The prospect for bacteriophage therapy in Western medicine

Nature Reviews Drug Discovery

Volumn 2, Issue 6, 2003, Pages 489-497

  Merril, Carl R ^a   Scholl, Dean ^a   Adhya, Sankar L ^b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; BACTERIOPHAGE DNA; CHOLERA TOXIN; CYTOTOXIN; DIPHTHERIA TOXIN; ENVELOPE PROTEIN; GLUCOSYLTRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; HEMOLYSIN; NEUROTOXIN; O ANTIGEN; PENICILLIN G; SHIGA TOXIN; SIALIDASE; STAPHYLOCOCCUS ENTEROTOXIN A; SUPEROXIDE DISMUTASE; TOXIC SHOCK SYNDROME TOXIN 1; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTEREMIA; BACTERIAL INFECTION; BACTERIOPHAGE; CHOLERA; CLOSTRIDIUM BOTULINUM; CORYNEBACTERIUM DIPHTHERIAE; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG ELIMINATION; DRUG PURIFICATION; DRUG SCREENING; DRUG SYNTHESIS; ESCHERICHIA COLI; GENE INSERTION; GLYCOSYLATION; HUMAN; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA; SHIGELLA FLEXNERI; SHIGELLOSIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES; VIBRIO CHOLERAE; ANIMAL; CHEMISTRY; GENETICS; METHODOLOGY; PHARMACEUTICS; REVIEW;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; BACTERIAL INFECTIONS; BACTERIOPHAGES; HUMANS; TECHNOLOGY, PHARMACEUTICAL;

EID: 0038808883     PISSN: 14741776     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrd1111     Document Type: Article

References (83)

1. Thornsberry, C. et al. Regional trends in antimicrobial resistance among clinical isolates of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis in the United States: results from the TRUST Surveillance Program, 1999-2000. Clin. Infect. Dis. 34, S4-S16 (2002).
2. National Center for Infectious Diseases. Campaign to prevent antimicrobial resistance in healthcare settings. Centers for Disease Control and Prevention [online] (cited 30 Sep 2002) http://www.cdc. gov/drugresistance/healthcare/problem.htm (2002).
3. Hashimoto, H. Drug resistance of methicillin-resistant Staphylococcus aureus (MRSA) in Japan until 1993. Jpn J. Antibiot. 47, 575-584 (1994).
4. Twort, F. W. An investigation on the nature of ultramicroscopic viruses. Lancet 2, 1241-1243 (1915).
5. d'Herelle, F. The Bacteriophage and its Behavior 490-541 (Williams & Wilkins, Baltimore, Maryland, 1926).
6. Summers, W. C. Felix d'Herelle and the origins of Molecular Biology 125-144 (Yale University Press, New Haven and London, 2001).
7. Summers, W. C. Bacteriophage therapy. Annu. Rev. Microbiol. 55, 437-451 (2001).
8. Alinsky, J., Iczkowski, K., Rapoport, A., & Troitsky, N. Bacteriophages show promise as antimicrobial agents. J. Infect. 16, 5-15 (1998).
9. Sulakvelidze, A., Alavidze, Z. & Morris, J. G. Jr Bacteriophage therapy. Antimicrob. Agents Chemother. 45, 649-659 (2001).
10. Straub, M. E. & Applebaum, M. Studies on commercial bacteriophage products. JAMA 100, 110-113 (1933).
11. Larkum, N. W. Bacteriophage in clinical medicine. J. Lab. Clin. Med. 17, 675-680 (1932).
12. Van Helvoort, T. Bacteriological and physiological research styles in the early controversy on the nature of the bacteriophage phenomenon. Med. Hist. 36, 234-270 (1992).
13. Randall-Hazelbauer, L. & Schwartz, M. Isolation of the bacteriophage λ receptor from Escherichia coli. J. Bacteriol. 116, 1436-1446 (1973).
