Synergy between the Host Immune System and Bacteriophage Is Essential for Successful Phage Therapy against an Acute Respiratory Pathogen

Cell Host and Microbe

Volumn 22, Issue 1, 2017, Pages 38-47.e4

  Roach, Dwayne R ^a   Leung, Chung Yin ^b   Henry, Marine ^a   Morello, Eric ^a   Singh, Devika ^b   Di Santo, James P ^a,c   Weitz, Joshua S ^b   Debarbieux, Laurent ^a  

^a INSTITUT PASTEUR   (France)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPHAGE; COMPUTER MODEL; CONTROLLED STUDY; FEMALE; HOST RESISTANCE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INNATE IMMUNITY; LOBAR PNEUMONIA; LYMPHOCYTE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGE THERAPY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MULTIDRUG RESISTANCE; MUTATION; PATHOGENICITY; PATHOLOGY; PROCEDURES; PSEUDOMONAS INFECTION; RESPIRATORY TRACT INFECTION; VIROLOGY;

CYTOKINE; MYD88 PROTEIN, MOUSE; MYELOID DIFFERENTIATION FACTOR 88;

ANIMALS; BACTERIOPHAGES; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; IMMUNE SYSTEM; LUNG; LYMPHOCYTES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUTATION; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHILS; PHAGE THERAPY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS;

EID: 85021795668     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.06.018     Document Type: Article

References (68)

