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Bacteriophage Pharmacology and Immunology

  • Krystyna Dąbrowska
  • Andrzej Górski
  • Stephen T. Abedon
Living reference work entry

Abstract

The discovery of bacterial viruses approximately 100 years ago fairly quickly led to their use as antibacterial agents. For roughly two decades – early 1920s to early 1940s – bacteriophages represented the only means readily available to medicine by which many bacterial infections might be treated and cured. This near monopoly, however, came to a close as antibiotics became generally available. Antibiotics, especially as more broadly specific, selectively toxic antibacterials were both more easily developed and more easily used medicinals than phages. Phage therapy did not disappear from medical practice altogether, however, and increasingly is viewed as a viable alternative to antibiotics under circumstances where bacterial resistance to antibiotics is an issue. In addition are circumstances where a more selectively toxic antibacterial is desired, antibacterials that, for example, have less of a negative impact on nontarget members of a body’s microbiome. As for any drug, the successful development of phage therapeutics requires a pharmacological approach, whether implicit or, ideally, explicitly implemented. In this chapter, we consider pharmacokinetic and pharmacodynamic principles, body impact on drugs and drug impact on body, respectively, and both as they may be applied to the development of phage-based antimicrobials. As an important facet of both the pharmacokinetics and pharmacodynamics of phage therapy, we take a close look particularly at phage interactions with the mammalian immune system.

Notes

Acknowledgments

KD’s work was supported by National Science Centre in Poland, grant UMO-2012/05/E/NZ6/03314.

AG’s work was supported by National Science Centre in Poland, grant DEC-2013/11/B/NZ1/02107.

References

  1. Abedon ST (2008) Phage, bacteria, and food. Appendix: rate of adsorption is function of phage density. In: Abedon ST (ed) Bacteriophage ecology. Cambridge University Press, Cambridge, UK, pp 321–324CrossRefGoogle Scholar
  2. Abedon ST (2009) Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog Dis 6:807–815PubMedCrossRefGoogle Scholar
  3. Abedon ST (2010) The ‘nuts and bolts’ of phage therapy. Curr Pharm Biotechnol 11:1PubMedCrossRefGoogle Scholar
  4. Abedon S (2011a) Phage therapy pharmacology: calculating phage dosing. Adv Appl Microbiol 77:1–40PubMedCrossRefGoogle Scholar
  5. Abedon ST (2011b) Bacteriophages and biofilms: ecology, phage therapy, plaques. Nova Science Publishers, HauppaugeGoogle Scholar
  6. Abedon ST (2011c) Envisaging bacteria as phage targets. Bacteriophage 1:228–230PubMedPubMedCentralCrossRefGoogle Scholar
  7. Abedon ST (2011d) Lysis from without. Bacteriophage 1:46–49PubMedPubMedCentralCrossRefGoogle Scholar
  8. Abedon ST (2012a) Bacterial ‘immunity’ against bacteriophages. Bacteriophage 2:50–54PubMedPubMedCentralCrossRefGoogle Scholar
  9. Abedon ST (2012b) Phage therapy best practices. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 256–272CrossRefGoogle Scholar
  10. Abedon ST (2012c) Spatial vulnerability: bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 4:663–687PubMedPubMedCentralCrossRefGoogle Scholar
  11. Abedon ST (2014a) Bacteriophages as drugs: the pharmacology of phage therapy. In: Borysowski J, Międzybrodzki R, Górski A (eds) Phage therapy: current research and applications. Caister Academic Press, Norfolk, pp 69–100Google Scholar
  12. Abedon ST (2014b) Phage therapy: eco-physiological pharmacology. Scientifica 2014:581639PubMedPubMedCentralCrossRefGoogle Scholar