14. Eaton, M. D. & Bayne-Jones, S. Bacteriophage therapy. JAMA 103, 1769-1776, 1847-1853 & 1934-1939 (1934).
15. Ho, K. Bacteriophage therapy for bacterial infections. Perspect. Biol. Med. 44, 1-16 (2001).
16. Barrow, P. A. & Soothill, J. S. Bacteriophage therapy and prophylaxis: rediscovery and renewed assessment of potential. Trends Microbiol. 5, 268-271 (1997)
17. Evans, A. C. Inactivation of antistreptococcus bacteriophage by animal fluids. Public Health Rep. 48, 411-426 (1933).
18. Dubos, R. J., Straus, J. H. & Pierce, C. The multiplication of bacteriophage in vivo and its protective effects against experimental infection with Shigella dysenteria. J. Exp. Med. 20, 161-168 (1943).
19. Asheshov, I. N., Wilson, J. & Topley, W. W. C. The effect of an anti-vi bacteriophage on typhoid infection in mice. Lancet 319-320 (1937).
20. Stent, G. S. Molecular Biology of Bacterial Viruses (W. H. Freeman, San Francisco, 1963).
21. Biswas, B. et al. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect. Immun. 70, 204-210 (2002).
22. Matsuzaki, S. et al. Experimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage MR11. J. Infect. Dis. 187, 613-624 (2003).
23. Soothill, J. S. Treatment of experimental infections of mice with bacteriophages. J. Med. Microbiol. 37, 258-262 (1992).
24. Cerveny, K. E, Depaola, A., Duckworth, D. H & Gulig, P. A. Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice. Infect. Immun. 70, 6251-6262 (2002).
25. Broxmeyer, L. et al. Killing of Mycobacterium avium and Mycobacterium tuberculosis by a mycobacteriophage delivered by a nonvirulent mycobacterium: a model for phage therapy of intracellular bacterial pathogens. J. Infect. Dis. 186, 1155-1160 (2002).
26. Smith, H. W. & Huggins, M. B. Successful treatment of experimental E. coli infections in mice using phage: its general superiority over antibiotics. J. Gen. Microbiol. 128, 307-318 (1982).
27. Smith, H. W., Huggins, M. B. & Shaw, K. M. The control of experimental E. coli diarrhea in calves by means of bacteriophages. J. Gen. Microbiol. 133, 1111-1126 (1987).
28. Smith, H. W., Huggins, M. B. & Shaw, K. M. Factors influencing the survival and multiplication of bacteriophages in calves and their environments. J. Gen. Microbiol. 133, 1127-1135 (1987).
29. Ramesh, V., Fralick, J. A. & Rolfe, R. D. Prevention of Clostridium difficile-induced ileocecitis with bacteriophage. Anaerobe 5, 69-78 (1999).
30. Soothill, J. S. Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns 20, 209-211 (1994).
31. Nakai, T. & Park, S. C. Bacteriophage therapy for infectious diseases in aquiculture. Res. Microbiol. 153, 13-18 (2002).
32. Flaherty, J. E., Harbaugh, B. K., Jones, J. B., Somodi, G. C. & Jackson, L. E. H-mutant bacteriophages as a potential biocontrol of bacterial blight of geraniums. Hortscience 36, 90-100 (2001).
33. Flaherty, J. E., Jones J. B., Harbaugh, B. K., Somodi, G. C. & Jackson, L. E. Control of bacterial spot on tomato in the greenhouse and field with H-mutant bacteriophages. Hortscience 35, 882-884 (2000).
34. Geier, M. R., Trigg, M. E. & Merril, C. R. The fate of bacteriophage λ in non-immune germ-free mice. Nature 246, 221-223 (1973).
35. Appelmans, R. Le bacteriophage dans l'organisme. Comp. Rend. Soc. de Biol. (Paris) 85, 722-724 (1921).
36. Nungester, W. J. & Watrous, R. M. Accumulation of bacteriophage in spleen and liver following its intravenous inoculation. Proc. Soc. Exper. Biol. Med. 31, 901-905 (1934).
37. Inchley, C. J. The activity of mouse kupffer cells following intravenous injection of T4 bacteriophage. Clin. Exp. Immunol. 5, 173-187 (1969).
38. Merril, C. R. et al. Long-circulating bacteriophage as antibacterial agents. Proc. Natl Acad. Sci. USA 93, 3188-3192 (1996).