1. Abedon, S.T., Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog. Dis. 6 (2009), 807–815.
2. Abedon, S.T., Kuhl, S.J., Blasdel, B.G., Kutter, E.M., Phage treatment of human infections. Bacteriophage 1 (2011), 66–85.
3. Adams, M.H., Bacteriophages. 1959, Interscience Publishers.
4. Albanesi, M., Mancardi, D.A., Jönsson, F., Iannascoli, B., Fiette, L., Di Santo, J.P., Lowell, C.A., Bruhns, P., Neutrophils mediate antibody-induced antitumor effects in mice. Blood 122 (2013), 3160–3164.
5. Andreu, N., Zelmer, A., Wiles, S., Noninvasive biophotonic imaging for studies of infectious disease. FEMS Microbiol. Rev. 35 (2011), 360–394.
6. Azeredo, J., Sutherland, I.W., The use of phages for the removal of infectious biofilms. Curr. Pharm. Biotechnol. 9 (2008), 261–266.
7. Bansal, S., Grenfell, B.T., Meyers, L.A., When individual behaviour matters: homogeneous and network models in epidemiology. J. R. Soc. Interface 4 (2007), 879–891.
8. Barletta, K.E., Cagnina, R.E., Wallace, K.L., Ramos, S.I., Mehrad, B., Linden, J., Leukocyte compartments in the mouse lung: distinguishing between marginated, interstitial, and alveolar cells in response to injury. J. Immunol. Methods 375 (2012), 100–110.
9. Bocian, K., Borysowski, J., Zarzycki, M., Pacek, M., Weber-Dąbrowska, B., Machcińska, M., Korczak-Kowalska, G., Górski, A., The effects of T4 and A3/R bacteriophages on differentiation of human myeloid dendritic cells. Front. Microbiol., 7, 2016, 1267.
10. Bohannan, B.J., Kerr, B., Jessup, C.M., Hughes, J.B., Sandvik, G., Trade-offs and coexistence in microbial microcosms. Antonie van Leeuwenhoek 81 (2002), 107–115.
11. Brogan, D.M., Mossialos, E., A critical analysis of the review on antimicrobial resistance report and the infectious disease financing facility. Global. Health, 12, 2016, 8.
12. Brown, C.M., Bidle, K.D., Attenuation of virus production at high multiplicities of infection in Aureococcus anophagefferens. Virology 466-467 (2014), 71–81.
13. Bruttin, A., Brüssow, H., Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob. Agents Chemother. 49 (2005), 2874–2878.
14. Bull, J.J., Levin, B.R., DeRouin, T., Walker, N., Bloch, C.A., Dynamics of success and failure in phage and antibiotic therapy in experimental infections. BMC Microbiol., 2, 2002, 35.
15. Campbell, A., Conditions for the existence of bacteriophage. Evolution 15 (1961), 153–165.
16. CDC (United States Centers for Disease Control and Prevention) (2013). Antibiotic resistance threats in the United States. https://www.cdc.gov/drugresistance/threat-report-2013.
17. 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., 6, 2016, 26717.
18. Colucci, F., Soudais, C., Rosmaraki, E., Vanes, L., Tybulewicz, V.L., Di Santo, J.P., Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl proto-oncogene in murine NK cell differentiation. J. Immunol. 162 (1999), 2761–2765.
19. Czaplewski, L., Bax, R., Clokie, M., Dawson, M., Fairhead, H., Fischetti, V.A., Foster, S., Gilmore, B.F., Hancock, R.E., Harper, D., et al. Alternatives to antibiotics-a pipeline portfolio review. Lancet Infect. Dis. 16 (2016), 239–251.
20. Debarbieux, L., Bacterial sensing of bacteriophages in communities: the search for the Rosetta stone. Curr. Opin. Microbiol. 20 (2014), 125–130.
21. Debarbieux, L., Leduc, D., Maura, D., Morello, E., Criscuolo, A., Grossi, O., Balloy, V., Touqui, L., Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. J. Infect. Dis. 201 (2010), 1096–1104.
22. Dennehy, J.J., What can phages tell us about host-pathogen coevolution?. Int. J. Evol. Biol., 2012, 2012, 396165.
23. Drusano, G.L., Vanscoy, B., Liu, W., Fikes, S., Brown, D., Louie, A., Saturability of granulocyte kill of Pseudomonas aeruginosa in a murine model of pneumonia. Antimicrob. Agents Chemother. 55 (2011), 2693–2695.
24. Eberl, G., Colonna, M., Di Santo, J.P., McKenzie, A.N., Innate lymphoid cells: a new paradigm in immunology. Science, 348, 2015, aaa6566.
25. El-Benna, J., Hurtado-Nedelec, M., Marzaioli, V., Marie, J.C., Gougerot-Pocidalo, M.A., Dang, P.M., Priming of the neutrophil respiratory burst: role in host defense and inflammation. Immunol. Rev. 273 (2016), 180–193.
26. Florens, M., Sapoval, B., Filoche, M., An anatomical and functional model of the human tracheobronchial tree. J. Appl. Physiol. 110 (2011), 756–763.
27. Henry, M., Lavigne, R., Debarbieux, L., Predicting in vivo efficacy of therapeutic bacteriophages used to treat pulmonary infections. Antimicrob. Agents Chemother. 57 (2013), 5961–5968.
28. Henry, M., Bobay, L.M., Chevallereau, A., Saussereau, E., Ceyssens, P.J., Debarbieux, L., The search for therapeutic bacteriophages uncovers one new subfamily and two new genera of Pseudomonas-infecting Myoviridae. PLoS One, 10, 2015, e0117163.
29. Heron, M., Grutters, J.C., ten Dam-Molenkamp, K.M., Hijdra, D., van Heugten-Roeling, A., Claessen, A.M., Ruven, H.J., van den Bosch, J.M., van Velzen-Blad, H., Bronchoalveolar lavage cell pattern from healthy human lung. Clin. Exp. Immunol. 167 (2012), 523–531.
30. Kawai, T., Adachi, O., Ogawa, T., Takeda, K., Akira, S., Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11 (1999), 115–122.
31. Knoll, B.M., Mylonakis, E., Antibacterial bioagents based on principles of bacteriophage biology: an overview. Clin. Infect. Dis. 58 (2014), 528–534.
32. Kolaczkowska, E., Kubes, P., Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13 (2013), 159–175.
33. Leung, C.Y., Weitz, J.S., Synergistic elimination of bacteria by phage and the immune system. J. Theor. Biol., 2017, 10.1016/j.jtbi.2017.06.037 Published online June 28, 2017.
34. Levin, B.R., Bull, J.J., Phage therapy revisited: the population biology of a bacterial infection and its treatment with bacteriophage and antibiotics. The American Naturalist 147 (1996), 881–898.
35. Levin, B.R., Bull, J.J., Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2 (2004), 166–173.