  13. Abedon ST (2015a) Bacteriophage secondary infection. Virol Sin 30:3–10PubMedCrossRefGoogle Scholar
  14. Abedon ST (2015b) Ecology of anti-biofilm agents I. Antibiotics versus bacteriophages. Pharmaceuticals 8:525–558PubMedPubMedCentralCrossRefGoogle Scholar
  15. Abedon ST (2015c) Ecology of anti-biofilm agents II. Bacteriophage exploitation and biocontrol of biofilm bacteria. Pharmaceuticals 8:559–589PubMedPubMedCentralCrossRefGoogle Scholar
  16. Abedon ST (2015d) Phage therapy of pulmonary infections. Bacteriophage 5:e1020260PubMedPubMedCentralCrossRefGoogle Scholar
  17. Abedon ST (2016a) Bacteriophage exploitation of bacterial biofilms: phage preference for less mature targets? FEMS Microbiol Lett 363:fnv246PubMedCrossRefGoogle Scholar
  18. Abedon ST (2016b) Phage therapy dosing: the problem(s) with multiplicity of infection (MOI). Bacteriophage 6:e1220348PubMedPubMedCentralCrossRefGoogle Scholar
  19. Abedon ST (2017a) Active bacteriophage biocontrol and therapy on sub-millimeter scales towards removal of unwanted bacteria from foods and microbiomes. AIMS Microbiol 3:649–688CrossRefGoogle Scholar
  20. Abedon ST (2017b) Bacteriophage clinical use as antibactertial “drugs”: utility precident. Microbiol Spectr 5: BAD-0003-2016Google Scholar
  21. Abedon ST (2017c) Information phage therapy research should report. Pharmaceuticals (Basel) 10:43CrossRefGoogle Scholar
  22. Abedon ST (2017d) Phage “delay” towards enhancing bacterial escape from biofilms: a more comprehensive way of viewing resistance to bacteriophages. AIMS Microbiol 3:186–226CrossRefGoogle Scholar
  23. Abedon ST (2018a) Bacteriophage-mediated biocontrol of wound infections, and ecological exploitation of biofilms by phages. In: Shiffman M (ed) Recent clinical techniques, results, and research in wounds. SpringerGoogle Scholar
  24. Abedon ST (2018b) Phage therapy: various perspectives on how to improve the art. In: Medina C, López-Baena F (eds) Host-pathogen interactions. Humana Press, New York, pp 113–127CrossRefGoogle Scholar
  25. Abedon ST, Thomas-Abedon C (2010) Phage therapy pharmacology. Curr Pharm Biotechnol 11:28–47PubMedCrossRefGoogle Scholar
  26. Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM (2011) Phage treatment of human infections. Bacteriophage 1:66–85PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ackermann H-W (2005) Bacteriophage classification. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and application. CRC Press, Boca Raton, pp 67–90Google Scholar
  28. Aronow R, Danon D, Shahar A, Aronson M (1964) Electron microscopy of in vitro endocytosis of T2 phage by cells from rabbit peritoneal exudate. J Exp Med 120:943–954PubMedPubMedCentralCrossRefGoogle Scholar
  29. Barr JJ (2017) A bacteriophages journey through the human body. Immunol Rev 279:106–122CrossRefPubMedGoogle Scholar
  30. Boratyński J, Syper D, Weber-Dąbrowska B, Łusiak-Szelachowska M, Poźniak G, Górski A (2004) Preparation of endotoxin-free bacteriophages. Cell Mol Biol Lett 9:253–259PubMedPubMedCentralGoogle Scholar
  31. Borysowski J, Międzybrodzki R, Górski A (2014) Phage therapy: current research and applications. Caister Academic Press, NorfolkGoogle Scholar
  32. Brussow H (2013) Bacteriophage-host interaction: from splendid isolation into a messy reality. Curr Opin Microbiol 16:500–506PubMedCrossRefPubMedCentralGoogle Scholar
  33. Bruttin A, Brüssow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49:2874–2878PubMedPubMedCentralCrossRefGoogle Scholar
  34. Bryan D, El-Shibiny A, Hobbs Z, Porter J, Kutter EM (2016) Bacteriophage T4 infection of stationary phase E. coli: life after log from a phage perspective. Front Microbiol 7:1391PubMedPubMedCentralCrossRefGoogle Scholar
