Advertisement

Virologica Sinica

, Volume 30, Issue 1, pp 11–18 | Cite as

Bacteriophage therapy against Enterobacteriaceae

  • Youqiang Xu
  • Yong Liu
  • Yang Liu
  • Jiangsen Pei
  • Su Yao
  • Chi Cheng
Review

Abstract

The Enterobacteriaceae are a class of gram-negative facultative anaerobic rods, which can cause a variety of diseases, such as bacteremia, septic arthritis, endocarditis, osteomyelitis, lower respiratory tract infections, skin and soft-tissue infections, urinary tract infections, intra-abdominal infections and ophthalmic infections, in humans, poultry, animals and fish. Disease caused by Enterobacteriaceae cause the deaths of millions of people every year, resulting in enormous economic loss. Drug treatment is a useful and efficient way to control Enterobacteriaceae infections. However, with the abuse of antibiotics, drug resistance has been found in growing number of Enterobacteriaceae infections and, as such, there is an urgent need to find new methods of control. Bacteriophage therapy is an efficient alternative to antibiotics as it employs a different antibacterial mechanism. This paper summarizes the history of bacteriophage therapy, its bacterial lytic mechanisms, and the studies that have focused on Enterobacteriaceae and bacteriophage therapy.

Keywords

bacteriophage therapy Enterobacteriaceae antibiotics bacteriolytic mechanism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abedon ST, Thomas-Abedon C. 2010. Phage therapy pharmacology. Curr Pharm Biotechnol, 11:28–47.CrossRefPubMedGoogle Scholar
  2. Albert MJ, Faruque SM, Faruque AS, Neogi PK, Ansaruzzaman M, Bhuiyan NA, Alam K, Akbar MS. 1995. Controlled study of Escherichia coli diarrheal infections in Bangladeshi children. J Clin Microbiol, 33:973–977.PubMedCentralPubMedGoogle Scholar
  3. Anderson ES, Ward L, DeSaxe M, de Sa JD. 1977. Bacteriophage-typing designations of Salmonella typhimurium. J Hyg (Lond), 78:297–300.CrossRefGoogle Scholar
  4. Angulo FJ, Johnson KR, Tauxe RV, Cohen ML. 2000. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States. Microb Drug Resist, 6:77–83.CrossRefPubMedGoogle Scholar
  5. Atterbury RJ, Van Bergen MA, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA. 2007. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol, 73:4543–4549.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Babalova EG, Katsitadze KT, Sakvarelidze LA, Imnaishvili NSh, Sharashidze TG, Badashvili VA, Kiknadze GP, Meĭpariani AN, Gendzekhadze ND, Machavariani EV, Gogoberidze KL, Gozalov EI, Dekanosidze NG. 1968. Preventive value of dried dysentery bacteriophage. Zh Mikrobiol Epidemiol Immunobiol, 45:143–145. (In Russian)PubMedGoogle Scholar
  7. Bentley R, Bennett JW. 2003. What is an antibiotic? Revisited. Adv Appl Microbiol, 52:303–331.CrossRefGoogle Scholar
  8. Bhan MK, Mahalanabis D, Fontaine O, Pierce NF. 1994. Clinical trials of improved oral rehydration salt formulations: a review. Bull World Health Organ, 72:945–955.PubMedCentralPubMedGoogle Scholar
  9. Born Y, Fieseler L, Marazzi J, Lurz R, Duffy B, Loessner MJ. 2011. Novel virulent and broad-host-range Erwinia amylovora bacteriophages reveal a high degree of mosaicism and a relationship to Enterobacteriaceae phages. Appl Environ Microbiol, 77:5945–5954.CrossRefPubMedCentralPubMedGoogle Scholar
