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Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases

Abstract

Bacteriophage (phage) therapy involves using phages or their products as bioagents for the treatment or prophylaxis of bacterial infectious diseases. Much evidence in support of the effectiveness of phage therapy against bacterial infectious diseases has accumulated since 1980 from animal model studies conducted in Western countries. Reports indicate that appropriate administration of living phages can be used to treat lethal infectious diseases caused by gram-negative bacteria, such as Escherichia coli, Pseudomonas aeruginosa, Acinetobacter baumannii, Klebsiella pneumoniae, Vibrio vulnificus, and Salmonella spp., and gram-positive bacteria, such as Enterococcus faecium and Staphylococcus aureus. The phage display system and genetically modified nonreplicating phages are also effective for treatment of Helicobacter pylori and P. aeruginosa, respectively. In addition to phage particles per se, purified phage-encoded peptidoglycan hydrolase (lysin) is also reported to be effective for the treatment of bacterial infectious diseases caused by gram-positive bacteria such as Streptococcus pyogenes, S. pneumoniae, Bacillus anthracis, and group B streptococci. All phage lysins that have been studied to date exhibit immediate and strong bacteriolytic activity when applied exogenously. Furthermore, phage-coded inhibitors of peptidoglycan synthesis (protein antibiotics), search methods for novel antibacterial agents using phage genome informatics, and vaccines utilizing phages or their products are being developed. Phage therapy will compensate for unavoidable complications of chemotherapy such as the appearance of multidrug resistance or substituted microbism.

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References

  1. WC Summers (1999) Félix d'Herelle and the origins of molecular biology Yale University Press Connecticut

    Google Scholar 

  2. K Ho (2001) ArticleTitleBacteriophage therapy for bacterial infections. Rekindling a memory from the pre-antibiotics era Perspect Biol Med 44 1–16 Occurrence Handle11253299

    PubMed  Google Scholar 

  3. A Sulakvelidze Z Alavidze JG Morris SuffixJr (2001) ArticleTitleBacteriophage therapy Antimicrob Agents Chemother 45 649–59 Occurrence Handle10.1128/AAC.45.3.649-659.2001 Occurrence Handle11181338

    Article  PubMed  Google Scholar 

  4. S Slopek B Weber-Dabrowska M Dabrowski A Kucharewicz-Krukowska (1987) ArticleTitleResults of bacteriophage treatment of suppurative bacterial infections in the years 1981–1986 Arch Immunol Ther Exp 35 569–83

    Google Scholar 

  5. J Alisky K Iczkowski A Rapoport N Troitsky (1998) ArticleTitleBacteriophages show promise as antimicrobial agents J Infect 36 5–15 Occurrence Handle10.1016/S0163-4453(98)92874-2 Occurrence Handle9515662

    Article  PubMed  Google Scholar 

  6. B Weber-Dabrowska M Mulczyk A Górski (2000) ArticleTitleBacteriophage therapy of bacterial infections: an update of our institute's experience Arch Immunol Ther Exp 48 547–51

    Google Scholar 

  7. Chanishvili N, Tediashvili M, Chanishvili T. Phages and experience for their application in the former Soviet Union. IUMS Congress (Paris); 2002

  8. Phage therapy [editorial]. Lancet 1983;2:1287–8

  9. J Lederberg (1996) ArticleTitleSmaller fleas . . . ad infinitum: therapeutic bacteriophage redux Proc Natl Acad Sci USA 93 3617–8 Occurrence Handle10.1073/pnas.93.8.3167

    Article  Google Scholar 

  10. PA Barrow JM Soothill (1997) ArticleTitleBacteriophage therapy and prophylaxis: rediscovery and renewed assessment of potential Trends Microbiol 5 268–71 Occurrence Handle10.1016/S0966-842X(97)01054-8 Occurrence Handle9234508

    Article  PubMed  Google Scholar 

  11. RM Carlton (1999) ArticleTitlePhage therapy: past history and future prospects Arch Immunol Ther Exp 5 267–74

    Google Scholar 

  12. A Pirisi (2000) ArticleTitlePhage therapy-advantages over antibiotics? Lancet 356 1418 Occurrence Handle10.1016/S0140-6736(05)74059-9 Occurrence Handle11052592

