Phage associated polysaccharide depolymerases – characteristics and application

COMMENTARY ON THE LAW

Phage associated polysaccharide depolymerases – characteristics and application

Agnieszka Maszewska 1

1. Zakład Immunobiologii Bakterii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki

Published: 2015-06-16
DOI: 10.5604/17322693.1157422
GICID: 01.3001.0009.6543
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2015; 69 : 690-702

 

Abstract

Bacteriophages have been of interest as agents combating undesirable bacteria since their discovery nearly 100 years ago. Currently, intensive research is being conducted into two groups of phage enzymes, which cause damage to bacterial cells. The first group includes lysins responsible for breaking down the cell wall in order to release progeny phages and the second is polysaccharides depolymerases (PDs), which degrade capsular and structural polysaccharides, including exopolysaccharides (EPS) – a dominant bacterial biofilm component. PDs can be attached to a phage tail or present as a free form diffused to the medium, their production takes place constitutively or is induced by the polysaccharide presence. PDs belong to two groups of enzymes: hydrolases (glycanases) or polysaccharide lyases. These enzymes are a very heterogeneous group with regard to substrate specificity, the molecular weight or sensitivity bakteriofato physical and chemical factors. Phages producing PDs act against encapsulated infectious bacteria and have a great potential as a new class of anti-biofilm agents. Polysaccharide depolymerases depriving bacteria of the capsule, reduce their virulence and sensitize them to the immune system. The variety of biofilms forming bacteria and exopolysaccharides produced by them requires the use of specific phages producing DP. The problem of DP and phages specificity can be solved by using phage cocktails or introducing into the virus genome genes encoding enzymes degrading various bacterial exopolysaccharides important in the biofilm formation or broadening the host range. The use of DP or a DP-producing phage combined with other antibiofilm agents brings promising results. This indicates a direction for further research to develop effective methods to combat bacterial biofilms. Phage-borne PDs can be used for determination of the bacterial polysaccharides structure or efficient capsular typing.

References

  • 1. Ackermann H.W.: Bacteriophage taxonomy. Microbiol. Australia,2011; 32: 90-94
    Google Scholar
  • 2. Adams M.H., Park B.H.: An enzyme produced by a phage-hostcell system. II. The properties of the polysaccharide depolymerase.Virology, 1956; 2: 719-736
    Google Scholar
  • 3. Antibiotic Resistance Threats in the United States, 2013; http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf(18.06.2014)
    Google Scholar
  • 4. Azeredo J., Sutherland I.W.: The use of phages for the removalof infectious biofilms. Curr. Pharm. Biotechnol., 2008; 9: 261-266
    Google Scholar
  • 5. Barnet Y.M., Humphrey B.: Exopolysaccharide depolymerasesinduced by Rhizobium bacteriophages. Can. J. Microbiol., 1975, 21:1647-1650
    Google Scholar
  • 6. Bartell P.F., Lam G.K., Orr T.E.: Purification and properties of polysaccharidedepolymerase associated with phage-infected Pseudomonasaeruginosa. J. Biol. Chem., 1968; 243: 2077-2080
    Google Scholar
  • 7. Bartell P.F., Orr T.E.: Origin of polysaccharide depolymerase associatedwith bacteriophage infection. J. Virol., 1969, 3: 290-296
    Google Scholar
