Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection

Science

Volumn 363, Issue 6434, 2019, Pages

  Sweere, Johanna M ^a,b   Van Belleghem, Jonas D ^a   Ishak, Heather ^a,c   Bach, Michelle S ^a   Popescu, Medeea ^a,b   Sunkari, Vivekananda ^a   Kaber, Gernot ^a   Manasherob, Robert ^a   Suh, Gina A ^a,g   Cao, Xiou ^a   de Vries, Christiaan R ^a   Lam, Dung N ^a   Marshall, Payton L ^a,b   Birukova, Maria ^a,b   Katznelson, Ethan ^a   Lazzareschi, Daniel V ^a   Balaji, Swathi ^d   Keswani, Sundeep G ^d   Hawn, Thomas R ^e   Secor, Patrick R ^f   Bollyky, Paul L ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Palo Alto Veterans Institute for Research   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MONTANA   (United States)

^g Mayo Clinic College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MONOCLONAL ANTIBODY; RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR; TICAM-1 PROTEIN, MOUSE; TLR3 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN; VIRUS ANTIBODY;

BACTERIAL DISEASE; BACTERIOPHAGE; DISEASE CONTROL; IMMUNITY; IMMUNIZATION; INFECTIOUS DISEASE; INHIBITION; PROTEIN; RNA; TUMOR; VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIOPHAGE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOCYTOSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; OPSONIZATION; PASSIVE IMMUNIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; VIRUS IMMUNITY; WOUND INFECTION; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MUTANT MOUSE STRAIN; PATHOGENICITY; PHYSIOLOGY; PSEUDOMONAS INFECTION; PSEUDOMONAS PHAGE; VIROLOGY;

BACTERIA (MICROORGANISMS); DNA VIRUSES; MAMMALIA; MURINAE; MUS; PSEUDOMONAS AERUGINOSA;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIBODIES, VIRAL; HUMANS; IMMUNE TOLERANCE; INTERFERONS; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PHAGOCYTOSIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PSEUDOMONAS PHAGES; TOLL-LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR-ALPHA; WOUND INFECTION;

EID: 85064138980     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aat9691     Document Type: Article

References (55)

