Bacteriophages: Protagonists of a post-antibiotic era

Antibiotics

Volumn 7, Issue 3, 2018, Pages

  Domingo Calap, Pilar ^a   Delgado Martínez, Jennifer ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Antibiotic resistance; Bacteriophages; Enzybiotics; Phage display; Phage therapy

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM DETECTION; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; EPIFLUORESCENCE MICROSCOPY; NONHUMAN; PHAGE DISPLAY; PHAGE THERAPY; PRIORITY JOURNAL; PSEUDOMONAS FLUORESCENS; REVIEW; STAPHYLOCOCCUS AUREUS; TRANSMISSION ELECTRON MICROSCOPY;

EID: 85051079683     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics7030066     Document Type: Review

References (83)

1. Domingo-Calap, P.; Georgel, P.; Bahram, S. Back to the future: Bacteriophages as promising therapeutic tools. HLA 2016, 87, 133–140.
2. El-Shibiny, A.; El-Sahhar, S. Bacteriophages: The possible solution to treat infections caused by pathogenic bacteria. Can. J. Microbiol. 2017, 63, 865–879.
3. Cisek, A.; Dąbrowska, I.; Gregorczyk, K.; Wyżewski, Z. Phage therapy in bacterial infections treatment: One hundred years after the discovery of bacteriophages. Curr. Microbiol. 2016, 74, 277–283.
4. Guzmán, M. El bacteriófago, cien años de hallazgos trascendentales. Biomédica 2015, 35, 159–161.
5. Trudil, D. Phage lytic enzymes: A history. Virol. Sin. 2015, 30, 26–32.
6. Sadava, D.; Heller, G.; Orians, G.; Purves, W.; Hillis, D. Life: The Science of Biology, 8th ed.; Médica Panamericana: México, Mexico, 2008; pp. 286–287. ISBN 9789500682695.
7. Gelman, D.; Eisenkraft, A.; Chanishvili, N.; Nachman, D.; Coppenhagem Glazer, S.; Hazan, R. The history and promising future of phage therapy in the military service. J. Trauma Acute Care Surg. 2018, 85, S18–S26.
8. Wittebole, X.; De Roock, S.; Opal, S. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 2013, 5, 226–235.
9. Kutateladze, M. Experience of the Eliava Institute in bacteriophage therapy. Virol. Sin. 2015, 30, 80–81.
10. Haddad Kashani, H.; Schmelcher, M.; Sabzalipoor, H.; Seyed Hosseini, E.; Moniri, R. Recombinant endolysins as potential therapeutics against antibiotic-resistant Staphylococcus aureus: Current status of research and novel delivery strategies. Clin. Microbiol. Rev. 2017, 31.
11. Golkar, Z.; Bagasra, O.; Pace, D. Bacteriophage therapy: A potential solution for the antibiotic resistance crisis. J. Infect. Dev. Ctries. 2014, 8, 129–136.
12. Martínez, J. General principles of antibiotic resistance in bacteria. Drug Discov. Today Technol. 2014, 11, 33–39.
13. Jansen, K.; Knirsch, C.; Anderson, A. The role of vaccines in preventing bacterial antimicrobial resistance. Nat. Med. 2018, 24, 10–19.
14. Bassegoda, A.; Ivanova, K.; Ramón, E.; Tzanov, T. Strategies to prevent the occurrence of resistance against antibiotics by using advanced materials. Appl. Microbiol. Biotechnol. 2018, 102, 2075–2089.
15. Ackermann, H. 5500 Phages examined in the electron microscope. Arch. Virol. 2006, 152, 227–243.
16. Weinbauer, M. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 2004, 28, 127–181.
17. Ofir, G.; Sorek, R. Contemporary phage biology: From classic models to new insights. Cell 2018, 172, 1260–1270.
18. Furfaro, L.; Chang, B.; Payne, M. Applications for bacteriophage therapy during pregnancy and the perinatal period. Front. Microbiol. 2018, 8.
19. Criscuolo, E.; Spadini, S.; Lamanna, J.; Ferro, M.; Burioni, R. Bacteriophages and their immunological applications against infectious threats. J. Immunol. Res. 2017, 2017.
20. Nilsson, A. Phage therapy—Constraints and possibilities. Ups. J. Med. Sci. 2014, 119, 192–198.