    Article  PubMed  Google Scholar 

  13. P Das (2001) ArticleTitleBacteriophage therapy offers new hope for streptococcal infections Lancet 357 938 Occurrence Handle10.1016/S0140-6736(05)71639-1

    Article  Google Scholar 

  14. R Stone (2002) ArticleTitleBacteriophage therapy. Stalin's forgotten cure Science 298 728–31 Occurrence Handle10.1126/science.298.5594.728 Occurrence Handle12399562

    Article  PubMed  Google Scholar 

  15. CR Merril D Scholl L Adhya (2003) ArticleTitleThe prospect for bacteriophage therapy in Western medicine Nat Rev Drug Discov 2 489–97 Occurrence Handle10.1038/nrd1111 Occurrence Handle12776223

    Article  PubMed  Google Scholar 

  16. PD Thacker (2003) ArticleTitleSet a microbe to kill a microbe: drug resistance renews interest in phage therapy JAMA 290 3183–5 Occurrence Handle10.1001/jama.290.24.3183 Occurrence Handle14693857

    Article  PubMed  Google Scholar 

  17. J Bradbury (2004) ArticleTitleMy enemy's enemy is my friend.” Using phages to fight bacteria Lancet 363 624–5 Occurrence Handle10.1016/S0140-6736(04)15629-8 Occurrence Handle14989277

    Article  PubMed  Google Scholar 

  18. B Dixon (2004) ArticleTitleNew dawn for phage therapy Lancet Infect Dis 4 186 Occurrence Handle10.1016/S1473-3099(04)00951-X Occurrence Handle14998510

    Article  PubMed  Google Scholar 

  19. BR Levin JJ Bull (2004) ArticleTitlePopulation and evolutionary dynamics of phage therapy Nat Rev Microbiol 2 166–73 Occurrence Handle10.1038/nrmicro822 Occurrence Handle15040264

    Article  PubMed  Google Scholar 

  20. Renaissance phage [editorial]. Nat Rev Microbiol 2004;2:922

    Google Scholar 

  21. H-W Ackermann MS DuBow (1987) Viruses of prokaryotes. I. General properties of bacteriophages CRC Press Florida

    Google Scholar 

  22. H-W Ackermann (2001) ArticleTitleFrequency of morphological phage descriptions in the year 2000 Arch Virol 146 843–57 Occurrence Handle10.1007/s007050170120 Occurrence Handle11448025

    Article  PubMed  Google Scholar 

  23. S Matsuzaki T Inoue M Kuroda S Kimura S Tanaka (1998) ArticleTitleCloning and sequencing of major capsid protein (mcp) gene of a vibriophage, KVP20, possibly related to T-even coliphages Gene (Amst) 222 25–30 Occurrence Handle10.1016/S0378-1119(98)00459-4

    Article  Google Scholar 

  24. S Matsuzaki S Tanaka T Koga T Kawata (1992) ArticleTitleA broad-host-range vibriophage, KVP40, isolated from sea water Microbiol Immunol 36 93–7 Occurrence Handle1584076

    PubMed  Google Scholar 

  25. S Matsuzaki T Inoue S Tanaka (1992) ArticleTitleEvidence for the existence of a restriction-modification system common to several species of the family Vibrionaceae FEMS Microbiol Lett 94 191–4 Occurrence Handle10.1016/0378-1097(92)90607-P

    Article  Google Scholar 

  26. T Inoue S Matsuzaki S Tanaka (1995) ArticleTitleA 26-kDa outer membrane protein, OmpK, common to Vibrio species is the receptor for a broad-host-range vibriophage, KVP40 FEMS Microbiol Lett 125 101–6 Occurrence Handle10.1016/0378-1097(94)00480-F Occurrence Handle7867914

    Article  PubMed  Google Scholar 

  27. T Inoue S Matsuzaki S Tanaka (1995) ArticleTitleCloning and sequence analysis of Vibrio parahaemolyticus ompK gene encoding a 26-kDa outer membrane protein, OmpK, that serves as receptor for a broad-host-range vibriophage, KVP40 FEMS Microbiol Lett 134 245–49 Occurrence Handle10.1016/0378-1097(95)00414-9 Occurrence Handle8586275

    Article  PubMed  Google Scholar 

  28. S Matsuzaki T Inoue S Tanaka (1998) ArticleTitleA vibriophage, KVP40, with major capsid protein homologous to gp23* of coliphage T4 Virology 242 314–18 Occurrence Handle10.1006/viro.1997.9018 Occurrence Handle9514973