  35. Bull JJ, Gill JJ (2014) The habits of highly effective phages: population dynamics as a framework for identifying therapeutic phages. Front Microbiol 5:618PubMedPubMedCentralCrossRefGoogle Scholar
  36. Bull JJ, Regoes RR (2006) Pharmacodynamics of non-replicating viruses, bacteriocins and lysins. Proc R Soc Lond B Biol Sci 273:2703–2712CrossRefGoogle Scholar
  37. Campbell AM (2006) General aspects of lysogeny. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford, pp 66–73Google Scholar
  38. Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp 47:267–274Google Scholar
  39. Casjens SR, Hendrix RW (2015) Bacteriophage lambda: early pioneer and still relevant. Virology 479–480:310–330PubMedCrossRefPubMedCentralGoogle Scholar
  40. Chan BK, Abedon ST (2012a) Bacteriophage adaptation, with particular attention to issues of phage host range. In: Quiberoni A, Reinheimer J (eds) Bacteriophages in dairy processing. Nova Science Publishers, Hauppauge, pp 25–52Google Scholar
  41. Chan BK, Abedon ST (2012b) Phage therapy pharmacology: phage cocktails. Adv Appl Microbiol 78:1–23PubMedCrossRefPubMedCentralGoogle Scholar
  42. Chan BK, Abedon ST (2015) Bacteriophages and their enzymes in biofilm control. Curr Pharm Des 21:85–99PubMedCrossRefPubMedCentralGoogle Scholar
  43. Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8:769–783PubMedCrossRefPubMedCentralGoogle Scholar
  44. Chan BK, Turner PE, Kim S, Mojibian HR, Elefteriades JA, Narayan D (2018) Phage treatment of an aortic graft infected with Pseudomonas aeruginosa. Evol Med Public Health 1:60–66CrossRefGoogle Scholar
  45. Chanishvili N (2012a) A literature review of the practical application of bacteriophage research. Nova Science Publishers, HauppaugeGoogle Scholar
  46. Chanishvili N (2012b) Phage therapy – history from Twort and d’Herelle through Soviet experience to current approaches. Adv Virus Res 83:3–40PubMedCrossRefPubMedCentralGoogle Scholar
  47. Christie GE, Allison HA, Kuzio J, McShan M, Waldor MK, Kropinski AM (2012) Prophage-induced changes in cellular cytochemistry and virulence. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 33–60CrossRefGoogle Scholar
  48. Curtright AJ, Abedon ST (2011) Phage therapy: emergent property pharmacology. J Bioanal Biomed S3:010Google Scholar
  49. Dąbrowska K, Miernikiewicz P, Piotrowicz A, Hodyra K, Owczarek B, Lecion D, Kaźmierczak Z, Letarov A, Górski A (2014) Immunogenicity studies of proteins forming the T4 phage head surface. J Virol 88:12551–12557PubMedPubMedCentralCrossRefGoogle Scholar
  50. Dy RL, Richter C, Salmond GP, Fineran PC (2014) Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol 1:307–331PubMedCrossRefPubMedCentralGoogle Scholar
  51. Fan X, Li W, Zheng F, Xie J (2013) Bacteriophage inspired antibiotics discovery against infection involved biofilm. Crit Rev Eukaryot Gene Expr 23:317–326PubMedCrossRefPubMedCentralGoogle Scholar
  52. Fish R, Kutter E, Wheat G, Blasdel B, Kutateladze M, Kuhl S (2016) Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. J Wound Care 25(Suppl 7):S27–S33PubMedCrossRefPubMedCentralGoogle Scholar
  53. Fogelman I, Davey V, Ochs HD, Elashoff M, Feinberg MB, Mican J, Siegel JP, Sneller M, Lane HC (2000) Evaluation of CD4+ T cell function in vivo in HIV-infected patients as measured by bacteriophage phiX174 immunization. J Infect Dis 182:435–441PubMedCrossRefPubMedCentralGoogle Scholar
  54. Geier MR, Trigg ME, Merril CR (1973) The fate of bacteriophage lambda in non-immune germ-free mice. Nature (London) 246:221–223CrossRefGoogle Scholar