  • 8. Bartell P.F., Orr T.E.: Distinct slime polysaccharide depolymerasesof bacteriophage-infected Pseudomonas aeruginosa: evidenceof close association with the structured bacteriophage particle. J.Virol., 1969; 4: 580-584
    Google Scholar
  • 9. Bedi M.S., Verma V., Chhibber S.: Amoxicillin and specific bacteriophagecan be used together for eradication of biofilm of Klebsiellapneumoniae B5055. World J. Microbiol. Biotechnol., 2009; 25:1145-1151
    Google Scholar
  • 10. Berlutti N., Morea C., Battistoni A., Sarli S., Cipriani P., Superti F.,Ammendolia M.G., Valenti P.: Iron availability influences aggregation,biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderiacenocepacia. Int. J. Imunopathol. Pharmacol., 2005; 18: 661-670
    Google Scholar
  • 11. Bessler W., Fehmel F., Freund-Mölbert E., Knüfermann H., SirimS.: Escherichia coli capsule bacteriophages IV. Free capsule depolymerase 29 J. Virol., 1975; 15: 976-984
    Google Scholar
  • 12. Betts A., Vasse M., Kaltz O., Hochberg M.E.: Back to the future:evolving bacteriophages to increase their effectiveness against thepathogen Pseudomonas aeruginosa PAO1. Evol. Appl., 2013; 6: 1054-1063
    Google Scholar
  • 13. Borysowski J., Łobocka M., Międzybrodzki R., Weber-DąbrowskaB., Górski A.: Potential of bacteriophages and their lysins in thetreatment of MRSA. Current status and future perspectives. Biodrugs,2011; 25: 347-355
    Google Scholar
  • 14. Borysowski J., Weber-Dąbrowska B., Górski A.: Bacteriophageendolysins as a novel class of antibacterial agents. Exp. Biol. Med.,2006; 231: 366-377
    Google Scholar
  • 15. Boucher H.W., Corey G.R.: Epidemiology of methicillin-resistantStaphylococcus aureus. Clin. Infect. Dis. 2008; 46: S344-S349
    Google Scholar
  • 16. Boucher H.W., Talbot G.H., Bradley J.S., Edwards J.E.Jr, Gilbert D.,Rice L.B., Scheld M., Spellberg B., Bartlett J.: Bad bugs, no drugs: noESKAPE! An update from the infectious diseases Society of America.Clin. Infect. Dis, 2009; 48: 1-12
    Google Scholar
  • 17. Brzozowska E., Bazan J., Gamian A.: Funkcje białek bakteriofagowych.Postępy Hig. Med. Dośw., 2011; 65: 167-76
    Google Scholar
  • 18. Carlton R.M.: Phage therapy: past history and future prospects.Arch. Immunol. Ther. Exp., 1999; 47: 267-274
    Google Scholar
  • 19. Carson L., Gorman S.P., Gilmore B.F.: The use of lytic bacteriophagesin the prevention and eradication of biofilms of Proteusmirabilis and Escherichia coli. FEMS Immunol. Med. Microbiol., 2010;59: 447-455
    Google Scholar
  • 20. Castillo F.J., Bartell P.F.: Localization and functional role of thePseudomonas bacteriophage 2 depolymerase. J. Virol., 1976; 18: 701-708
    Google Scholar
  • 21. Chen L., Wen Y.: The role of bacterial biofilm in persistent infectionsand control strategies. Int. J. Oral. Sci., 2011; 3: 66-73
    Google Scholar
  • 22. Chhibber S., Nag D., Bansal S.: Inhibiting biofilm formation byKlebsiella pneumoniae B5055 using an iron antagonizing molecule anda bacteriophage. BMC Microbiol., 2013; 13: 174
    Google Scholar
  • 23. Chibeu A., Lingohr E.J., Masson L., Manges A., Harel J., AckermannH.W., Kropinski A.M., Boerlin P.: Bacteriophages with theability to degrade uropathogenic Escherichia coli biofilms. Viruses,2012; 4: 471-487
    Google Scholar
  • 24. Clarke B.R., Esumeh F., Roberts I.S.: Cloning, expression, andpurification of the K5 capsular polysaccharide lyase (KflA) fromcoliphage K5A: evidence for two distinct K5 lyase enzymes. J. Bacteriol.,2000; 182: 3761-3766
    Google Scholar
  • 25. Comeau A.M., Tétart F., Trojet S.N., Prére M.F., Krisch H.M.:Phage-antibiotic synergy (PAS): β-lactam and quinolone antibioticsstimulate virulent phage growth. PLoS One, 2007; 2: e799