1. E. A. Azzopardi et al., Gram negative wound infection in hospitalised adult burn patients—Systematic review and metanalysis-. PLOS ONE 9, e95042 (2014). doi: 10.1371/journal.pone.0095042; pmid: 24751699
2. K. Kirketerp-Møller et al., Distribution, organization, and ecology of bacteria in chronic wounds. J. Clin. Microbiol. 46, 2717–2722 (2008). doi: 10.1128/JCM.00501-08; pmid: 18508940
3. C. K. Sen et al., Human skin wounds: A major and snowballing threat to public health and the economy. Wound Repair Regen. 17, 763–771 (2009). doi: 10.1111/j.1524-475X.2009.00543.x; pmid: 19903300
4. S. Shrivastava, P. Shrivastava, J. Ramasamy, World Health Organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. J. Med. Soc. 32, 76–77 (2018). doi: 10.4103/ jms.jms_25_17
5. T.-B. Tsay et al., Blocking TNF-a enhances Pseudomonas aeruginosa-induced mortality in burn mice through induction of IL-1b. Cytokine 63, 58–66 (2013). doi: 10.1016/ j.cyto.2013.04.002; pmid: 23623770
6. D. Gosselin et al., Role of tumor necrosis factor alpha in innate resistance to mouse pulmonary infection with Pseudomonas aeruginosa. Infect. Immun. 63, 3272–3278 (1995). pmid: 7642255
7. R. T. Sadikot et al., Targeted immunomodulation of the NF-kB pathway in airway epithelium impacts host defense against Pseudomonas aeruginosa. J. Immunol. 176, 4923–4930 (2006). doi: 10.4049/jimmunol.176.8.4923; pmid: 16585588
8. S. L. Gellatly, R. E. W. Hancock, Pseudomonas aeruginosa: New insights into pathogenesis and host defenses. Pathog. Dis. 67, 159–173 (2013). doi: 10.1111/2049-632X.12033; pmid: 23620179
9. M. Alhede, T. Bjarnsholt, M. Givskov, M. Alhede, Pseudomonas aeruginosa Biofilms: Mechanisms of Immune Evasion (Elsevier, ed. 1, 2014), vol. 86.
10. J. S. Webb, M. Lau, S. Kjelleberg, Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186, 8066–8073 (2004). doi: 10.1128/JB.186.23.8066-8073.2004; pmid: 15547279
11. S. A. Rice et al., The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 3, 271–282 (2009). doi: 10.1038/ ismej.2008.109; pmid: 19005496
12. P. R. Secor et al., Filamentous Bacteriophage Promote Biofilm Assembly and Function. Cell Host Microbe 18, 549–559 (2015). doi: 10.1016/j.chom.2015.10.013; pmid: 26567508
13. P. R. Secor et al., Filamentous Bacteriophage Produced by Pseudomonas aeruginosa Alters the Inflammatory Response and Promotes Noninvasive Infection In Vivo. Infect. Immun. 85, e00648-16 (2016). doi: 10.1128/IAI.00648-16; pmid: 27795361
14. A. Mai-Prochnow et al., ‘Big things in small packages: The genetics of filamentous phage and effects on fitness of their host’. FEMS Microbiol. Rev. 39, 465–487 (2015). doi: 10.1093/ femsre/fuu007; pmid: 25670735
15. E. Martínez, J. Campos-Gómez, Pf Filamentous Phage Requires UvrD for Replication in Pseudomonas aeruginosa. MSphere 1, e00104 (2016). pmid: 27303696
16. P. Knezevic, M. Voet, R. Lavigne, Prevalence of Pf1-like (pro) phage genetic elements among Pseudomonas aeruginosa isolates. Virology 483, 64–71 (2015). doi: 10.1016/j. virol.2015.04.008; pmid: 25965796
17. G. Chaby et al., Refractory venous leg ulcers: A study of risk factors. Dermatol. Surg. 32, 512–519 (2006). pmid: 16681658
18. P. J. Franks et al., Factors associated with healing leg ulceration with high compression. Age Ageing 24, 407–410 (1995). doi: 10.1093/ageing/24.5.407; pmid: 8669344
19. C. J. Moffatt et al., Community clinics for leg ulcers and impact on healing. BMJ 305, 1389–1392 (1992). doi: 10.1136/ bmj.305.6866.1389; pmid: 1486301
20. J. S. Chen, M. T. Longaker, G. C. Gurtner, in Methods in Molecular Biology (Humana Press, Totowa, NJ, 2013), vol. 1037 of Methods in Molecular Biology, pp. 265–274.
21. J. Park, J. E. Babensee, Differential functional effects of biomaterials on dendritic cell maturation. Acta Biomater. 8, 3606–3617 (2012). doi: 10.1016/j.actbio.2012.06.006; pmid: 22705044
22. D. Yang, K. S. Jones, Effect of alginate on innate immune activation of macrophages. J. Biomed. Mater. Res. A 90, 411–418 (2009). doi: 10.1002/jbm.a.32096; pmid: 18523947
23. T. Cantaert, D. Baeten, P. P. Tak, L. G. M. van Baarsen, Type I IFN and TNFa cross-regulation in immune-mediated inflammatory disease: Basic concepts and clinical relevance. Arthritis Res. Ther. 12, 219 (2010). doi: 10.1186/ar3150; pmid: 21062511
24. I. Sauer et al., Interferons limit inflammatory responses by induction of tristetraprolin. Blood 107, 4790–4797 (2006). doi: 10.1182/blood-2005-07-3058; pmid: 16514065
25. T. Kawasaki, T. Kawai, Toll-like receptor signaling pathways. Front. Immunol. 5, 461 (2014). doi: 10.3389/ fimmu.2014.00461; pmid: 25309543
26. A.-J. Tong et al., A Stringent Systems Approach Uncovers Gene-Specific Mechanisms Regulating Inflammation. Cell 165, 165–179 (2016). doi: 10.1016/j.cell.2016.01.020; pmid: 26924576
27. L. Wang et al., Regulation of lipopolysaccharide-induced translation of tumor necrosis factor-alpha by the toll-like receptor 4 adaptor protein TRAM. J. Innate Immun. 3, 437–446 (2011). doi: 10.1159/000324833; pmid: 21494017
28. T. Abe et al., STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell 50, 5–15 (2013). doi: 10.1016/ j.molcel.2013.01.039; pmid: 23478444