21. Viertel, T.; Ritter, K.; Horz, H. Viruses versus bacteria—Novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J. Antimicrob. Chemother. 2014, 69, 2326–2336.
22. Parikka, K.; Le Romancer, M.; Wauters, N.; Jacquet, S. Deciphering the virus-to-prokaryote ratio VPR: Insights into virus-host relationships in a variety of ecosystems. Biol. Rev. 2016, 92, 1081–1100.
23. Matsuzaki, S.; Uchiyama, J.; Takemura-Uchiyama, I.; Daibata, M. Perspective: The age of the phage. Nature 2014, 509.
24. Clokie, M.; Millard, A.; Letarov, A.; Heaphy, S. Phages in nature. Bacteriophage 2011, 1, 31–45.
25. De Vos, D.; Pirnay, J. Phage therapy: Could viruses help resolve the worldwide antibiotic crisis? In AMR Control 2015: Overcoming Global Antibiotic Resistance; Carlet, J., Upham, G., Eds.; Global Health Dynamics Limited: Ipswich, UK, 2015; pp. 110–114. ISBN 9780957607231.
26. Ashelford, K.; Day, M.; Fry, J. Elevated abundance of bacteriophage infecting bacteria in soil. Appl. Environ. Microbiol. 2003, 69, 285–289.
27. Sharma, S.; Chatterjee, S.; Datta, S.; Prasad, R.; Dubey, D.; Prasad, R.K.; Vairale, M.G. Bacteriophages and its applications: An overview. Folia Microbiol. 2016, 62, 17–55.
28. Buckling, A.; Rainey, P. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. B Biol. Sci. 2002, 269, 931–936.
29. Paterson, S.; Vogwill, T.; Buckling, A.; Benmayor, R.; Spiers, A.J.; Thomson, N.R.; Quail, M.; Smith, F.; Walker, D.; Libberton, B. et al. Antagonistic coevolution accelerates molecular evolution. Nature 2010, 464, 275–278.
30. Stern, A.; Sorek, R. The phage-host arms race: Shaping the evolution of microbes. BioEssays 2010, 33, 43–51.
31. Díaz-Muñoz, S.; Koskella, B. Bacteria–phage interactions in natural environments. Adv. Appl. Microbiol. 2014, 89, 135–183.
32. Srinivasiah, S.; Bhavsar, J.; Thapar, K.; Liles, M.; Schoenfeld, T.; Wommack, K.E. Phages across the biosphere: Contrasts of viruses in soil and aquatic environments. Res. Microbiol. 2008, 159, 349–357.
33. Forde, A.; Hill, C. Phages of life-the path to pharma. Br. J. Pharmacol. 2018, 175, 412–418.
34. Manrique, P.; Dills, M.; Young, M. The human gut phage community and its implications for health and disease. Viruses 2017, 9, 141.
35. Van Geelen, L.; Meier, D.; Rehberg, N.; Kalscheuer, R. Some current concepts in antibacterial drug discovery. Appl. Microbiol. Biotechnol. 2018, 102, 2949–2963.
36. Hua, Y.; Luo, T.; Yang, Y.; Dong, D.; Wang, R.; Wang, Y.; Xu, M.; Guo, X.; Hu, F.; He, P. Phage therapy as a promising new treatment for lung infection caused by carbapenem-resistant Acinetobacter baumannii in mice. Front. Microbiol. 2017, 8, 2659.
37. Jeon, J.; Ryu, C.M.; Lee, J.Y.; Park, J.H.; Yong, D.; Lee, K. In vivo application of bacteriophage as a potential therapeutic agent to control OXA-66-like carbapenemase-producing Acinetobacter baumannii strains belonging to sequence type 357. Appl. Environ. Microbiol. 2016, 82, 4200–4208.
38. Peng, F.; Mi, Z.; Huang, Y.; Yuan, X.; Niu, W.; Wang, Y.; Hua, Y.; Fan, H.; Bai, C.; Tong, Y. Characterization, sequencing and comparative genomic analysis of vB_AbaM-IME-AB2, a novel lytic bacteriophage that infects multidrug-resistant Acinetobacter baumannii clinical isolates. BMC Microbiol. 2014, 14, 181.
39. Lood, R.; Ertürk, G.; Mattiasson, B. Revisiting antibiotic resistance spreading in wastewater treatment plants–bacteriophages as a much neglected potential transmission vehicle. Front. Microbiol. 2017, 8.
40. Phage Therapy Center. Available online: http://www.phagetherapycenter.com/pii/PatientServlet?command=static_phagetherapy&secnavpos=1&language=0 (accessed on 29 June 2018).