    Google Scholar
  • 26. Cornelissen A., Ceyssens P.J., Krylov V.N., Noben J.P., VolckaertG., Lavigne R.: Identification of EPS-degrading activity with in thetail spikes of the novel Pseudomonas putida phage AF. Virology, 2012;434: 251-256
    Google Scholar
  • 27. Cornelissen A., Ceyssens P.J., T’Syen J., Van Praet H., Noben J.P.,Shaburova O.V., Krylov V.N., Volckaert G., Lavigne R.: The T7-relatedPseudomonas putida phage φ15 displays virion-associated biofilmdegradation properties. PLoS One, 2011; 6: e18597
    Google Scholar
  • 28. Curtin J.J., Donlan R.M.: Using bacteriophages to reduce formationof catheter-associated biofilms by Staphylococcus epidermidis.Antimicrob. Agents Chemother., 2006; 50: 1268-1275
    Google Scholar
  • 29. Davidson I.W., Lawson C.J., Sutherland I.W.: An alginate lyasefrom Azotobacter vinelandii phage. J. Gen. Microbiol., 1977; 98: 223-229
    Google Scholar
  • 30. Donlan R.M.: Preventing biofilms of clinically relevant organismsusing bacteriophage. Trends Microbiol., 2009; 17: 66-72
    Google Scholar
  • 31. Donlan R.M.: Biofilm elimination on intravascular catheters:important considerations for the infectious disease practitioner.Clin. Infect. Dis., 2011; 52: 1038-1045
    Google Scholar
  • 32. Drulis-Kawa Z., Majkowska-Skrobek G., Maciejewska B., DelattreA.S., Lavigne R.: Learning from bacteriophages – advantages andlimitations of phage and phage-encoded protein applications. Curr.Protein Pept. Sci., 2012; 13: 699-722
    Google Scholar
  • 33. El-Safory N.S., Lee G.C., Lee C.K.: Characterization of hyaluronatelyase from Streptococcus pyogenes bacteriophage H4489A. CarbohydratePolymers, 2011; 84: 1182-1191
    Google Scholar
  • 34. Fenton M., Ross P., McAuliffe O., O’Mahony J., Coffey A.: Recombinantbacteriophage lysins as antibacterials. Bioeng. Bugs.,2010; 1: 9-16
    Google Scholar
  • 35. Fischetti V.A.: Bacteriophage endolysins: a novel anti-infectiveto control Gram-positive pathogens. Int. J. Med. Microbiol., 2010;300: 357-362
    Google Scholar
  • 36. Fu W., Forster T., Mayer O., Curtin J.J., Lehman S.M., Donlan R.M.:Bacteriophage cocktail for the prevention of biofilm formation byPseudomonas aeruginosa on catheters in an in vitro model system.Antimicrob. Agents Chemother., 2010; 54: 397-404
    Google Scholar
  • 37. Glonti T., Chanishvili N., Taylor P.W.: Bacteriophage-derivedenzyme that depolymerizes the alginic acid capsule associated withcystic fibrosis isolates of Pseudomonas aeruginosa. J. Appl. Microbiol.,2010; 108: 695-702
    Google Scholar
  • 38. Gutiérrez D., Martínez B., Rodríguez A., García P.: Genomic characterizationof two Staphylococcus epidermidis bacteriophages withanti-biofilm potential. BMC Genomics, 2012; 13: 228
    Google Scholar
  • 39. Hallenbeck P.C., Vimr E.R., Yu F., Bassler B.O., Troy F.A.: Purificationand properties of a bacteriophage-induced endo-N-acetylneuraminidasespecific for poly-α-2,8-sialosyl carbohydrate units.J. Biol. Chem., 1987; 262: 3553-3561
    Google Scholar
  • 40. Hancock V., Dahl M., Klemm P.: Abolition of biofilm formationin urinary tract Escherichia coli and Klebsiella isolates by metal interferencethrough competition for Fur. Appl. Environ. Microbiol.,2010; 76: 3836-3841
    Google Scholar
  • 41. Hanlon G.W., Denyer S.P., Olliff C.J., Ibrahim L.J.: Reduction inexopolysaccharide viscosity as an aid to bacteriophage penetrationthrough Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol.,2001; 67: 2746-2753
    Google Scholar