    Article  PubMed  Google Scholar 

  29. S Matsuzaki M Kuroda S Kimura S Tanaka (1999) ArticleTitleMajor capsid proteins of certain Vibrio and Aeromonas phages are homologous to the equivalent protein, gp23*, of coliphage T4 Arch Virol 144 1647–51 Occurrence Handle10.1007/s007050050618 Occurrence Handle10486118

    Article  PubMed  Google Scholar 

  30. S Matsuzaki M Kuroda S Kimura S Tanaka (1999) ArticleTitleVibriophage KVP40 and coliphage T4 genomes share a homologous 7-kbp region immediately upstream of the gene encoding the major capsid protein Arch Virol 144 2007–12 Occurrence Handle10.1007/s007050050721 Occurrence Handle10550672

    Article  PubMed  Google Scholar 

  31. MS Mitchel S Matsuzaki S Imai VB Rao (2002) ArticleTitleSequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases Nucleic Acids Res 30 4009–21 Occurrence Handle10.1093/nar/gkf524 Occurrence Handle12235385

    Article  PubMed  Google Scholar 

  32. S Matsuzaki T Inoue S Tanaka T Koga M Kuroda S Kimura S Imai (2000) ArticleTitleCharacterization of a novel Vibrio parahaemolyticus phage, KVP241, and its relatives frequently isolated from seawater Microbiol Immunol 44 953–56 Occurrence Handle11145278

    PubMed  Google Scholar 

  33. S Matsuzaki M Yasuda H Nishikawa M Kuroda T Ujihara T Shuin et al. (2003) ArticleTitleExperimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage S61542MR11 J Infect Dis 187 613–24 Occurrence Handle10.1086/374001 Occurrence Handle12599078

    Article  PubMed  Google Scholar 

  34. J Maniloff H-W Ackermann (1998) ArticleTitleTaxonomy of bacterial viruses: establishment of tailed virus genera and the order Caudovirales Arch Virol 143 2051–63 Occurrence Handle10.1007/s007050050442 Occurrence Handle9856093

    Article  PubMed  Google Scholar 

  35. TG Bernhardt WD Roof R Young (2000) ArticleTitleGenetic evidence that the bacteriophage S61542X174 lysis protein inhibits cell wall synthesis Proc Natl Acad Sci USA 97 4297–302 Occurrence Handle10.1073/pnas.97.8.4297 Occurrence Handle10760296

    Article  PubMed  Google Scholar 

  36. TG Bernhardt DK Struck R Young (2000) ArticleTitleThe lysis protein E of S61542X174 is a specific inhibitor of the MraY-catalyzed step in peptidoglycan synthesis J Biol Chem 276 6093–7 Occurrence Handle10.1074/jbc.M007638200 Occurrence Handle11078734

    Article  PubMed  Google Scholar 

  37. TG Bernhardt I-N Wang DK Struck R Young (2001) ArticleTitleA protein antibiotic in the phage QS61538 virion: diversity in lysis target Science 292 2326–9 Occurrence Handle10.1126/science.1058289 Occurrence Handle11423662

    Article  PubMed  Google Scholar 

  38. J Cao Y Sun T Berglindh B Mellgard Z Li B Mardh S Mardh (2000) ArticleTitleHelicobacter pylori-antigen-binding fragments expressed on the filamentous M13 phage prevent bacterial growth Biochem Biophys Acta 1474 107–13 Occurrence Handle10699497

    PubMed  Google Scholar 

  39. S Hagens A Habel U von Ahsen A von Gabain U Blasi (2004) ArticleTitleTherapy of experimental pseudomonas infections with a nonreplicating genetically modified phage Antimicrob Agents Chemother 48 3817–22 Occurrence Handle10.1128/AAC.48.10.3817-3822.2004 Occurrence Handle15388440

    Article  PubMed  Google Scholar 

  40. MJ Betley JJ Mekalanos (1985) ArticleTitleStaphylococcal enterotoxin A is encoded by phage Science 229 185–7 Occurrence Handle3160112

    PubMed  Google Scholar 

  41. WR Bishai JR Murphy (1988) Bacteriophage gene products that cause human diseases R Calendar (Eds) The bacteriophages Plenum Press New York and London 683–724