41. Drulis-Kawa, Z.; Majkowska-Skrobek, G.; Maciejewska, B.; Delattre, A.; Lavigne, R. Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Curr. Protein Pept. Sci. 2012, 13, 699–722.
42. Reardon, S. Phage therapy gets revitalized. Nature 2014, 510, 15–16.
43. Pires, D.; Melo, L.; Vilas Boas, D.; Sillankorva, S.; Azeredo, J. Phage therapy as an alternative or complementary strategy to prevent and control biofilm-related infections. Curr. Opin. Microbiol. 2017, 39, 48–56.
44. Knoll, B.; Mylonakis, E. Antibacterial bioagents based on principles of bacteriophage biology: An overview. Clin. Infect. Dis. 2013, 58, 528–534.
45. Torres-Barceló, C.; Hochberg, M. Evolutionary rationale for phages as complements of antibiotics. Trends Microbiol. 2016, 24, 249–256.
46. Kutateladze, M.; Adamia, R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010, 28, 591–595.
47. Ghannad, M.; Mohammadi, A. Bacteriophage: Time to re-evaluate the potential of phage therapy as a promising agent to control multidrug-resistant bacteria. Iran. J. Basic Med. Sci. 2012, 15, 693–701.
48. Levin, B.; Bull, J. Opinion: Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2004, 2, 166–173.
49. Tao, P.; Zhu, J.; Mahalingam, M.; Batra, H.; Rao, V.B. Bacteriophage T4 nanoparticles for vaccine delivery against infectious diseases. Adv. Drug Deliv. Rev. 2018, 6.
50. Roach, D.; Debarbieux, L. Phage therapy: Awakening a sleeping giant. Emerg. Top. Life Sci. 2017, 1, 93–103.
51. Sarker, S.; McCallin, S.; Barretto, C.; Berger, B.; Pittet, A.C.; Sultana, S.; Krause, L.; Huq, S.; Bibiloni, R.; Bruttin, A. et al. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 2012, 434, 222–232.
52. Cortés, P.; Cano-Sarabia, M.; Colom, J.; Otero, J.; Maspoch, D.; Llagostera, M. Nano/Micro formulations for bacteriophage delivery. Methods Mol. Biol. 2018, 1693, 271–283.
53. Makarova, K.; Haft, D.H.; Barrangou, R.; Brouns, S.J.; Charpentier, E.; Horvath, P.; Moineau, S.; Mojica, F.J.; Wolf, Y.I.; Yakunin, A.F. et al. Evolution and classification of the CRISPR–Cas systems. Nat. Rev. Microbiol. 2011, 9, 467–477.
54. Yosef, I.; Manor, M.; Kiro, R.; Qimron, U. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc. Natl. Acad. Sci. USA 2015, 112, 7267–7272.
55. Seed, K. Battling phages: How bacteria defend against viral attack. PLoS Pathog. 2015, 11, e1004847.
56. Scanlan, P.; Buckling, A.; Hall, A. Experimental evolution and bacterial resistance: Coevolutionary costs and trade-offs as opportunities in phage therapy research. Bacteriophage 2015, 5.
57. Valério, N.; Oliveira, C.; Jesus, V.; Branco, T.; Pereira, C.; Moreirinha, C.; Almeida, A. Effects of single and combined use of bacteriophages and antibiotics to inactivate Escherichia coli. Virus Res. 2017, 240, 8–17.
58. Comeau, A.; Tétart, F.; Trojet, S.; Prère, M.; Krisch, H. La «synergie phages-antibiotiques». Med. Sci. 2008, 24, 449–451.
59. Ryan, E.; Alkawareek, M.; Donnelly, R.; Gilmore, B. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol. Med. Microbiol. 2012, 65, 395–398.
60. Torres-Barceló, C.; Arias-Sánchez, F.I.; Vasse, M.; Ramsayer, J.; Kaltz, O.; Hochberg, M.E. A window of opportunity to control the bacterial pathogen Pseudomonas aeruginosa combining antibiotics and phages. PLoS ONE 2014, 9, e106628.
61. Maciejewska, B.; Olszak, T.; Drulis-Kawa, Z. Applications of bacteriophages versus phage enzymes to combat and cure bacterial infections: An ambitious and also a realistic application? Appl. Microbiol. Biotechnol. 2018, 102, 2563–2581.
62. Maxted, W. The active agent in nascent phage lysis of streptococci. J. Gen. Microbiol. 1957, 16, 584–595.