  • 42. Hoiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O.: Antibioticresistance of bacterial biofilms. Int. J. Antimicrob. Agents,2010; 35: 322-332
    Google Scholar
  • 43. Hsu C.R., Lin T.L., Pan Y.J., Hsieh P.F., Wang J.T.: Isolation ofa bacteriophage specific for a new capsular type of Klebsiella pneumoniaeand characterization of its polysaccharide depolymerase.PLoS One, 2013; 8: e70092
    Google Scholar
  • 44. Hughes K.A., Sutherland I.W., Jones M.V.: Biofilm susceptibilityto bacteriophage attack: the role of phage-borne polysaccharidedepolymerase. Microbiology, 1998; 144: 3039-3047
    Google Scholar
  • 45. Jakobsson E., Schwarzer D., Jokilammi A., Finne J.: Endosialidases:versatile tools for the study of polysialic acid. Top. Curr.Chem., 2012
    Google Scholar
  • 46. Kashiwagi A., Yomo T.: Ongoing phenotypic and genomic changesin experimental coevolution of RNA bacteriophage Qβ and Escherichiacoli. PLoS Genetics, 2011; 7: e1002188
    Google Scholar
  • 47. Kassa T., Chhibber S.: Thermal treatment of the bacteriophagelysate of Klebsiella pneumoniae B5055 as a step for the purification ofcapsular depolymerase enzyme. J. Virol. Methods , 2012; 179: 135-141
    Google Scholar
  • 48. Kim K.P., Cha J.D., Jang E.H. Klumpp J., Hagens S., Hardt W.D.,Lee K.Y., Loessner M.J.: PEGylation of bacteriophages increases bloodcirculation time and reduces T-helper type 1 immune response. Microb.Biotechnol., 2008; 1: 247-257
    Google Scholar
  • 49. Kostakioti M., Hadjifrangiskou M., and Hultgren S.J.: Bacterialbiofilms: development, dispersal, and therapeutic strategies in thedawn of the postantibiotic era. Cold Spring Harb. Perspect. Med.,2013; 3: a010306
    Google Scholar
  • 50. Kutateladze M., Adamia R.: Bacteriophages as potential newtherapeutics to replace or supplement antibiotics. Trends Biotechnol.,2010; 28: 591-595
    Google Scholar
  • 51. Legoux R., Lelong P., Jourde C., Feuillerat C., Capdevielle J., SureV., Ferran E., Kaghad M., Delpech B., Shire D., Ferrara P., Loison G.,Salomé M.: N-acetyl-heparosan lyase of Escherichia coli K5: gene cloningand expression. J. Bacteriol. 1996; 178: 7260-7264
    Google Scholar
  • 52. Lindsay A.M., Zhang M., Mitchell Z., Holden M.T., Waller A.S.,Sutcliffe I.C., Black G.W.: The Streptococcus equi prophage-encodedprotein SEQ2045 is a hyaluronan-specific hyaluronate lyase that isproduced during equine infection. Microbiology, 2009; 155: 443-449
    Google Scholar
  • 53. Linnerborg M., Weintraub A., Albert M.J., Widmalm G.: Depolymerizationof the capsular polysaccharide from Vibrio cholerae O139by a lyase associated with the bacteriophage JA1. Carbohydr. Res.,2001; 333: 263-269
    Google Scholar
  • 54. Liu Y., Li G., Mo Z., Chai Z., Shang A., Mou H.: Properties of Klebsiellaphage P13 and associated exopolysaccharide depolymerase.J. Ocean Univ. China, 2014; 13: 163-168
    Google Scholar
  • 55. Lu T.K., Collins J.J.: Dispersing biofilms with engineered enzymaticbacteriophage. Proc. Natl. Acad. Sci. USA, 2007; 104: 11197-11202
    Google Scholar
  • 56. Lu T.K., Collins J.J.: Engineered bacteriophage targeting genenetworks as adjuvants for antibiotic therapy. Proc. Natl. Acad. Sci.USA, 2009; 106: 4629-4634
    Google Scholar
  • 57. Lu T.K., Koeris M.S.: The next generation of bacteriophage therapy.Curr. Opinion Microbiol., 2011; 14: 524-531
    Google Scholar
  • 58. Łysiak K.: Bakteriofagi jako alternatywa dla antybiotyków – moż-liwości praktycznego ich zastosowania w chirurgii stomatologicznej– przegląd piśmiennictwa. Dent. Med. Probl., 2004; 41: 761-768
    Google Scholar