  55. Gill JJ, Hyman P (2010) Phage choice, isolation and preparation for phage therapy. Curr Pharm Biotechnol 11:2–14PubMedCrossRefPubMedCentralGoogle Scholar
  56. Goodridge LD (2010) Designing phage therapeutics. Curr Pharm Biotechnol 11:15–27PubMedCrossRefPubMedCentralGoogle Scholar
  57. Górski A, Weber-Dąbrowska B (2005) The potential role of endogenous bacteriophages in controlling invading pathogens. Cell Mol Life Sci 62:511–519PubMedCrossRefPubMedCentralGoogle Scholar
  58. Górski A, Kniotek M, Perkowska-Ptasinska A, Mroz A, Przerwa A, Gorczyca W, Dąbrowska K, Weber-Dąbrowska B, Nowaczyk M (2006a) Bacteriophages and transplantation tolerance. Transplant Proc 38:331–333PubMedCrossRefPubMedCentralGoogle Scholar
  59. Górski A, Wazna E, Dąbrowska B-W, Switala-Jelén K, Międzybrodzki R (2006b) Bacteriophage translocation. FEMS Immunol Med Microbiol 46:313–319PubMedCrossRefPubMedCentralGoogle Scholar
  60. Górski A, Międzybrodzki R, Borysowski J, Dąbrowska K, Wierzbicki P, Ohams M, Korczak-Kowalska G, Olszowska-Zaremba N, Łusiak-Szelachowska M, Kłak M, Jończyk E, Kaniuga E, Gołas A, Purchla S, Weber-Dąbrowska B, Letkiewicz S, Fortuna W, Szufnarowski K, Pawełczyk Z, Rogóz P, Kłosowska D (2012) Phage as a modulator of immune responses: practical implications for phage therapy. Adv Virus Res 83:41–71PubMedCrossRefPubMedCentralGoogle Scholar
  61. Górski A, Dąbrowska K, Hodyra-Stefaniak K, Borysowski J, Międzybrodzki R, Weber-Dąbrowska B (2015) Phages targeting infected tissues: novel approach to phage therapy. Future Microbiol 10:199–204PubMedCrossRefGoogle Scholar
  62. Gutíerrez D, Rodríguez-Rubio L, Martínez B, Rodríguez A, García P (2016) Bacteriophages as weapons against bacterial biofilms in the food industry. Front Microbiol 7:825PubMedPubMedCentralCrossRefGoogle Scholar
  63. Hagens S, Loessner MJ (2010) Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol 11:58–68PubMedCrossRefGoogle Scholar
  64. Hajek P (1967) Properties of natural 19S antibodies in normal pig serum against the FX174 and T2 phages. Folia Microbiol 12:551–556CrossRefGoogle Scholar
  65. Harper DR, Morales S (2012) Bacteriophage therapy: practicability and clinical need meet in the multidrug-resistance era. Future Microbiol 7:797–799PubMedCrossRefGoogle Scholar
  66. Harper DR, Parracho HMR, Walker J, Sharp R, Hughes G, Werthrén M, Lehman S, Morales S (2014) Bacteriophages and biofilms. Antibiotics 3:270–284PubMedCentralCrossRefPubMedGoogle Scholar
  67. Henry M, Lavigne R, Debarbieux L (2013) Predicting in vivo efficacy of therapeutic bacteriophages used to treat pulmonary infections. Antimicrob Agents Chemother 57:5961–5968PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hobbs Z, Abedon ST (2016) Diversity of phage infection types and associated terminology: the problem with ‘Lytic or lysogenic’. FEMS Microbiol Lett 363:fnw047PubMedCrossRefGoogle Scholar
  69. Hodyra-Stefaniak K, Miernikiewicz P, Drapala J, Drab M, Jończyk-Matysiak E, Lecion D, Kaźmierczak Z, Beta W, Majewska J, Harhala M, Bubak B, Kłopot A, Górski A, Dąbrowska K (2015) Mammalian host-versus-phage immune response determines phage fate in vivo. Sci Rep 5:14802PubMedPubMedCentralCrossRefGoogle Scholar
  70. Huff WE, Huff GR, Rath NC, Donoghue AM (2010) Immune interference of bacteriophage efficacy when treating colibacillosis in poultry. Poult Sci 89:895–900PubMedCrossRefGoogle Scholar
  71. Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248PubMedCrossRefGoogle Scholar
  72. Hyman P, Abedon ST (2012) Bacteriophages in health and disease. CABI Press, WallingfordCrossRefGoogle Scholar