    Google Scholar 

  42. J Kaneko T Kimura Y Kawakami T Tomita Y Kamio (1997) ArticleTitlePanton-valentine leukocidin genes in a phage-like particle isolated from mitomycin C-treated Staphylococcus aureus V8 (ATCC 49775) Biosci Biotechnol Biochem 61 1960–2 Occurrence Handle9404084

    PubMed  Google Scholar 

  43. J Kaneko T Kimura S Narita T Tomita Y Kamio (1998) ArticleTitleComplete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage S61542PVL carrying Panton–Valentine leukocidin genes Gene (Amst) 215 57–67 Occurrence Handle10.1016/S0378-1119(98)00278-9

    Article  Google Scholar 

  44. T Yamaguchi T Hayashi H Takami K Nakasone M Ohnishi K Nakayama et al. (2000) ArticleTitlePhage conversion of exfoliative toxin A production in Staphylococcus aureus Mol Microbiol 38 694–705 Occurrence Handle10.1046/j.1365-2958.2000.02169.x Occurrence Handle11115106

    Article  PubMed  Google Scholar 

  45. RY Young (1992) ArticleTitleBacteriophage lysis: mechanism and regulation Microbiol Rev 56 430–81 Occurrence Handle1406491

    PubMed  Google Scholar 

  46. H-W Ackermann (1998) ArticleTitleTailed bacteriophages: the order Caudovirales Adv Virus Res 51 135–201 Occurrence Handle9891587

    PubMed  Google Scholar 

  47. IN Wang DL Smith R Young (2000) ArticleTitleHolins: the protein clocks of bacteriophage infections Annu Rev Microbiol 54 799–825 Occurrence Handle10.1146/annurev.micro.54.1.799 Occurrence Handle11018145

    Article  PubMed  Google Scholar 

  48. HW Smith MB Huggins (1982) ArticleTitleSuccessful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics J Gen Microbiol 128 307–18 Occurrence Handle7042903

    PubMed  Google Scholar 

  49. HW Smith MB Huggins (1983) ArticleTitleEffectiveness of phages in treating experimental Escherichia coli diarrhoea in calves, piglets, and lambs J Gen Microbiol 129 2659–75 Occurrence Handle6355391

    PubMed  Google Scholar 

  50. HW Smith MB Huggins KM Shaw (1987) ArticleTitleFactors influencing the survival and multiplication of bacteriophages in calves and in their environment J Gen Microbiol 133 1127–35 Occurrence Handle3309178

    PubMed  Google Scholar 

  51. HW Smith MB Huggins KM Shaw (1987) ArticleTitleThe control of experimental Escherichia coli diarrhoea in calves by means of bacteriophages J Gen Microbiol 133 1111–26 Occurrence Handle3309177

    PubMed  Google Scholar 

  52. CR Merril B Biswas R Carlton NC Jensen GJ Creed S Zullo et al. (1996) ArticleTitleLong-circulating bacteriophage as antibacterial agents Proc Natl Acad Sci USA 93 3188–92 Occurrence Handle10.1073/pnas.93.8.3188 Occurrence Handle8622911

    Article  PubMed  Google Scholar 

  53. P Barrow M Lovell A Berchieri SuffixJr (1998) ArticleTitleUse of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves Clin Diagn Lab Immunol 5 294–8 Occurrence Handle9605979

    PubMed  Google Scholar 

  54. S Chibani-Chennoufi J Sidoti A Bruttin E Kutter S Sarker H Brussow (2004) ArticleTitleIn vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy Antimicrob Agents Chemother 48 2558–69 Occurrence Handle10.1128/AAC.48.7.2558-2569.2004 Occurrence Handle15215109

    Article  PubMed  Google Scholar 

  55. JS Soothill (1992) ArticleTitleTreatment of experimental infections of mice with bacteriophages J Med Microbiol 37 258–61 Occurrence Handle1404324

    PubMed  Google Scholar 

  56. JS Soothill (1994) ArticleTitleBacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa Burns 20 209–11 Occurrence Handle10.1016/0305-4179(94)90184-8 Occurrence Handle8054131

    Article  PubMed  Google Scholar 

  57. SI Ahmad (2002) ArticleTitleTreatment of post-burns bacterial infections by bacteriophages, specifically ubiquitous Pseudomonas spp. notoriously resistant to antibiotics Med Hypotheses 58 327–31 Occurrence Handle10.1054/mehy.2001.1522 Occurrence Handle12027527