  • 59. Maura D., Debarbieux L.: Bacteriophages as twenty-first centuryantibacterial tools for food and medicine. Appl. Microbiol. Biotechnol.,2011; 90: 851-859
    Google Scholar
  • 60. Merril C.R., Biswas B., Carlton R., Jensen N.C., Creed G.J., ZulloS., Adhya S.: Long-circulating bacteriophage as antibacterial agents.Proc. Natl. Acad. Sci. USA, 1996; 93: 3188-3192
    Google Scholar
  • 61. Międzybrodzki R., Borysowski J., Fortuna W., Weber-DąbrowskaB., Górski A.: Terapia fagowa jako alternatywa w leczeniu zakażeńwywołanych przez bakterie antybiotykooporne. Kardiochir. Torakochir.Pol., 2006; 3: 201-205
    Google Scholar
  • 62. Międzybrodzki R., Borysowski J., Weber-Dabrowska B., LetkiewiczS., Szufnarowski K., Pawelczyk Z., Rogoz P., Klak M., Wojtasik E., GorskiA.: Clinical aspects of phage therapy. Adv. Virus Res., 2012; 83:73-121
    Google Scholar
  • 63. Moons P., Faster D., Aertsen A.: Lysogenic conversion and phageresistance development in phage exposed Escherichia coli biofilms.Viruses, 2013; 5: 150-161
    Google Scholar
  • 64. Moryl M., Torzewska A., Jałmużna P., Różalski A.: Analysis ofProteus mirabilis distribution in multi-species biofilms on urinarycatheters and determination of bacteria resistance to antimicrobialagents. Pol. J. Microbiol., 2013; 62: 377-384
    Google Scholar
  • 65. Mushtaq N., Redpath M.B., Luzio J.P., Taylor P.W.: Treatment ofexperimental Escherichia coli infection with recombinant bacteriophage-derivedcapsule depolymerase. J. Antimicrob. Chemother.,2005; 56: 160-165
    Google Scholar
  • 66. Nimmich W.: Detection of Escherichia coli K95 strains by bacteriophages.J. Clin. Microbiol., 1994; 32: 2843-2845
    Google Scholar
  • 67. Nimmich W., Schmidt G., Krallmann-Wenzel U.: Two differentEscherichia coli capsular polysaccharide depolymerases each associatedwith one of the coliphage φK5 and φK20. FEMS Microbiol.Lett., 1991; 82: 137-141
    Google Scholar
  • 68. Park J.K., Choi D.J., Kim S.M., Choi H.N., Park J.W., Jang S.J., ChooY.K., Lee C.G., Park Y.I.: Purification and characterization of a polysialicacid-specific sialidase from Pseudomonas fluorescens JK-0412. Biotechnol.Bioprocess Eng., 2012; 17: 526-537
    Google Scholar
  • 69. Pires D., Sillankorva S., Faustino A., Azeredo J.: Use of newly isolatedphages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res. Microbiol., 2011; 162: 798-806
    Google Scholar
  • 70. Potera C.: Phage renaissance: new hope against antibiotic resistance.Environ. Health Perspect., 2013; 121: a48-a53
    Google Scholar
  • 71. Rieger D., Freund-Molbert E., Stirm S.: Escherichia coli capsulebacteriophages. III. Fragments of bacteriophage 29. J. Virol., 1975;15: 964-975
    Google Scholar
  • 72. Rieger-Hug D., Stirm S.: Comparative study of host capsule depolymerasesassociated with Klebsiella bacteriophages. Virology,1981; 113: 363-378
    Google Scholar
  • 73. Ryan E.M., Alkawareek M.Y., Donnelly R.F., Gilmore B.F.: Synergisticphage-antibiotic combinations for the control of Escherichia colibiofilms in vitro. FEMS Immunol. Med. Microbiol., 2012; 65: 395-398
    Google Scholar
  • 74. Scholl D., Adhya S., Merril C.: Escherichia coli K1’s capsule is a barrierto bacteriophage T7. Appl. Environ. Microbiol., 2005; 71: 4872-4874
    Google Scholar
  • 75. Scholl D., Rogers S., Adhya S., Merril C.R.: Bacteriophage K1-5encodes two different tail fiber proteins, allowing it to infect andreplicate on both K1 and K5 strains of Escherichia coli. J. Virol., 2001;75: 2509-2515
    Google Scholar
  • 76. Siringan P., Connerton P.L., Payne R.J., Connerton I.F.: Bacteriophage-mediateddispersal of Campylobacter jejuni biofilms. Appl.Environ. Microbiol., 2011; 77: 3320-3326