29. D. Gao et al., Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc. Natl. Acad. Sci. U.S.A. 112, E5699–E5705 (2015). doi: 10.1073/ pnas.1516465112; pmid: 26371324
30. A. Baird, Gene transfer into mammalian cells using targeted filamentous bacteriophage. Cold Spring Harb. Protoc. 2011, 950–957 (2011). doi: 10.1101/pdb.prot5653; pmid: 21807851
31. S. N. Lester, K. Li, Toll-like receptors in antiviral innate immunity. J. Mol. Biol. 426, 1246–1264 (2014). doi: 10.1016/ j.jmb.2013.11.024; pmid: 24316048
32. Z. Kaźmierczak et al., Molecular imaging of T4 phage in mammalian tissues and cells. Bacteriophage 4, e28364–e28366 (2014). doi: 10.4161/bact.28364; pmid: 24653943
33. M. Gaubin et al., Processing of filamentous bacteriophage virions in antigen-presenting cells targets both HLA class I and class II peptide loading compartments. DNA Cell Biol. 22, 11–18 (2003). doi: 10.1089/104454903321112451; pmid: 12590733
34. Y. Tian et al., Probing the endocytic pathways of the filamentous bacteriophage in live cells using ratiometric pH fluorescent indicator. Adv. Healthc. Mater. 4, 413–419 (2015). doi: 10.1002/adhm.201400508; pmid: 25308797
35. H.-K. Lee, S. Dunzendorfer, K. Soldau, P. S. Tobias, Double-stranded RNA-mediated TLR3 activation is enhanced by CD14. Immunity 24, 153–163 (2006). doi: 10.1016/ j.immuni.2005.12.012; pmid: 16473828
36. S. Nguyen et al., Bacteriophage Transcytosis Provides a Mechanism To Cross Epithelial Cell Layers. mBio 8, e01874 (2017). doi: 10.1128/mBio.01874-17; pmid: 29162715
37. K. Hodyra-Stefaniak et al., Mammalian Host-Versus-Phage immune response determines phage fate in vivo. Sci. Rep. 5, 14802 (2015). pmid: 26440922
38. E. Bille et al., A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation. PLOS Pathog. 13, e1006495 (2017). doi: 10.1371/journal. ppat.1006495; pmid: 28704569
39. E. Jończyk-Matysiak et al., The Effect of Bacteriophage Preparations on Intracellular Killing of Bacteria by Phagocytes. J. Immunol. Res. 2015, 482863 (2015). doi: 10.1155/2015/ 482863; pmid: 26783541
40. J. D. Van Belleghem, F. Clement, M. Merabishvili, R. Lavigne, M. Vaneechoutte, Pro- and anti-inflammatory responses of peripheral blood mononuclear cells induced by Staphylococcus aureus and Pseudomonas aeruginosa phages. Sci. Rep. 7, 8004 (2017). pmid: 28808331
41. D. R. Roach et al., Synergy between the Host Immune System and Bacteriophage Is Essential for Successful Phage Therapy against an Acute Respiratory Pathogen. Cell Host Microbe 22, 38–47.e4 (2017). doi: 10.1016/j.chom.2017.06.018; pmid: 28704651
42. J. De Smet, H. Hendrix, B. G. Blasdel, K. Danis-Wlodarczyk, R. Lavigne, Pseudomonas predators: Understanding and exploiting phage-host interactions. Nat. Rev. Microbiol. 15, 517–530 (2017). doi: 10.1038/nrmicro.2017.61; pmid: 28649138
43. S. M. Burns-Guydish et al., Monitoring age-related susceptibility of young mice to oral Salmonella enterica serovar Typhimurium infection using an in vivo murine model. Pediatr. Res. 58, 153–158 (2005). doi: 10.1203/01.PDR.0000157725.44213.C4; pmid: 15774831
44. J. Sambrook, E. F. Fritsch, T. Maniatis, Molecular Cloning. A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, ed. 1, 1989).
45. P. Boulanger, Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol. Biol. 502, 227–238 (2009). doi: 10.1007/978-1-60327-565-1_13; pmid: 19082559
46. K. Zimmermann, H. Hagedorn, C. C. Heuck, M. Hinrichsen, H. Ludwig, The ionic properties of the filamentous bacteriophages Pf1 and fd. J. Biol. Chem. 261, 1653–1655 (1986). pmid: 3944103
47. H. Cho et al., Regulation of endothelial cell activation and angiogenesis by injectable peptide nanofibers. Acta Biomater. 8, 154–164 (2012). doi: 10.1016/j.actbio.2011.08.029; pmid: 21925628
48. S. G. Keswani et al., Intraplacental gene therapy with Ad-IGF-1 corrects naturally occurring rabbit model of intrauterine growth restriction. Hum. Gene Ther. 26, 172–182 (2015). doi: 10.1089/hum.2014.065; pmid: 25738403
49. H. F. Kuipers et al., Hyaluronan synthesis is necessary for autoreactive T-cell trafficking, activation, and Th1 polarization. Proc. Natl. Acad. Sci. U.S.A. 113, 1339–1344 (2016). doi: 10.1073/pnas.1525086113; pmid: 26787861
50. E. Amiel, R. R. Lovewell, G. A. O’Toole, D. A. Hogan, B. Berwin, Pseudomonas aeruginosa evasion of phagocytosis is mediated by loss of swimming motility and is independent of flagellum expression. Infect. Immun. 78, 2937–2945 (2010). doi: 10.1128/IAI.00144-10; pmid: 20457788
51. P. Chomczynski, N. Sacchi, The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nat. Protoc. 1, 581–585 (2006). doi: 10.1038/nprot.2006.83; pmid: 17406285
52. J. A. Gebe et al., Modified High-molecular-weight hyaluronan promotes allergen-specific immune tolerance. Am. J. Respir. Cell Mol. Biol. 56, 109–120 (2017). doi: 10.1165/rcmb.2016-0111OC; pmid: 27598620
53. T. Horng, G. M. Barton, R. Medzhitov, TIRAP: An adapter molecule in the Toll signaling pathway. Nat. Immunol. 2, 835–841 (2001). doi: 10.1038/ni0901-835; pmid: 11526399
54. Z. Jiang et al., CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6, 565–570 (2005). doi: 10.1038/ ni1207; pmid: 15895089
55. F. M. Tomley, in Basic DNA and RNA Protocols, A. J. Harwood, Ed. (Humana Press, Totowa, NJ, 1996), Basic DNA and RNA Protocols, pp. 359–362.