  10. Bruynoghe R, Maisin J. 1921. Essais de the rapeutique au moyen du bacteriophage. C R Soc Biol, 85:1120–1121.Google Scholar
  11. Burrowes B, Harper DR, Anderson J, McConville M, Enright MC. 2011. Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev Anti Infect Ther, 9:775–785.CrossRefPubMedGoogle Scholar
  12. Capparelli R, Nocerino N, Iannaccone M, Ercolini D, Parlato M, Chiara M, Iannelli D. 2010. Bacteriophage therapy of Salmonella enterica: a fresh appraisal of bacteriophage therapy. J Infect Dis, 201:52–61.CrossRefPubMedGoogle Scholar
  13. Carlton RM. 1999. Phage therapy: past history and future prospects. Arch Immunol Ther Exp (Warsz), 47:267–274.Google Scholar
  14. Chaudhry WN, Haq IU, Andleeb S, Qadri I. 2014. Characterization of a virulent bacteriophage LK1 specific for Citrobacter freundii isolated from sewage water. J Basic Microbiol, 54:531–541.CrossRefPubMedGoogle Scholar
  15. Chhibber S, Kaur S, Kumari S. 2008. Therapeutic potential of bacteriophage in treating Klebsiella pneumoniae B5055-mediated lobar pneumonia in mice. J Med Microbiol, 57:1508–1513.CrossRefPubMedGoogle Scholar
  16. Daniel A, Euler C, Collin M, Chahales P, Gorelick KJ, Fischetti VA. 2010. Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother, 54:1603–1612.CrossRefPubMedCentralPubMedGoogle Scholar
  17. Denou E, Bruttin A, Barretto C, Ngom-Bru C, Brüssow H, Zuber S. 2009. T4 phages against Escherichia coli diarrhea: potential and problems. Virology, 388:21–30.CrossRefPubMedGoogle Scholar
  18. Denyes JM, Krell PJ, Manderville RA, Ackermann HW, She YM, Kropinski AM. 2014. The genome and proteome of Serratia bacteriophage η which forms unstable lysogens. Virol J, 11:6.CrossRefPubMedCentralPubMedGoogle Scholar
  19. d’Herelle F. 1917. Sur un microbe invisible antagoniste des bacilles dysentériques. Cr Acad Sci (Paris), 165: 373–375. (In French)Google Scholar
  20. Díaz E, López R, García JL. 1990. Chimeric phage-bacterial enzymes:a clue to the modular evolution of genes. Proc Natl Acad Sci U S A, 87:8125–8129.CrossRefPubMedCentralPubMedGoogle Scholar
  21. Donnenberg MS. 2002. Evolution of pathogenic Escherichia coli. In Escherichia coli: virulence mechanisms of a versatile pathogen. Amsterdam: Academic Press. pp. 55–173.Google Scholar
  22. Falagas ME, Kastoris AC, Kapaskelis AM, Karageorgopoulos DE. 2010. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum beta-lactamase producing, Enterobacteriaceae infections: a systematic review. Lancet Infect Dis, 10:43–50.CrossRefPubMedGoogle Scholar
  23. Fischetti VA. 2008. Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol, 11:393–400.CrossRefPubMedCentralPubMedGoogle Scholar
  24. Gründling A, Bläsi U, Young R. 2000. Genetic and biochemical analysis of dimer and oligomer interactions of the lambda S holin. J Bacteriol, 182: 6082–6090.CrossRefPubMedCentralPubMedGoogle Scholar
  25. Gründling A, Smith DL, Bläsi U, Young R. 2000. Dimerization between the holin and holin inhibitor of phage lambda. J Bacteriol, 182:6075–6081.CrossRefPubMedCentralPubMedGoogle Scholar
  26. Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, Sun C, Feng X. 2012. A method for generation phage cocktail with great therapeutic potential. PLoS One, 7:e31698.CrossRefPubMedCentralPubMedGoogle Scholar
  27. Gupta R, Prasad Y. 2011. Efficacy of polyvalent bacteriophage p-27/HP to control multidrug resistant Staphylococcus aureus associated with human infections. Curr Microbiol, 62:255–260.CrossRefPubMedGoogle Scholar