36. Levin, B.R., Stewart, F.M., Chao, L., Resource-limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. The American Naturalist 111 (1977), 3–24.
37. Li, Y., Karlin, A., Loike, J.D., Silverstein, S.C., A critical concentration of neutrophils is required for effective bacterial killing in suspension. Proc. Natl. Acad. Sci. USA 99 (2002), 8289–8294.
38. Liu, W.M., Hethcote, H.W., Levin, S.A., Dynamical behavior of epidemiological models with nonlinear incidence rates. J. Math. Biol. 25 (1987), 359–380.
39. Luria, S.E., Delbrück, M., Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28 (1943), 491–511.
40. Łusiak-Szelachowska, M., Zaczek, M., Weber-Dąbrowska, B., Międzybrodzki, R., Kłak, M., Fortuna, W., Letkiewicz, S., Rogóż, P., Szufnarowski, K., Jończyk-Matysiak, E., et al. Phage neutralization by sera of patients receiving phage therapy. Viral Immunol. 27 (2014), 295–304.
41. Łusiak-Szelachowska, M., Żaczek, M., Weber-Dąbrowska, B., Międzybrodzki, R., Letkiewicz, S., Fortuna, W., Rogóż, P., Szufnarowski, K., Jończyk-Matysiak, E., Olchawa, E., et al. Antiphage activity of sera during phage therapy in relation to its outcome. Future Microbiol. 12 (2017), 109–117.
42. Majewska, J., Beta, W., Lecion, D., Hodyra-Stefaniak, K., Kłopot, A., Kaźmierczak, Z., Miernikiewicz, P., Piotrowicz, A., Ciekot, J., Owczarek, B., et al. Oral application of T4 phage induces weak antibody production in the gut and in the blood. Viruses 7 (2015), 4783–4799.
43. Mazurier, F., Fontanellas, A., Salesse, S., Taine, L., Landriau, S., Moreau-Gaudry, F., Reiffers, J., Peault, B., Di Santo, J.P., de Verneuil, H., A novel immunodeficient mouse model–RAG2 x common cytokine receptor gamma chain double mutants–requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J. Interferon Cytokine Res. 19 (1999), 533–541.
44. Merril, C.R., Biswas, B., Carlton, R., Jensen, N.C., Creed, G.J., Zullo, S., Adhya, S., Long-circulating bacteriophage as antibacterial agents. Proc. Natl. Acad. Sci. USA 93 (1996), 3188–3192.
45. Meyer, J.R., Dobias, D.T., Weitz, J.S., Barrick, J.E., Quick, R.T., Lenski, R.E., Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335 (2012), 428–432.
46. Mirzaei, M.K., Maurice, C.F., Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat. Rev. Microbiol. 15 (2017), 397–408.
47. Moir, D.T., Ming, Di, Opperman, T., Schweizer, H.P., Bowlin, T.L., A high-throughput, homogeneous, bioluminescent assay for Pseudomonas aeruginosa gyrase inhibitors and other DNA-damaging agents. J. Biomol. Screen. 12 (2007), 855–864.
48. Munder, A., Wölbeling, F., Klockgether, J., Wiehlmann, L., Tümmler, B., In vivo imaging of bioluminescent Pseudomonas aeruginosa in an acute murine airway infection model. Pathog. Dis. 72 (2014), 74–77.
49. Murray, J.L., Kwon, T., Marcotte, E.M., Whiteley, M., Intrinsic antimicrobial resistance determinants in the superbug Pseudomonas aeruginosa. MBio 6 (2015), e01603–e01615.
50. Newburger, P.E., Dale, D.C., Evaluation and management of patients with isolated neutropenia. Semin. Hematol. 50 (2013), 198–206.
51. Pabary, R., Singh, C., Morales, S., Bush, A., Alshafi, K., Bilton, D., Alton, E.W., Smithyman, A., Davies, J.C., Antipseudomonal bacteriophage reduces infective burden and inflammatory response in murine lung. Antimicrob. Agents Chemother. 60 (2015), 744–751.
52. Reutershan, J., Basit, A., Galkina, E.V., Ley, K., Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 289 (2005), L807–L815.
53. 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 18 (2009), 237–238 240–243.
54. Roach, D.R., Debarbieux, L., Phage therapy: awakening a sleeping giant. Emerging Topics in Life Sciences 1 (2017), 93–103.
55. Roy, M., Pascual, M., On representing network heterogeneities in the incidence rate of simple epidemic models. Ecological Complexity 3 (2006), 80–90.
56. Salmond, G.P., Fineran, P.C., A century of the phage: past, present and future. Nat. Rev. Microbiol. 13 (2015), 777–786.
57. Salsgiver, E.L., Fink, A.K., Knapp, E.A., LiPuma, J.J., Olivier, K.N., Marshall, B.C., Saiman, L., Changing epidemiology of the respiratory bacteriology of patients with cystic fibrosis. Chest 149 (2016), 390–400.
58. Sarker, S.A., Sultana, S., Reuteler, G., Moine, D., Descombes, P., Charton, F., Bourdin, G., McCallin, S., Ngom-Bru, C., Neville, T., et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from bangladesh. EBioMedicine 4 (2016), 124–137.
59. Sarker, S.A., Berger, B., Deng, Y., Kieser, S., Foata, F., Moine, D., Descombes, P., Sultana, S., Huq, S., Bardhan, P.K., et al. Oral application of Escherichia coli bacteriophage: safety tests in healthy and diarrheal children from Bangladesh. Environ. Microbiol. 19 (2017), 237–250.
60. Skerrett, S.J., Liggitt, H.D., Hajjar, A.M., Wilson, C.B., Cutting edge: myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J. Immunol. 172 (2004), 3377–3381.
61. 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. 128 (1982), 307–318.
62. Stanojevic, S., Waters, V., Mathew, J.L., Taylor, L., Ratjen, F., Effectiveness of inhaled tobramycin in eradicating Pseudomonas aeruginosa in children with cystic fibrosis. J. Cyst. Fibros. 13 (2014), 172–178.
63. Vandenheuvel, D., Lavigne, R., Brüssow, H., Bacteriophage therapy: advances in formulation strategies and human clinical trials. Annu. Rev. Virol. 2 (2015), 599–618.
64. Warner, N., Núñez, G., MyD88: a critical adaptor protein in innate immunity signal transduction. J. Immunol. 190 (2013), 3–4.
65. Weibel, E.R., Morphometry of the Human Lung. 1963, Academic Press.
66. Weitz, J.S., Quantitative Viral Ecology: Dynamics of Viruses and Their Microbial Hosts. 2015, Princeton University Press, Priceton, New Jersey.
67. Weitz, J.S., Dushoff, J., Alternative stable states in host–phage dynamics. Theor. Ecol. 1 (2008), 13–19.
68. Zhang, Z., Louboutin, J.P., Weiner, D.J., Goldberg, J.B., Wilson, J.M., Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect. Immun. 73 (2005), 7151–7160.