39. Doerfler, W. et al. On the insertion of foreign DNA into mammalian genomes: mechanism and consequences. Gene 157, 241-245 (1995).
40. Schubbert, R., Hohlweg, U., Renz, D. & Doerfler, W. On the fate of orally ingested foreign DNA in mice: chromosomal association and placental transmission to the fetus. Mol. Gen. Genet. 259, 569-576 (1998).
41. Schubbert, R., Renz, D., Schmitz, B. & Doerfler, W. Foreign (M13) DNA ingested by mice reaches peripheral leukocytes, spleen, and liver via the intestinal wall mucosa and can be covalently linked to mouse DNA. Proc. Natl Acad. Sci. USA 94, 961-966 (1997).
42. Merril, C. R., Geier, M. R. & Petricciani, J. C. Bacterial virus gene expression in human cells. Nature 233, 398-400 (1971).
43. Horst, J., Kluge, F., Beyreuther, K. & Gerok, W. Gene transfer to human cells: transducing phage λ plac gene expression in GM1-gangliosidosis fibroblasts. Proc. Natl Acad. Sci. USA 72, 3531-3535 (1975).
44. Larocca, D. et al. Evolving phage vectors for cell targeted gene delivery. Curr. Pharm. Biotechnol. 3, 45-57 (2002).
45. Kucharewica-Krukowska A. & Slopek S. Immunogenic effect of bacteriophage in patients subjected to phage therapy. Arch Immunol. Ther. Exp. (Warsz.) 35, 553-561 (1987).
46. Levin, B. R. & Bull, J. J. Phage therapy revisited: the population biology of a bacterial infection and its treatment with bacteriophage and antibiotics. Am. Nat. 147, 881-898 (1996).
47. Payne, R. J. H. & Jansen, V. A. A. Pharmacokinetic principles of bacteriophage therapy. Clin. Pharmacokinet. 42, 315-325 (2003).
48. Francis, K. P. et al. Visualizing Pneumococcal infections in the lungs of live mice using bioluminescent Streptococcus pneumoniae transformed with a novel Gram-positive lux transposon. Infect. Immun. 69, 3350-3358 (2001).
49. Ochs, H. D., Davis, S. D. & Wedgwood, R. J. Immunologic responses to bacteriophage φX174 in immunodeficiency diseases. J. Clin. Invest. 50, 2559-2568 (1971).
50. Ochs, H. D., Nonoyama, S., Zhu, Q., Farrington, M. & Wedgwood, R. J. Regulation of antibody responses: the role of complement and adhesion molecules. Clin. Immunol. Immunopathol. 3, S33-S40 (1993).
51. Clark, L., Greenbaum, C., Jiang, J., Lernmark, Å. & Ochs, H. The antibody response to bacteriophage is linked to the lymphopenia gene in congenic BioBreeding rats. FEMS Immunol. Med. Microbiol. 32, 205-209 (2002).
52. Ching, Y-C., Davis, S. D. & Wedgwood, R. J. Antibody studies in hypogammaglobulinemia. J. Clin. Invest. 45, 1593-1600 (1966).
53. Jenne, S., Brepoels, K., Collen, D. & Jespers, L. High-resolution mapping of the B cell epitopes of staphylokinase in humans using negative selection of a phage-displayed antigen library. J. Immunol. 161, 3161-3168 (1998).
54. Bartlett, J. G. Antibiotic-associated diarrhea. N. Engl. J. Med. 346, 334-339 (2002).
55. Scholl, D., Rogers, S., Adhya, S. & Merril, C. Bacteriophage K1-5 encodes two different tail fiber proteins allowing it to infect and replicate on both K1 and K5 strains of E. coli. J. Virol. 75, 2509-2515 (2001).
56. Scholl, D., Adhya, S. & Merril, C. R. Bacteriophage SP6 is closely related to phages K1-5, K5 and K1E but encodes a tail protein very similar to that of the distantly related P22. J. Bacteriol. 184, 2833-2836 (2002).