  28. Hankin E. 1896. L’action bactéricide des eaux de la Jumna et du Gange sur le vibrion du choléra. Ann Inst Pasteur (Paris), 10:511–523. (In French)Google Scholar
  29. Heithoff DM, Shimp WR, Lau PW, Badie G, Enioutina EY, Daynes RA, Byrne BA, House JK, Mahan MJ. 2008. Human Salmonella clinical isolates distinct from those of animal origin. Appl Environ Microbiol, 74:1757–1766.CrossRefPubMedCentralPubMedGoogle Scholar
  30. Hung CH, Kuo CF, Wang CH, Wu CM, Tsao N. 2011. Experimental phage therapy in treating Klebsiella pneumoniae-mediated liver abscesses and bacteremia in mice. Antimicrob Agents Chemother, 55:1358–1365.CrossRefPubMedCentralPubMedGoogle Scholar
  31. Iino T, Mitani M. 1967. Infection of Serratia marcescens by bacteriophage χ. J Virol, 1:445–447.PubMedCentralPubMedGoogle Scholar
  32. Larson EL, Cimiotti JP, Haas J, Nesin M, Allen A, Della-Latta P, Saiman L. 2005. Gram-negative bacilli associated with catheter-associated and non-catheter-associated bloodstream infections and hand carriage by healthcare workers in neonatal intensive care units. Pediatr Crit Care Med, 6:457–461.CrossRefPubMedGoogle Scholar
  33. Lazareva EB, Smirnov SV, Khvatov VB, Spiridonova TG, Bitkova EE, Darbeeva OS, Maĭskaia LM, Parfeniuk RL, Men’shikov DD. 2001. Efficacy of bacteriophages in complex treatment of patients with burn wounds. Antibiot Khimioter, 46:10–14.PubMedGoogle Scholar
  34. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A. 2001. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Prot, 64:1116–1121.PubMedGoogle Scholar
  35. Levine OS, Levine MM. 1991. Houseflies (Musca domestica) as mechanical vectors of shigellosis. Rev Infect Dis, 13:688–696.CrossRefPubMedGoogle Scholar
  36. Loessner MJ. 2005. Bacteriophage endolysins—current state of research and applications. Curr Opin Microbol, 8:480–487.CrossRefGoogle Scholar
  37. Malik R, Chhibber S. 2009. Protection with bacteriophage KØ1 against fatal Klebsiella pneumoniae-induced burn wound infection in mice. J Microbiol Immunol Infect, 42:134–140.PubMedGoogle Scholar
  38. Maragakis LL, Winkler A, Tucker MG, Cosgrove SE, Ross T, Lawson E, Carroll KC, Perl TM. 2008. Outbreak of multidrug-resistant Serratia marcescens infection in a neonatal intensive care unit. Infect Control Hosp Epidemiol, 29:418–423.CrossRefPubMedGoogle Scholar
  39. Matsushita K, Uchiyama J, Kato S, Ujihara T, Hoshiba H, Sugihara S, Muraoka A, Wakiguchi H, Matsuzaki S. 2009. Morphological and genetic analysis of three bacteriophages of Serratia marcescens isolated from environmental water. FEMS Microbiol Lett, 291:201–208.CrossRefPubMedGoogle Scholar
  40. McAuliffe O, Ross RP, Fitzgerals GF. 2007. The new phage biology: from genomics to applications. In Bacteriophage: Genetics and Molecular Biology (1st ed.). Mc Grath S and van Sinderen D. Norfolk, Engand: Caister Academic Press. pp. 1–42.Google Scholar
  41. Merril CR, Scholl D, Adhya SL. 2003. The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov, 2:489–497.CrossRefPubMedGoogle Scholar
  42. Messerschmidt A, Prayer D, Olischar M, Pollak A, Birnbacher R. 2004. Brain abscesses after Serratia marcescens infection on a neonatal intensive care unit: differences on serial imaging. Neuroradiology, 46:148–152.CrossRefPubMedGoogle Scholar