  73. Inchley CJ (1969) The activity of mouse Kuppfer cells following intravenous injection of T4 bacteriophage. Clin Exp Immunol 5:173–187PubMedPubMedCentralGoogle Scholar
  74. Janeway CA, Travers P, Walport M, Shlomchik MJ (2005) Immunology. Garland Science, New YorkGoogle Scholar
  75. Jończyk-Matysiak E, Łusiak-Szelachowska M, Kłak M, Bubak B, Międzybrodzki R, Weber-Dąbrowska B, Żaczek M, Fortuna W, Rogóz P, Letkiewicz S, Szufnarowski K, Gorski A (2015) The effect of bacteriophage preparations on intracellular killing of bacteria by phagocytes. J Immunol Res 2015:482863PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kantoch M (1958) Studies on phagocytosis of bacterial viruses. Arch Immunol Ther Exp 6:63–84Google Scholar
  77. Kantoch M (1961) The role of phagocytes in virus infections. Arch Immunol Ther Exp 9:261–340Google Scholar
  78. Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7:131–137PubMedCrossRefGoogle Scholar
  79. Khalifa L, Shlezinger M, Beyth S, Houri-Haddad Y, Coppenhagen-Glazer S, Beyth N, Hazan R (2016) Phage therapy against Enterococcus faecalis in dental root canals. J Oral Microbiol 8:32157PubMedCrossRefGoogle Scholar
  80. Kucharewicz-Krukowska A, Slopek S (1987) Immunogenic effect of bacteriophage in patients subjected to phage therapy. Arch Immunol Ther Exp 35:553–561Google Scholar
  81. Kuhl S, Hyman P, Abedon ST (2012) Diseases caused by phages. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 21–32CrossRefGoogle Scholar
  82. Kumari S, Harjai K, Chhibber S (2010) Evidence to support the therapeutic potential of bacteriophage Kpn5 in burn wound infection caused by Klebsiella pneumoniae in BALB/c mice. J Microbiol Biotechnol 20:935–941PubMedCrossRefGoogle Scholar
  83. Kutateladze M, Adamia R (2008) Phage therapy experience at the Eliava institute. Med Mal Infect 38:426–430PubMedCrossRefGoogle Scholar
  84. Kutter E, Sulakvelidze A (2005) Bacteriophages: biology and application. CRC Press, Boca RatonGoogle Scholar
  85. Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86PubMedCrossRefGoogle Scholar
  86. Kutter E, Borysowski J, Międzybrodzki R, Górski A, Weber-Dąbrowska B, Kutateladze M, Alavidze Z, Goderdzishvili M, Adamia R (2014) Clinical phage therapy. In: Borysowski J, Międzybrodzki R, Górski A (eds) Phage therapy: current research and applications. Caister Academic Press, Norfolk, pp 257–288Google Scholar
  87. Kutter EM, Kuhl SJ, Abedon ST (2015) Re-establishing a place for phage therapy in western medicine. Future Microbiol 10:685–688PubMedCrossRefGoogle Scholar
  88. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327PubMedCrossRefGoogle Scholar
  89. Langbeheim H, Teitelbaum D, Arnon R (1978) Cellular immune response toward MS-2 phage and a synthetic fragment of its coat protein. Cell Immunol 38:193–197PubMedCrossRefGoogle Scholar
  90. Letarov AV, Golomidova AK, Tarasyan KK (2010) Ecological basis of rational phage therapy. Acta Nat 2:60–71Google Scholar
  91. Lindberg HM, McKean KA, Wang I-N (2014) Phage fitness may help predict phage therapy efficacy. Bacteriophage 4:e964081PubMedPubMedCentralCrossRefGoogle Scholar
  92. Łobocka M, Hejnowicz MS, Gagala U, Weber-Dąbrowska B, Wegrzyn G, Dadlez M (2014) The first step to bacteriophage therapy: how to choose the correct phage. In: Borysowski J, Międzybrodzki R, Górski A (eds) Phage therapy: current research and applications. Caister Academic Press, Norfolk, pp 23–67Google Scholar
  93. Łusiak-Szelachowska M, Żaczek M, Weber-Dąbrowska B, Międzybrodzki R, Kłak M, Fortuna W, Letkiewicz S, Rogóz P, Szufnarowski K, Jończyk-Matysiak E, Owczarek B, Górski A (2014) Phage neutralization by sera of patients receiving phage therapy. Viral Immunol 27:295–304PubMedPubMedCentralCrossRefGoogle Scholar