57. Sandmeier, H. Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres. Mol. Microbiol. 12, 343-350 (1994).
58. Liu, M. et al. Reverse transcriptase-mediated tropism switching in bordetella bacteriophage. Science 295, 2091-2094 (2002).
59. Moffatt, B. A. & Studier, F. W. Entry of bacteriophage T7 DNA into the cell and escape from host restriction. J. Bacteriol. 170, 2095-2105 (1988).
60. Hollon, T. Impossible vaccine tames Staphylococcus aureus. The Scientist 16, 24-28 (2002).
61. Gabig, M. et al. The cell surface protein Ag43 facilitates phage infection of Escherichia coli in the presence of bile salts and carbohydrates. Microbiology 148, 1533-1542 (2002).
62. Danese, P. N., Pratt, L. A., Dove, S. L. & Kolter, R. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol. Microbiol. 37, 424-432 (2000).
63. Colvin, M. G. Behavior of bacteriophage in body fluids and in exudates. J. Infect. Dis. 51, 527-541 (1932).
64. Calalb, G. Action de la bile sur bacteriophage et importance de cette action. Compt. Rend. Soc. De biol. (Paris) 92, 1442-1443 (1925).
65. Wagner, P. L. & Waldor, M. K. Bacteriophage control of bacterial virulence. Infect. Immun. 70, 3985-3993 (2002).
66. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
67. Loessner, M. J., Rees, C. E. D., Steward, A. B. & Scherer, S. Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl. Environ. Microbiol. 62, 1133-1140 (1996).
68. Carriere, C. J. et al. Conditionally replicating luciferase reporter phages: improved sensitivity for rapid detection and assessment of drug susceptibility of Mycobacterium tuberculosis. J. Clin. Microbiol. 35, 3232-3239 (1997).
69. Schuch, R., Nelson, D. & Fischetti, V. A. A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418, 884-889 (2002).
70. Lay, J. O. Jr MALDI-TOF mass spectrometry of bacteria. Mass Spectrom. Rev. 20, 172-194 (2001).
71. Van Baar, B. L. M. Characterization of bacteria by matrix-assisted laser desorption/ionisation and electrospray mass spectrometry. FEMS Microbiol. Rev. 24, 193-219 (2000).
72. Hamels, S. et al. Consensus PCR and microarray for diagnosis of the genus Staphylococcus species and methicillin resistance. BioTechniques 31, 1364-1366, 1368, 1370-1372 (2001).
73. Uhr, J. W., Finkelstein, M. S. & Baumann, J. B. Antibody formation: III. the primary and secondary antibody response to bacteriophage φX 174 in guinea pigs. J. Exp. Med. 116, 655-670 (1962 ).
74. Lederberg, J. Smaller fleas...ad infinitum: therapeutic bacteriophage redux. Proc. Natl Acad. Sci. USA 93, 3167-3168 (1996).
75. Knight, J. Superbugs reveal chink in armour. Nature 417, 477 (2002).
76. Kilman, S. FDA restricts antibiotic use in livestock to protect people. The Wall Street Journal D3 (12 September, 2002).
77. Merril, C. R. et al. Isolation of bacteriophages from commercial sera. In Vitro 8, 91-93 (1972).
78. Merril, C. R. Phage in human vaccines. Science 188, 8 (1975).
79. Bernhardt, T. G., Wang, I-N., Struck, D. K. & Young, R. A protein antibiotic in the phage Qb virion: diversity in lysis targets. Science 292, 2326-2329 (2001).
80. Nelson, D., Loomis, L. & Fischetti, V. A. Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl Acad. Sci. USA 98, 4107-4112 (2001).
81. Gaeng, S., Scherer, S., Neve, H. & Loessner, M. J. Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl. Environ. Microbiol. 66, 2951-2958 (2000).
82. Naidu, B. P. B. & Avari, C. R. Bacteriophage in the treatment of plague. Ind. J. Med. Res. 19, 737-748 (1932).
83. Boyd, E. F., Davis, B. M. & Hochhut, B. Bacteriophage-bacteriophage interactions in the evolution of pathogenic bacteria. Trends Microbiol. 9, 137-144 (2001).