  43. Niyogi SK. 2005. Shigellosis. J Microbiol, 43:133–143.PubMedGoogle Scholar
  44. Pang T, Savva CG, Fleming KG, Struck DK, Young R. 2009. Structure of the lethal phage pinhole. Proc Natl Acad Sci U S A, 106:18966–18971.CrossRefPubMedCentralPubMedGoogle Scholar
  45. Pastagia M, Schuch R, Fischetti VA, Huang DB. 2013. Lysins: the arrival of pathogen-directed anti-infectives. J Med Microbiol, 62:1506–1516.CrossRefPubMedGoogle Scholar
  46. Paterson DL. 2006. Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med, 119:S20–28.CrossRefPubMedGoogle Scholar
  47. Payne RJ, Phil D, Jansen VA. 2000. Bacteriaphage therapy: the pecculiar kinetics of self-replicating pharmaceuticals. Clin Pharmacol Ther, 68: 225–230.CrossRefPubMedGoogle Scholar
  48. Phalipon A, Sansonetti PJ. 2007. Shigella’s ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? Immunol Cell Biol, 85:119–129.CrossRefPubMedGoogle Scholar
  49. Qian ZW, Yue QA, Tian FL. 2007. Study overview of phagotherapy. Med Recapitulate, 13:1256–1258. (In Chinese)Google Scholar
  50. Ramanculov E, Young R. 2001. Genetic analysis of the T4 holin: timing and topology. Gene, 265:25–36.CrossRefPubMedGoogle Scholar
  51. Reed CA, Langlais C, Kuznetsov V, Young R. 2012. Inhibitory mechanism of the Qβ lysis protein A2. Mol Microbiol, 86:836–844.CrossRefPubMedGoogle Scholar
  52. Samsygina GA, Boni EG. 1984. Bacteriophages and phage therapy in pediatric practice. Pediatriia, 4:67–70. (In Russian)PubMedGoogle Scholar
  53. Savva CG, Dewey JS, Deaton J, White RL, Struck DK, Holzenburg A, Young R. 2008. The holin of bacteriophage lambda forms rings with large diameter. Mol Microbiol, 69:784–793.CrossRefPubMedGoogle Scholar
  54. Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, Krause L, Huq S, Bibiloni R, Bruttin A, Reuteler G, Brüssow H. 2012. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology, 434:222–232.CrossRefPubMedGoogle Scholar
  55. Savarino SJ, Hall ER, Bassily S, Wierzba TF, Youssef FG, Peruski LF Jr, Abu-Elyazeed R, Rao M, Francis WM, El Mohamady H, Safwat M, Naficy AB, Svennerholm AM, Jertborn M, Lee YJ, Clemens JD. 2002. Introductory evaluation of an oral, killed whole cell enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine in Egyptian infants. Pediatr Infect Dis J, 21:322–330.CrossRefPubMedGoogle Scholar
  56. Sharma M, Patel JR, Conway WS, Ferguson S, Sulakvelidze A. 2009. Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettucet. J Food Prot, 72:1481–1485.PubMedGoogle Scholar
  57. Shi Y, Yan Y, Ji W, Du B, Meng X, Wang H, Sun J. 2012. Characterization and determination of holin protein of Streptococcus suis bacteriophage SMP in heterologous host. Virol J, 9:70.CrossRefPubMedCentralPubMedGoogle Scholar
  58. Si XD. 1955. Bacillary dysentery therapy using dysentery phage. Nat Med J China, 41:824–834. (In Chinese)Google Scholar
  59. Smith HW, Huggins MB. 1983. Effectiveness of phages in treating experimental Escherichia coli diarrhea in calves, piglets and lambs. J Gen Microbiol, 129:2659–2675.PubMedGoogle Scholar
  60. Snyder JD, Merson MH. 1982. The magnitude of the global problem of acute diarrheal disease: a review of active surveillance data. Bull World Health Organ, 60:605–613.PubMedCentralPubMedGoogle Scholar