  94. Majewska J, Beta W, Lecion D, Hodyra-Stefaniak K, Klopot A, Kazmierczak Z, Miernikiewicz P, Piotrowicz A, Ciekot J, Owczarek B, Kopciuch A, Wojtyna K, Harhala M, Mąkosa M, Dąbrowska K (2015) Oral application of T4 phage induces weak antibody production in the gut and in the blood. Viruses 7:4783–4799PubMedPubMedCentralCrossRefGoogle Scholar
  95. McCallin S, Alam SS, Barretto C, Sultana S, Berger B, Huq S, Krause L, Bibiloni R, Schmitt B, Reuteler G, Brüssow H (2013) Safety analysis of a Russian phage cocktail: from metaGenomic analysis to oral application in healthy human subjects. Virology 443:187–196PubMedCrossRefGoogle Scholar
  96. Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature (London) 449:819–826CrossRefGoogle Scholar
  97. Merril CR (2008) Interaction of bacteriophages with animals. In: Abedon ST (ed) Bacteriophage ecology. Cambridge University Press, Cambridge, UK, pp 332–352CrossRefGoogle Scholar
  98. Merril CR, Biswas B, Carlton R, Jensen NC, Creed GJ, Zullo S, Adhya S (1996) Long-circulating bacteriophage as antibacterial agents. Proc Natl Acad Sci U S A 93:3188–3192PubMedPubMedCentralCrossRefGoogle Scholar
  99. Miedzybrodzki R, Switala-Jelen K, Fortuna W, Weber-Dabrowska B, Przerwa A, Lusiak-Szelachowska M, Dabrowska K, Kurzepa A, Boratynski J, Syper D, Pozniak G, Lugowski C, Górski A (2008) Bacteriophage preparation inhibition of reactive oxygen species generation by endotoxin-stimulated polymorphonuclear leukocytes. Virus Res 131:233–242PubMedCrossRefGoogle Scholar
  100. Międzybrodzki R, Fortuna W, Weber-Dąbrowska B, Górski A (2009) A retrospective analysis of changes in inflammatory markers in patients treated with bacterial viruses. Clin Exp Med 9:303–312PubMedCrossRefGoogle Scholar
  101. Międzybrodzki R, Borysowski J, Weber-Dąbrowska B, Fortuna W, Letkiewicz S, Szufnarowski K, Pawełczyk Z, Rogóz P, Kłak M, Wojtasik E, Górski A (2012) Clinical aspects of phage therapy. Adv Virus Res 83:73–121PubMedCrossRefGoogle Scholar
  102. Miernikiewicz P, Dąbrowska K, Piotrowicz A, Owczarek B, Wojas-Turek J, Kicielińska J, Rossowska J, Pajtasz-Piasecka E, Hodyra K, Macegoniuk K, Rzewucka K, Kopciuch A, Majka T, Letarov A, Kulikov E, Maciejewski H, Górski A (2013) T4 phage and its head surface proteins do not stimulate inflammatory mediator production. PLoS One 8:e71036PubMedPubMedCentralCrossRefGoogle Scholar
  103. Miernikiewicz P, Klopot A, Soluch R, Szkuta P, Kęska W, Hodyra-Stefaniak K, Konopka A, Nowak M, Lecion D, Kaźmierczak Z, Majewska J, Harhala M, Gorski A, Dąbrowska K (2016) T4 phage tail adhesin gp12 counteracts LPS-induced inflammation in vivo. Front Microbiol 7:1112PubMedPubMedCentralCrossRefGoogle Scholar
  104. Motlagh AM, Bhattacharjee AS, Goel R (2016) Biofilm control with natural and genetically-modified phages. World J Microbiol Biotechnol 32:67PubMedCrossRefGoogle Scholar
  105. Muckenfuss RS (1928) Studies on the bacteriophage of d’Hérelle. XI. An inquiry into the mode of action of antibacteriophage serum. J Exp Med 48:709–722PubMedPubMedCentralCrossRefGoogle Scholar
  106. Mushtaq N, Redpath MB, Luzio JP, Taylor PW (2004) Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob Agents Chemother 48:1503–1508PubMedPubMedCentralCrossRefGoogle Scholar
  107. Nguyen S, Baker K, Padman BS, Patwa R, Dunstan RA, Weston TA, Schlosser K, Bailey B, Lithgow T, Lazarou M, Luque A, Rohwer F, Blumberg RS, Barr JJ (2017) Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. MBio 8:e01874PubMedPubMedCentralGoogle Scholar
  108. Olszowska-Zaremba N, Borysowski J, Dąbrowska K, Górski A (2012) Phage translocation, safety, and immunomodulation. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 168–184CrossRefGoogle Scholar