63. Krause, R. Studies on the bacteriophages of hemolytic streptococci: II. Antigens released from the streptococcal cell wall by a phage-associated lysin. J. Exp. Med. 1958, 108, 803–821.
64. Fischetti, V. Purification and physical properties of group C streptococcal phage-associated lysin. J. Exp. Med. 1971, 133, 1105–1117.
65. São-José, C. Engineering of phage-derived lytic enzymes: Improving their potential as antimicrobials. Antibiotics 2018, 7.
66. Diez-Martínez, R.; De Paz, H.D.; García-Fernández, E.; Bustamante, N.; Euler, C.W.; Fischetti, V.A.; Menendez, M.; García, P. A novel chimeric phage lysin with high in vitro and in vivo bactericidal activity against Streptococcus pneumoniae. J. Antimicrob. Chemother. 2015, 70, 1763–1773.
67. Drulis-Kawa, Z.; Majkowska-Skrobek, G.; Maciejewska, B. Bacteriophages and phage-derived proteins—Application approaches. Curr. Med. Chem. 2015, 22, 1757–1773.
68. Wang, I.N.; Smith, D.L.; Young, R. Holins: The protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 2000, 54, 799–825.
69. Lin, H.; Paff, M.; Molineux, I.; Bull, J. Therapeutic application of phage capsule depolymerases against K1.; K5.; and K30 capsulated E. coli in mice. Front. Microbiol. 2017, 8, 2257.
70. Pires, D.; Oliveira, H.; Melo, L.; Sillankorva, S.; Azeredo, J. Bacteriophage-encoded depolymerases: Their diversity and biotechnological applications. Appl. Microbiol. Biotechnol. 2016, 100, 2141–2151.
71. Rodríguez-Rubio, L.; Martínez, B.; Donovan, D.; Rodríguez, A.; García, P. Bacteriophage virion-associated peptidoglycan hydrolases: Potential new enzybiotics. Crit. Rev. Microbiol. 2012, 39, 427–434.
72. Attai, H.; Rimbey, J.; Smith, G.; Brown, P. Expression of a peptidoglycan hydrolase from lytic bacteriophages Atu_ph02 and Atu_ph03 triggers lysis of Agrobacterium tumefaciens. Appl. Environ. Microbiol. 2017, 83.
73. Olsen, I. Modification of phage for increased antibacterial effect towards dental biofilm. J. Oral Microbiol. 2016, 8.
74. Hauser, A.; Mecsas, J.; Moir, D. Beyond antibiotics: New therapeutic approaches for bacterial infections. Clin. Infect. Dis. 2016, 63, 89–95.
75. Smith, G.P. Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science 1985, 228, 1315–1317.
76. Pande, J.; Szewczyk, M.; Grover, A. Phage display: Concept, innovations, applications and future. Biotechnol. Adv. 2010, 28, 849–858.
77. Christensen, D.; Gottlin, E.; Benson, R.; Hamilton, P. Phage display for target-based antibacterial drug discovery. Drug Discov. Today 2001, 6, 721–727.
78. Ebrahimizadeh, W.; Rajabibazl, M. Bacteriophage vehicles for phage display: Biology, mechanism and application. Curr. Microbiol. 2014, 69, 109–120.
79. Muteeb, G.; Rehman, M.T.; Ali, S.Z.; Al-Shahrani, AM.; Kamal, M.A.; Ashraf, G.M. Phage display technique: A novel medicinal approach to overcome antibiotic resistance by using peptide-based inhibitors against β-lactamases. Curr. Drug Metab. 2017, 18, 90–95.
80. Flachbartova, Z.; Pulzova, L.; Bencurova, E.; Potocnakova, L.; Comor, L.; Bednarikova, Z.; Bhide, M. Inhibition of multidrug resistant Listeria monocytogenes by peptides isolated from combinatorial phage display libraries. Microbiol. Res. 2016.
81. Kovacs, J.; Masur, H. Prophylaxis against opportunistic infections in patients with human immunodeficiency virus infection. N. Engl. J. Med. 2000, 342, 1416–1429.
82. Bazan, J.; Całkosiński, I.; Gamian, A. Phage display—A powerful technique for immunotherapy. Hum. Vaccin. Immunother. 2012, 8, 1829–1835.
83. Omidfar, K.; Daneshpour, M. Advances in phage display technology for drug discovery. Expert Opin. Drug Discov. 2015, 10, 651–669.