    Article  PubMed  Google Scholar 

  58. GG Bogovazova NN Voroshilova VM Bondarenko (1991) ArticleTitleThe efficacy of Klebsiella pneumoniae bacteriophage in the therapy of experimental Klebsiella infection Zh Mikrobiol Epidemiol Immunobiol 4 5–8 Occurrence Handle1882608

    PubMed  Google Scholar 

  59. GG Bogovazova NN Voroshilova VM Bondarenko GA Gorbatkova EV Afanas'eva TB Kazakova et al. (1992) ArticleTitleImmunobiological properties and therapeutic effectiveness of preparations from Klebsiella bacteriophages Zh Mikrobiol Epidemiol Immunobiol 3 30–3 Occurrence Handle1380753

    PubMed  Google Scholar 

  60. B Biswas S Adhya P Washart B Paul AN Trostel B Powell et al. (2002) ArticleTitleBacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium Infect Immun 70 204–10 Occurrence Handle10.1128/IAI.70.1.204-210.2002 Occurrence Handle11748184

    Article  PubMed  Google Scholar 

  61. KE Cerveny A DePaola DH Duckworth PA Gulig (2002) ArticleTitlePhage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice Infect Immun 70 6251–62 Occurrence Handle10.1128/IAI.70.11.6251-6262.2002 Occurrence Handle12379704

    Article  PubMed  Google Scholar 

  62. H Toro SB Price AS McKee FJ Hoerr J Krehling M Perdue et al. (2005) ArticleTitleUse of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens Avian Dis 49 118–24 Occurrence Handle15839424

    PubMed  Google Scholar 

  63. WC Noble (1998) Staphylococcal diseases Microbiology and microbial infections. Vol 3 Oxford University Press New York 231–56

    Google Scholar 

  64. K Hiramatsu L Cui M Kuroda T Ito (2001) ArticleTitleThe emergence and evolution of methicillin-resistant Staphylococcus aureus Trends Microbiol 9 486–93 Occurrence Handle10.1016/S0966-842X(01)02175-8 Occurrence Handle11597450

    Article  PubMed  Google Scholar 

  65. K Shimada K Nakano J Igari T Oguri H Ikemoto T Mori et al. (2004) ArticleTitle[Susceptibilities of bacteria isolated from patients with lower respiratory infectious diseases to antibiotics (2002)] Jpn J Antibiot 57 213–45 Occurrence Handle15376784

    PubMed  Google Scholar 

  66. K Hiramatsu N Aritaka H Hanaki S Kawasaki Y Hosoda S Hori et al. (1997) ArticleTitleDissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin Lancet 350 1670–3 Occurrence Handle10.1016/S0140-6736(97)07324-8 Occurrence Handle9400512

    Article  PubMed  Google Scholar 

  67. S Chang DM Sievert JC Hageman ML Boulton FC Tenover FP Downes et al. (2003) ArticleTitleInfection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene N Engl J Med 348 1342–7 Occurrence Handle10.1056/NEJMoa025025 Occurrence Handle12672861

    Article  PubMed  Google Scholar 

  68. M Kacica (2004) ArticleTitleVancomycin-resistant Staphylococcus aureus–New York, 2004 MMWR (Morb Mortal Wkly Rep) 53 322–3

    Google Scholar 

  69. SK Pillai G Sakoulas C Wennersten GM Eliopoulos RC Moellering SuffixJr MJ Ferraro et al. (2002) ArticleTitleLinezolid resistance in Staphylococcus aureus: characterization and stability of resistant phenotype J Infect Dis 186 1603–7 Occurrence Handle10.1086/345368 Occurrence Handle12447736

    Article  PubMed  Google Scholar 

  70. P Wilson JA Andrews R Charlesworth R Walesby M Singer DJ Farrell et al. (2003) ArticleTitleLinezolid resistance in clinical isolates of Staphylococcus aureus J Antimicrob Chemother 51 186–8 Occurrence Handle10.1093/jac/dkg104 Occurrence Handle12493812

