriophage replication in mice. Environ. Microbiol. 2012, 14:1844-1854.
17. Maura D., Galtier M., Le Bouguénec C., Debarbieux L. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob. Agents Chemother. 2012, 56(12):6235-6242.
18. Merabishvili M., Pirnay J.P., Verbeken G., Chanisvili N., Tediashvili M., Lashkhi N., Glonti T., Krylov V., Mast J., Van Parys L., Lavigne R., Volckaert G., Mattheus W., Verween G., De Corte P., Rose T., Jennes S., Zizi M., De Vos D., Vaneechoutte M. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS One 2009, 4:e4944.
19. Miller E.S., Kutter E., Mosig G., Arisaka F., Kunisawa T., Rüger W. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 2003, 67:86-156.
20. Ng T.F., Willner D.L., Lim Y.W., Schmieder R., Chau B., Nilsson C., Anthony S., Ruan Y., Rohwer F., Breitbart M. Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 2011, 6(6):e20579.
21. Perry L.L., SanMiguel P., Minocha U., Terekhov A.I., Shroyer M.L., Farris L.A., Bright N., Reuhs B.L., Applegate B.M. Sequence analysis of Escherichia coli O157:H7 bacteriophage PhiV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol. Lett. 2009, 292:182-186.
22. Pride D.T., Salzman J., Haynes M., Rohwer F., Davis-Long C., White R.A., Loomer P., Armitage G.C., Relman D.A. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J. 2012, 5:915-926.
23. Reyes A., Haynes M., Hanson N., Angly F.E., Heath A.C., Rohwer F., Gordon, J.I.Jeffrey I. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010, 466:334-338.
24. Reyes A., Semenkovich N.P., Whiteson K., Rohwer F., Gordon J.I. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat. Rev. Microbiol. 2012, 10(9):607-617.
25. Rhoads D.D., Wolcott R.D., Kuskowski M.A., Wolcott B.M., Ward L.S., Sulakvelidze A. Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J. Wound Care 2009, 18:237-243.
26. Santos S.B., Kropinski A.M., Ceyssens P.J., Ackermann H.W., Villegas A., Lavigne R., Krylov V.N., Carvalho C.M., Ferreira E.C., Azeredo J. Genomic and proteomic characterization of the broad-host-range Salmonella phage PVP-SE1: creation of a new phage genus. J. Virol. 2011, 85:11265-11273.
27. Sarker S.A., McCallin S., Barretto C., Berger B., Pittet A.-C., Sultana S., Krause L., Huq S., Bibiloni R., Bruttin A., Reuteler G., Brüssow H. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 2012, 434:222-232.
28. Scholl D., Adhya S., Merril C.R. Bacteriophage SP6 is closely related to phages K1-5, K5, and K1E but encodes a tail protein very similar to that of the distantly related P22. J. Bacteriol. 2002, 184:2833-2836.
29. Scholl D., Kieleczawa J., Kemp P., Rush J., Richardson C.C., Merril C., Adhya S., Molineux I.J. Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. J. Mol. Biol. 2004, 335:1151-1171.
30. Scholl D., Merril C. The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli. J. Bacteriol. 2005, 187:8499-8503.
31. Schwarzer D., Buettner F.F., Browning C., Nazarov S., Rabsch W., Bethe A., Oberbeck A., Bowman V.D., Stummeyer K., Mühlenhoff M., Leiman P.G., Gerardy-Schahn R. A multivalent adsorption apparatus explains the broad host range of phage phi92: a comprehensive genomic and structural analysis. J. Virol. 2012, 86:10384-10398.
32. Smith H.W., Huggins M.B. Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J. Gen. Microbiol. 1982, 128:307-318.
33. Stone R. Bacteriophage therapy. Stalin's Forgotten Cure. Science 2002, 298(5594):728-731.
34. Sulakvelidze A., Alavidze Z., Morris J.G. Bacteriophage therapy. Antimicrob. Agents Chemother. 2001, 45:649-659.
35. Sulakvelidze A., Kutter E. Bacteriophage therapy in humans. Bacteriophages-Biology and Applications 2005, 381-436. CRC Press, Boca Raton. E. Kutter, A. Sulakvelidze (Eds.).
36. Teeling H., Glöckner F.O. Current opportunities and challenges in microbial metagenome analysis-a bioinformatic perspective. Briefings in Bioinformatics 2012.
37. Tétart F., Desplats C., Krisch H.M. Genome plasticity in the distal tail fiber locus of the T-even bacteriophage: recombination between conserved motifs swaps adhesin specificity. J. Mol. Biol. 1998, 282:543-556.
38. Tse H., Tsang A.K., Tsoi H.W., Leung A.S., Ho C.C., Lau S.K., Woo P.C., Yuen K.Y. Identification of a novel bat papillomavirus by metagenomics. PLoS One 2012, 7(8):e43986.
39. Tsonos J., Adriaenssens E.M., Klumpp J., Hernalsteens J.P., Lavigne R., De-Greve H. Complete genome sequence of the novel Escherichia coli phage phAPEC8. J. Virol. 2012, 86:13117-13118.
40. Victoria J.G., Kapoor A., Li L., Blinkova O, Slikas B., Wang C., Naeem A., Zaidi S., Delwart E. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J. Virol. 2009, 83(9):4642-4651.
41. Villegas A., She Y.M., Kropinski A.M., Lingohr E.J., Mazzocco A., Ojha S., Waddell T.E., Ackermann H.W., Moyles D.M., Ahmed R., Johnson R.P. The genome and proteome of a virulent Escherichia coli O157:H7 bacteriophage closely resembling Salmonella phage Felix O1. Virol. J. 2009, 6:41.
42. Weiss M., Denou E., Bruttin A., Serra-Moreno R., Dillmann M.L., Brüssow H. In vivo replication of T4 and T7 bacteriophages in germ-free mice colonized with Escherichia coli. Virology 2009, 393:16-23.
43. Wietzorrek A., Schwarz H., Herrmann C., Braun V. The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage T1. J. Bacteriol. 2006, 188:1419-1436.
44. Willner D., Furlan M., Haynes M., Schmieder R., Angly F.E., Silva J., Tammadoni S., Nosrat B., Conrad D., Rohwer F. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 2009, 4(10):e7370.
45. Whichard J.M., Weigt L.A., Borris D.J., Li L.L., Zhang Q., Kapur V., Pierson F.W., Lingohr E.J., She Y.M., Kropinski A.M., Sriranganathan N. Complete genomic sequence of bacteriophage felix o1. Viruses 2010, 2:710-730.
46. WHO The evolving threat of antimicrobial resistance. Options for Action 2012, L. Martinez (Ed.), Geneva.
47. Wright A., Hawkins C.H., Anggard E.E., Harper D.R. A controlled clinical trial of a therapeutical bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin. Otolaryngol. 2009, 34:349-357.
48. Zhu J., Rao X., Tan Y., Xiong K., Hu Z., Chen Z., Jin X., Li S., Chen Y., Hu F. Identification of lytic bacteriophage MmP1, assigned to a new member of T7-like phages infecting Morganella morganii. Genomics 2010, 96:167-172.
49. Zuber S., Ngom-Bru C., Barretto C., Bruttin A., Brüssow H., Denou E. Genome analysis of phage JS98 defines a fourth major subgroup of T4-like phages in Escherichia coli. J. Bacteriol. 2007, 189:8206-8214.