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.
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References
Abedon ST, Thomas-Abedon C. 2010. Phage therapy pharmacology. Curr Pharm Biotechnol, 11:28–47.
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.
Anderson ES, Ward L, DeSaxe M, de Sa JD. 1977. Bacteriophage-typing designations of Salmonella typhimurium. J Hyg (Lond), 78:297–300.
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.
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.
Babalova EG, Katsitadze KT, Sakvarelidze LA, Imnaishvili NSh, Sharashidze TG, Badashvili VA, Kiknadze GP, MeÄpariani 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)
Bentley R, Bennett JW. 2003. What is an antibiotic? Revisited. Adv Appl Microbiol, 52:303–331.
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.
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.
Bruynoghe R, Maisin J. 1921. Essais de the rapeutique au moyen du bacteriophage. C R Soc Biol, 85:1120–1121.
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.
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.
Carlton RM. 1999. Phage therapy: past history and future prospects. Arch Immunol Ther Exp (Warsz), 47:267–274.
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.
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.
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.
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.
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.
d’Herelle F. 1917. Sur un microbe invisible antagoniste des bacilles dysentériques. Cr Acad Sci (Paris), 165: 373–375. (In French)
DÃaz E, López R, GarcÃa JL. 1990. Chimeric phage-bacterial enzymes:a clue to the modular evolution of genes. Proc Natl Acad Sci U S A, 87:8125–8129.
Donnenberg MS. 2002. Evolution of pathogenic Escherichia coli. In Escherichia coli: virulence mechanisms of a versatile pathogen. Amsterdam: Academic Press. pp. 55–173.
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.
Fischetti VA. 2008. Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol, 11:393–400.
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.
Gründling A, Smith DL, Bläsi U, Young R. 2000. Dimerization between the holin and holin inhibitor of phage lambda. J Bacteriol, 182:6075–6081.
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.
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.
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)
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.
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.
Iino T, Mitani M. 1967. Infection of Serratia marcescens by bacteriophage χ. J Virol, 1:445–447.
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.
Lazareva EB, Smirnov SV, Khvatov VB, Spiridonova TG, Bitkova EE, Darbeeva OS, MaÄskaia LM, Parfeniuk RL, Men’shikov DD. 2001. Efficacy of bacteriophages in complex treatment of patients with burn wounds. Antibiot Khimioter, 46:10–14.
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.
Levine OS, Levine MM. 1991. Houseflies (Musca domestica) as mechanical vectors of shigellosis. Rev Infect Dis, 13:688–696.
Loessner MJ. 2005. Bacteriophage endolysins—current state of research and applications. Curr Opin Microbol, 8:480–487.
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.
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.
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.
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.
Merril CR, Scholl D, Adhya SL. 2003. The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov, 2:489–497.
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.
Niyogi SK. 2005. Shigellosis. J Microbiol, 43:133–143.
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.
Pastagia M, Schuch R, Fischetti VA, Huang DB. 2013. Lysins: the arrival of pathogen-directed anti-infectives. J Med Microbiol, 62:1506–1516.
Paterson DL. 2006. Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med, 119:S20–28.
Payne RJ, Phil D, Jansen VA. 2000. Bacteriaphage therapy: the pecculiar kinetics of self-replicating pharmaceuticals. Clin Pharmacol Ther, 68: 225–230.
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.
Qian ZW, Yue QA, Tian FL. 2007. Study overview of phagotherapy. Med Recapitulate, 13:1256–1258. (In Chinese)
Ramanculov E, Young R. 2001. Genetic analysis of the T4 holin: timing and topology. Gene, 265:25–36.
Reed CA, Langlais C, Kuznetsov V, Young R. 2012. Inhibitory mechanism of the Qβ lysis protein A2. Mol Microbiol, 86:836–844.
Samsygina GA, Boni EG. 1984. Bacteriophages and phage therapy in pediatric practice. Pediatriia, 4:67–70. (In Russian)
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.
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.
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.
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.
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.
Si XD. 1955. Bacillary dysentery therapy using dysentery phage. Nat Med J China, 41:824–834. (In Chinese)
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.
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.
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.
Sulakvelidze A, Alavidze Z, Morris Jr JG. 2001. Bacteriophage therapy. Antimicrob Agents Chemother, 45: 649–659.
Summers WC. 1999. Bacteriophage discovered, in Felix d’Herelle and the origins of molecular biology. New Haven, CT: Yale University Press. pp. 47–59.
Tanaka S, Clemons WM Jr. 2012. Minimal requirements for inhibition of MraY by lysis protein E from bacteriophage φX174. Mol Microbiol, 85:975–985.
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.
Twort FW. 1915. An investigation on the nature of ultra-microscopic viruses. Lancet, 189:1241–1243.
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.
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.
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.
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.
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.
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.
Young R. 1992. Bacteriophage lysis: mechanism and regulation. Microbiol Rev, 56:430–481.
Young R, Bläsi U. 1995. Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev, 17:191–205.
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Xu, Y., Liu, Y., Liu, Y. et al. Bacteriophage therapy against Enterobacteriaceae . Virol. Sin. 30, 11–18 (2015). https://doi.org/10.1007/s12250-014-3543-6
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DOI: https://doi.org/10.1007/s12250-014-3543-6