  61. Subekti D, Oyofo BA, Tjaniadi P, Corwin AL, Larasati W, Putri M, Simanjuntak CH, Punjabi NH, Taslim J, Setiawan B, Djelantik AA, Sriwati L, Sumardiati A, Putra E, Campbell JR, Lesmana M. 2001. Shigella spp. surveillance in Indonesia: the emergence or reemergence of S. dysenteriae. Emerg Infect Dis, 7:137–140.CrossRefPubMedCentralPubMedGoogle Scholar
  62. Sulakvelidze A, Alavidze Z, Morris Jr JG. 2001. Bacteriophage therapy. Antimicrob Agents Chemother, 45: 649–659.CrossRefPubMedCentralPubMedGoogle Scholar
  63. Summers WC. 1999. Bacteriophage discovered, in Felix d’Herelle and the origins of molecular biology. New Haven, CT: Yale University Press. pp. 47–59.Google Scholar
  64. Tanaka S, Clemons WM Jr. 2012. Minimal requirements for inhibition of MraY by lysis protein E from bacteriophage φX174. Mol Microbiol, 85:975–985.CrossRefPubMedCentralPubMedGoogle Scholar
  65. Tsay RW, Siu LK, Fung CP, Chang FY. 2002. Characteristics of bacteremia between community-acquired and nosocomial Klebsiella pneumoniae infection: risk factor for mortality and the impact of capsular serotypes as a herald for community-acquired infection. Arch Intern Med, 162:1021–1027.CrossRefPubMedGoogle Scholar
  66. Twort FW. 1915. An investigation on the nature of ultra-microscopic viruses. Lancet, 189:1241–1243.CrossRefGoogle Scholar
  67. Verma V, Harjai K, Chhibber S. 2010. Structural changes induced by a lytic bacteriophage make ciprofloxacin effective against older biofilm of Klebsiella pneumoniae. Biofouling, 26:729–737.CrossRefPubMedGoogle Scholar
  68. Verma V, Harjai K, Chhibber S. 2009. Restricting ciprofloxacin-induced resistant variant formation in biofilm of Klebsiella pneumoniae B5055 by complementary bacteriophage treatment. J Antimicrob Chemother, 64:1212–1218.CrossRefPubMedGoogle Scholar
  69. Wall SK, Zhang J, Rostagno MH, Ebner PD. 2010. Phage therapy to reduce preprocessing Salmonella infections in market-weight swine. Appl Environ Microbiol, 76:48–53.CrossRefPubMedCentralPubMedGoogle Scholar
  70. Xu M, Struck DK, Deaton J, Wang IN, Young R. 2004. A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci U S A, 101:6415–6420.CrossRefPubMedCentralPubMedGoogle Scholar
  71. Yang Q, Wang H, Chen M, Ni Y, Yu Y, Hu B, Sun Z, Huang W, Hu Y, Ye H, Badal RE, Xu Y. 2010. Surveillance of antimicrobial susceptibility of aerobic and facultative Gram-negative bacilli isolated from patients with intra-abdominal infections in China: the 2002–2009 study for monitoring antimicrobial Resistance trends (SMART). Int J Antimicrob Agents, 36:507–512.CrossRefPubMedGoogle Scholar
  72. Yasuike M, Sugaya E, Nakamura Y, Shigenobu Y, Kawato Y, Kai W, Fujiwara A, Sano M, Kobayashi T, Nakai T. 2013. Complete genome sequences of Edwardsiella tarda-lytic bacteriophages KF-1 and IW-1. Genome Announc, 1: e00089–12.PubMedCentralPubMedGoogle Scholar
  73. Young R. 1992. Bacteriophage lysis: mechanism and regulation. Microbiol Rev, 56:430–481.PubMedCentralPubMedGoogle Scholar
  74. Young R, Bläsi U. 1995. Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev, 17:191–205.CrossRefPubMedGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Youqiang Xu
    • 1
    • 2
  • Yong Liu
    • 1
    • 2
  • Yang Liu
    • 1
    • 2
  • Jiangsen Pei
    • 1
    • 2
  • Su Yao
    • 1
    • 2
  • Chi Cheng
    • 1
    • 2
  1. 1.China National Research Institute of Food and Fermentation IndustriesBeijingChina
  2. 2.China Center of Industrial Culture CollectionBeijingChina

Personalised recommendations