  109. Pancer Z, Cooper MD (2006) The evolution of adaptive immunity. Annu Rev Immunol 24:497–518PubMedCrossRefGoogle Scholar
  110. Parasion S, Kwiatek M, Gryko R, Mizak L, Malm A (2014) Bacteriophages as an alternative strategy for fighting biofilm development. Pol J Microbiol 63:137–145PubMedGoogle Scholar
  111. Park K, Cha KE, Myung H (2014) Observation of inflammatory responses in mice orally fed with bacteriophage T7. J Appl Microbiol 117:627–633PubMedCrossRefGoogle Scholar
  112. Payne RJH, Jansen VAA (2001) Understanding bacteriophage therapy as a density-dependent kinetic process. J Theor Biol 208:37–48PubMedCrossRefGoogle Scholar
  113. Payne RJH, Phil D, Jansen VAA (2000) Phage therapy: the peculiar kinetics of self-replicating pharmaceuticals. Clin Pharmacol Ther 68:225–230PubMedCrossRefGoogle Scholar
  114. Payne RJH, Jansen VAA (2003) Pharmacokinetic principles of bacteriophage therapy. Clin Pharmacokinet 42:315–325PubMedCrossRefPubMedCentralGoogle Scholar
  115. Perreau M, Guerin MC, Drouet C, Kremer EJ (2007) Interactions between human plasma components and a xenogenic adenovirus vector: reduced immunogenicity during gene transfer. Mol Ther 15:1998–2007PubMedCrossRefGoogle Scholar
  116. Pincus NB, Reckhow JD, Saleem D, Jammeh ML, Datta SK, Myles IA (2015) Strain specific phage treatment for Staphylococcus aureus infection is influenced by host immunity and site of infection. PLoS One 10:e0124280PubMedPubMedCentralCrossRefGoogle Scholar
  117. Pirnay JP, De VD, Verbeken G, Merabishvili M, Chanishvili N, Vaneechoutte M, Zizi M, Laire G, Lavigne R, Huys I, Van den Mooter G, Buckling A, Debarbieux L, Pouillot F, Azeredo J, Kutter E, Dublanchet A, Górski A, Adamia R (2011) The phage therapy paradigm: prêt-à-porter or sur-mesure? Pharm Res 28:934–937PubMedCrossRefGoogle Scholar
  118. Pirnay JP, Blasdel BG, Bretaudeau L, Buckling A, Chanishvili N, Clark JR, Corte-Real S, Debarbieux L, Dublanchet A, De VD, Gabard J, Garcia M, Goderdzishvili M, Górski A, Hardcastle J, Huys I, Kutter E, Lavigne R, Merabishvili M, Olchawa E, Parikka KJ, Patey O, Pouilot F, Resch G, Rohde C, Scheres J, Skurnik M, Vaneechoutte M, Van PL, Verbeken G, Zizi M, Van den Eede G (2015) Quality and safety requirements for sustainable phage therapy products. Pharm Res 32:2173–2179PubMedPubMedCentralCrossRefGoogle Scholar
  119. Przybylski M, Borysowski J, Jakubowska-Zahorska R, Weber-Dąbrowska B, Górski A (2015) T4 bacteriophage-mediated inhibition of adsorption and replication of human adenovirus in vitro. Future Microbiol 10:453–460PubMedCrossRefGoogle Scholar
  120. Rus H, Cudrici C, Niculescu F (2005) The role of the complement system in innate immunity. Immunol Res 33:103–112PubMedCrossRefGoogle Scholar
  121. Ryan EM, Gorman SP, Donnelly RF, Gilmore BF (2011) Recent advances in bacteriophage therapy: how delivery routes, formulation, concentration and timing influence the success of phage therapy. J Pharm Pharmacol 63:1253–1264PubMedCrossRefGoogle Scholar
  122. Sabour PM, Griffiths MW (2010) Bacteriophages in the control of food and, waterborne pathogens. ASM Press, Washington, DCGoogle Scholar
  123. Schmerer M, Molineux IJ, Bull JJ (2014) Synergy as a rationale for phage therapy using phage cocktails. PeerJ 2:e590PubMedPubMedCentralCrossRefGoogle Scholar
  124. Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, Barr JJ, Reed SL, Rohwer F, Benler S, Segall AM, Taplitz R, Smith DM, Kerr K, Kumaraswamy M, Nizet V, Lin L, McCauley MD, Strathdee SA, Benson CA, Pope RK, Leroux BM, Picel AC, Mateczun AJ, Cilwa KE, Regeimbal JM, Estrella LA, Wolfe DM, Henry MS, Quinones J, Salka S, Bishop-Lilly KA, Young R, Hamilton T (2017) Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother 61:e00954-17PubMedPubMedCentralCrossRefGoogle Scholar