    Article  PubMed  Google Scholar 

  71. JE Ross TR Anderegg HS Sader TR Fritsche RN Jones (2005) ArticleTitleTrends in linezolid susceptibility patterns in 2002: report from the worldwide Zyvox Annual Appraisal of Potency and Spectrum Program Diagn Microbiol Infect Dis 52 53–8 Occurrence Handle10.1016/j.diagmicrobio.2004.12.013 Occurrence Handle15878443

    Article  PubMed  Google Scholar 

  72. QF Wills C Kerrigan JS Soothill (2005) ArticleTitleExperimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model Antimicrob Agents Chemother 49 1220–1 Occurrence Handle10.1128/AAC.49.3.1220-1221.2005 Occurrence Handle15728933

    Article  PubMed  Google Scholar 

  73. S O'Flaherty RP Ross W Meaney GF Fitzgerald MF Elbreki A Coffey (2005) ArticleTitlePotential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals Appl Environ Microbiol 71 1836–42 Occurrence Handle10.1128/AEM.71.4.1836-1842.2005 Occurrence Handle15812009

    Article  PubMed  Google Scholar 

  74. MR Geier ME Trigg CR Merril (1973) ArticleTitleFate of bacteriophage lambda in non-immune germ-free mice Nature (Lond) 246 221–3 Occurrence Handle10.1038/246221a0

    Article  Google Scholar 

  75. T Nakai R Sugimoto KH Park S Matsuoka K Mori T Nishioka et al. (1999) ArticleTitleProtective effects of bacteriophage on experimental Lactococcus garvieae infection in yellowtail Dis Aquat Org 37 33–41 Occurrence Handle10439901

    PubMed  Google Scholar 

  76. SC Park I Shimamura M Fukunaga KI Mori T Nakai (2000) ArticleTitleIsolation of bacteriophages specific to a fish pathogen, Pseudomonas plecoglossicida, as a candidate for disease control Appl Environ Microbiol 66 1416–22 Occurrence Handle10.1128/AEM.66.4.1416-1422.2000 Occurrence Handle10742221

    Article  PubMed  Google Scholar 

  77. T Nakai SC Park (2002) ArticleTitleBacteriophage therapy of infectious diseases in aquaculture Res Microbiol 153 13–8 Occurrence Handle10.1016/S0923-2508(01)01280-3 Occurrence Handle11881893

    Article  PubMed  Google Scholar 

  78. SC Park T Nakai (2003) ArticleTitleBacteriophage control of Pseudomonas plecoglossicida infection in ayu Plecoglossus altivelis Dis Aquat Org 53 33–9 Occurrence Handle12608566

    PubMed  Google Scholar 

  79. B Leverentz WS Conway MJ Camp WJ Janisiewicz T Abuladze M Yang et al. (2003) ArticleTitleBiocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin Appl Environ Microbiol 69 4519–26 Occurrence Handle10.1128/AEM.69.8.4519-4526.2003 Occurrence Handle12902237

    Article  PubMed  Google Scholar 

  80. B Leverentz WS Conway W Janisiewicz MJ Camp (2004) ArticleTitleOptimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue J Food Prot 67 1682–6 Occurrence Handle15330534

    PubMed  Google Scholar 

  81. RJ Atterbury PL Connerton CE Dodd CE Rees IF Connerton (2003) ArticleTitleIsolation and characterization of Campylobacter bacteriophages from retail poultry Appl Environ Microbiol 69 4511–8 Occurrence Handle10.1128/AEM.69.8.4511-4518.2003 Occurrence Handle12902236

    Article  PubMed  Google Scholar 

  82. RJ Atterbury PL Connerton CE Dodd CE Rees IF Connerton (2003) ArticleTitleApplication of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni Appl Environ Microbiol 69 6302–6 Occurrence Handle10.1128/AEM.69.10.6302-6306.2003 Occurrence Handle14532096

    Article  PubMed  Google Scholar 

  83. D Goode VM Allen PA Barrow (2003) ArticleTitleReduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages Appl Environ Microbiol 69 5032–6 Occurrence Handle10.1128/AEM.69.8.5032-5036.2003 Occurrence Handle12902308

    Article  PubMed  Google Scholar 

  84. B Leverentz WS Conway Z Alavidze WJ Janisiewicz Y Fuchs MJ Camp et al. (2001) ArticleTitleExamination of bacteriophage as a biocontrol method for salmonella on fresh-cut fruit: a model study J Food Prot 64 1116–21 Occurrence Handle11510645

    PubMed  Google Scholar 

  85. RJ Payne D Phil VA Jansen (2000) ArticleTitlePhage therapy: the peculiar kinetics of self-replicating pharmaceuticals Clin Pharmacol Ther 68 225–30 Occurrence Handle10.1067/mcp.2000.109520 Occurrence Handle11014403

    Article  PubMed  Google Scholar 

  86. RJ Payne VA Jansen (2001) ArticleTitleUnderstanding bacteriophage therapy as a density-dependent kinetic process J Theor Biol 208 37–48 Occurrence Handle10.1006/jtbi.2000.2198 Occurrence Handle11162051

    Article  PubMed  Google Scholar 

  87. LM Kasman A Kasman C Westwater J Dolan MG Schmidt JS Norris (2002) ArticleTitleOvercoming the phage replication threshold: a mathematical model with implications for phage therapy J Virol 76 5557–64 Occurrence Handle10.1128/JVI.76.11.5557-5564.2002 Occurrence Handle11991984

    Article  PubMed  Google Scholar 

  88. RJ Payne VA Jansen (2002) ArticleTitleEvidence for a phage proliferation threshold? J Virol 76 13123–4 Occurrence Handle10.1128/JVI.76.24.13123-13124.2002 Occurrence Handle12438644

    Article  PubMed  Google Scholar 

  89. RJ Payne VA Jansen (2003) ArticleTitlePharmacokinetic principles of bacteriophage therapy Clin Pharmacokinet 42 315–25 Occurrence Handle12648024

    PubMed  Google Scholar 

  90. RJ Weld C Butts JA Heinemann (2004) ArticleTitleModels of phage growth and their applicability to phage therapy J Theor Biol 227 1–11 Occurrence Handle10.1016/S0022-5193(03)00262-5 Occurrence Handle14969703

    Article  PubMed  Google Scholar 

  91. WW Navarre H Ton-That KF Faull O Schneewind (1999) ArticleTitleMultiple enzymatic activities of the murein hydrolase from staphylococcal phage S6154211 J Biol Chem 274 15847–56 Occurrence Handle10.1074/jbc.274.22.15847 Occurrence Handle10336488

    Article  PubMed  Google Scholar 

  92. I Jado R Lopez E Garcia A Fenoll J Casal P Garcia (2003) ArticleTitlePhage lytic enzymes as therapy for antibiotic-resistant Streptococcus pneumoniae infection in a murine sepsis model J Antimicrob Chemother 52 967–73 Occurrence Handle10.1093/jac/dkg485 Occurrence Handle14613958

    Article  PubMed  Google Scholar 

  93. D Nelson L Loomis VA Fischetti (2001) ArticleTitlePrevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme Proc Natl Acad Sci USA 98 4107–12 Occurrence Handle10.1073/pnas.061038398 Occurrence Handle11259652

    Article  PubMed  Google Scholar 

  94. JM Loeffler D Nelson VA Fischetti (2001) ArticleTitleRapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase Science 294 2170–2 Occurrence Handle10.1126/science.1066869 Occurrence Handle11739958

    Article  PubMed  Google Scholar 

  95. JM Loeffler S Djurkovic VA Fischetti (2003) ArticleTitlePhage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia Infect Immun 71 6199–204 Occurrence Handle10.1128/IAI.71.11.6199-6204.2003 Occurrence Handle14573637

    Article  PubMed  Google Scholar 

  96. JM Loeffler VA Fischetti (2003) ArticleTitleSynergistic lethal effect of a combination of phage lytic enzymes with different activities on penicillin-sensitive and -resistant Streptococcus pneumoniae strains Antimicrob Agents Chemother 47 375–7 Occurrence Handle10.1128/AAC.47.1.375-377.2003 Occurrence Handle12499217

    Article  PubMed  Google Scholar 

  97. R Schuch D Nelson VA Fischetti (2002) ArticleTitleA bacteriolytic agent that detects and kills Bacillus anthracis Nature (Lond) 418 884–9 Occurrence Handle10.1038/nature01026

    Article  Google Scholar 

  98. Q Cheng D Nelson S Zhu VA Fischetti (2005) ArticleTitleRemoval of group B streptococci colonizing the vagina and oropharynx of mice with a bacteriophage lytic enzyme Antimicrob Agents Chemother 49 111–7 Occurrence Handle10.1128/AAC.49.1.111-117.2005 Occurrence Handle15616283