  125. Seed KD (2015) Battling phages: how bacteria defend against viral attack. PLoS Pathog 11:e1004847PubMedPubMedCentralCrossRefGoogle Scholar
  126. Sillankorva S, Azeredo J (2014) The use of bacteriophages and bacteriophage-derived enzymes for clinically relevant biofilm control. In: Borysowski J, Międzybrodzki R, Górski A (eds) Phage therapy: current research and applications. Caister Academic Press, NorfolkGoogle Scholar
  127. Smith HW, Huggins MB, Shaw KM (1987) Factors influencing the survival and multiplication of bacteriophages in calves and in their environment. J Gen Microbiol 133:1127–1135PubMedGoogle Scholar
  128. Sokoloff AV, Bock I, Zhang G, Sebestyen MG, Wolff JA (2000) The interactions of peptides with the innate immune system studied with use of T7 phage peptide display. Mol Ther 2:131–139PubMedCrossRefGoogle Scholar
  129. Speck P, Smithyman A (2016) Safety and efficacy of phage therapy via the intravenous route. FEMS Microbiol Lett 363:fnv242PubMedCrossRefGoogle Scholar
  130. Srivastava AS, Kaido T, Carrier E (2004) Immunological factors that affect the in vivo fate of T7 phage in the mouse. J Virol Methods 115:99–104PubMedCrossRefGoogle Scholar
  131. Stent GS (1963) Molecular Biology of Bacterial Viruses. WH Freeman and Co., San Francisco, CAGoogle Scholar
  132. Sulakvelidze A, Kutter E (2005) Bacteriophage therapy in humans. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and application. CRC Press, Boca Raton, pp 381–436Google Scholar
  133. Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45:649–659PubMedPubMedCentralCrossRefGoogle Scholar
  134. Summers WC (2005) History of phage research and phage therapy. In: Waldor M, Friedman D, Adhya S (eds) Phages: their role in bacterial pathogenesis and biotechnology. ASM Press, Washington, DCGoogle Scholar
  135. Summers WC (2012) The strange history of phage therapy. Bacteriophage 2:130–133PubMedPubMedCentralCrossRefGoogle Scholar
  136. Szermer-Olearnik B, Boratyński J (2015) Removal of endotoxins from bacteriophage preparations by extraction with organic solvents. PLoS One 10:e0122672PubMedPubMedCentralCrossRefGoogle Scholar
  137. Uchiyama J, Maeda Y, Takemura I, Chess-Williams R, Wakiguchi H, Matsuzaki S (2009) Blood kinetics of four intraperitoneally administered therapeutic candidate bacteriophages in healthy and neutropenic mice. Microbiol Immunol 53:301–304PubMedCrossRefGoogle Scholar
  138. Wei W, Krone SM (2005) Spatial invasion by a mutant pathogen. J Theor Biol 236:335–348PubMedPubMedCentralCrossRefGoogle Scholar
  139. Zimecki M, Artym J, Kocięba M, Weber-Dąbrowska B, Borysowski J, Górski A (2009) Effects of prophylactic administration of bacteriophages to immunosuppressed mice infected with Staphylococcus aureus. BMC Microbiol 9:169PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Krystyna Dąbrowska
    • 1
  • Andrzej Górski
    • 1
    • 3
    • 4
    • 5
  • Stephen T. Abedon
    • 2
  1. 1.Institute of Immunology and Experimental TherapyPolish Academy of SciencesWrocławPoland
  2. 2.Department of MicrobiologyThe Ohio State UniversityMansfieldUSA
  3. 3.Bacteriophage LaboratoryHirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of SciencesWrocławPoland
  4. 4.Phage Therapy UnitHirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of SciencesWrocławPoland
  5. 5.Department of Clinical Immunology, Transplantation InstituteMedical University of WarsawWrocławPoland

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