    Article  PubMed  Google Scholar 

  99. P Yoong R Schuch D Nelson VA Fischetti (2004) ArticleTitleIdentification of a broadly active phage lytic enzyme with lethal activity against antibiotic-resistant Enterococcus faecalis and Enterococcus faecium J Bacteriol 186 4808–12 Occurrence Handle10.1128/JB.186.14.4808-4812.2004 Occurrence Handle15231813

    Article  PubMed  Google Scholar 

  100. J Liu M Dehbi G Moeck F Arhin P Bauda D Bergeron et al. (2004) ArticleTitleAntimicrobial drug discovery through bacteriophage genomics Nat Biotechnol 22 185–91 Occurrence Handle10.1038/nbt932 Occurrence Handle14716317

    Article  PubMed  Google Scholar 

  101. TG Bernhardt IN Wang DK Struck R Young (2002) ArticleTitleBreaking free: “protein antibiotics” and phage lysis Res Microbiol 153 493–501 Occurrence Handle10.1016/S0923-2508(02)01330-X Occurrence Handle12437210

    Article  PubMed  Google Scholar 

  102. K Panthel W Jechlinger A Matis M Rohde M Szostak W Lubitz et al. (2003) ArticleTitleGeneration of Helicobacter pylori ghosts by S61542X174 protein E-mediated inactivation and their evaluation as vaccine candidates Infect Immun 71 109–16 Occurrence Handle10.1128/IAI.71.1.109-116.2003 Occurrence Handle12496155

    Article  PubMed  Google Scholar 

  103. JR Clark JB March (2004) ArticleTitleBacterial viruses as human vaccines? Expert Rev Vaccines 3 463–76 Occurrence Handle10.1586/14760584.3.4.463 Occurrence Handle15270651

    Article  PubMed  Google Scholar 

  104. CD Jepson JB March (2004) ArticleTitleBacteriophage lambda is a highly stable DNA vaccine delivery vehicle Vaccine 22 2413–9 Occurrence Handle10.1016/j.vaccine.2003.11.065 Occurrence Handle15193403

    Article  PubMed  Google Scholar 

  105. JB March JR Clark CD Jepson (2004) ArticleTitleGenetic immunization against hepatitis B using whole bacteriophage lambda particles Vaccine 22 1666–71 Occurrence Handle10.1016/j.vaccine.2003.10.047 Occurrence Handle15068849

    Article  PubMed  Google Scholar 

  106. D Montag I Riede ML Eschbach M Degen U Henning (1987) ArticleTitleReceptor-recognizing proteins of T-even type bacteriophages. Constant and hypervariable regions and an unusual case of evolution J Mol Biol 196 165–74 Occurrence Handle10.1016/0022-2836(87)90519-5 Occurrence Handle2958637

    Article  PubMed  Google Scholar 

  107. K Drexler I Riede D Montag ML Eschbach U Henning (1989) ArticleTitleReceptor specificity of the Escherichia coli T-even type phage Ox2. Mutational alterations in host range mutants J Mol Biol 207 797–803 Occurrence Handle10.1016/0022-2836(89)90245-3 Occurrence Handle2547973

    Article  PubMed  Google Scholar 

  108. K Drexler J Dannull I Hindennach B Mutschler U Henning (1991) ArticleTitleSingle mutations in a gene for a tail fiber component of an Escherichia coli phage can cause an extension from a protein to a carbohydrate as a receptor J Mol Biol 219 655–63 Occurrence Handle10.1016/0022-2836(91)90662-P Occurrence Handle1829115

    Article  PubMed  Google Scholar 

  109. GK Schoolnik WC Summers JD Watson (2004) ArticleTitlePhage offer a real alternative Nat Biotechnol 22 505–6 Occurrence Handle10.1038/nbt0504-505 Occurrence Handle15122279

    Article  PubMed  Google Scholar 

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Correspondence to Shigenobu Matsuzaki.

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Matsuzaki, S., Rashel, M., Uchiyama, J. et al. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 11, 211–219 (2005). https://doi.org/10.1007/s10156-005-0408-9

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Key words

  • Phage therapy
  • Multidrug-resistant bacteria
  • Genetic modification
  • Lysin
  • Protein antibiotics