    Google Scholar
  • 77. Srey S., Jahid I.K., Ha S.D.: Biofilm formation in food industries:a food safety concern. Food Control, 2013; 31: 572-585
    Google Scholar
  • 78. Stickler D.J.: Bacterial biofilms in patients with indwelling urinarycatheters. Nat. Clin. Pract. Urol., 2008; 5: 598-608
    Google Scholar
  • 79. Stummeyer K., Schwarzer D., Claus H., Vogel U., Gerardy-SchahnR., Mühlenhoff M.: Evolution of bacteriophages infecting encapsulatedbacteria: lessons from Escherichia coli K1-spesific phages. Mol.Microbiol., 2006; 60: 1123-1135
    Google Scholar
  • 80. Sulakvelidze A., Alavidze Z., Morris J.G.Jr.: Bacteriophage therapy.Antimicrob. Agents Chemother., 2001; 45: 649-659
    Google Scholar
  • 81. Sutherland I.W.: Polysaccharases for microbial exopolysaccharides.Carbohydr. Polym., 1999; 38: 319-328
    Google Scholar
  • 82. Sutherland I.W.: The exopolysaccharides of Klebsiella serotype 2strains as substrates for phage-induced polysaccharide depolymerases.J. Gen. Microbiol., 1971; 70: 331-338
    Google Scholar
  • 83. Sutherland I.W., Hughes K.A., Skillman L.C., Tait K.: The interactionof phage and biofilms. FEMS Microbiol. Lett., 2004; 232: 1-6
    Google Scholar
  • 84. Sutherland I.W., Wilkinson J.F.: Depolymerases for bacterialexopolysaccharides obtained from phage-infected bacteria. J. Gen.Microbiol., 1965; 39: 373-383
    Google Scholar
  • 85. Szymanek-Majchrzak K., Młynarczyk A., Młynarczyk G.: OpornośćStaphylococcus aureus na glikopeptydy. Post. Mikrobiol., 2013;52: 171-184
    Google Scholar
  • 86. Tait K., Skilmann L.C., Sutherland I.W.: The efficacy of bacteriophageas a method of biofilm eradication. Biofouling, 2002; 18:305-311
    Google Scholar
  • 87. Thompson J.E., Pourhossein M., Waterhouse A., Hudson T., GoldrickM., Derrick J.P., Roberts I.S.: The K5 lyase KflA combines a viraltail spike structure with a bacterial polysaccharide lyase mechanism.J. Biol. Chem., 2010; 285: 23693-23969
    Google Scholar
  • 88. Tomlinson S., Taylor P.W.: Neuraminidase associated with coliphageE that specifically depolymerizes the Escherichia coli KI capsularpolysaccharide. J. Virol., 1985; 55: 374-378
    Google Scholar
  • 89. Vandamme E.J.: Phage therapy and phage control: to be revisitedurgently!! J. Chem. Technol. Biotechnol., 2014; 89: 329-333
    Google Scholar
  • 90. Vandenbergh P.A., Wright A.M., Vidaver A.K.: Partial purificationand characterization of a polysaccharide depolymerase associatedwith phage-infected Erwinia amylovora. Appl. Environ. Microbiol.,1985; 49: 994-996
    Google Scholar
  • 91. Verma V., Harjai K., Chhibber S.: Characterization of a T7-likelytic bacteriophage of Klebsiella pneumoniae B5055: a potential therapeuticagents. Curr. Microbiol., 2009; 59: 274-281
    Google Scholar
  • 92. Verma V., Harjai K., Chhibber S.: Restricting ciprofloxacin inducedresistant variant formation in biofilm of Klebsiella pneumoniaeB5055 by complementary bacteriophage treatment. J. Antimicrob.Chemother., 2009; 64: 1212-1218
    Google Scholar
  • 93. Verma V., Harjai K., Chhibber S.: Structural changes induced bya lytic bacteriophage make ciprofloxacin effective against older biofilmof Klebsiella pneumoniae. Biofouling, 2010; 26: 729-737
    Google Scholar
  • 94. Viertel T.M., Ritter K., Horz H.P.: Viruses versus bacteria – novelapproaches to phage therapy as a tool against multidrug-resistantpathogens. J. Antimicrob. Chemother., 2014; 69: 2326-2336
    Google Scholar
  • 95. Vitiello C.L., Merril C.R., Adhya S.: An amino acid substitutionin a capsid protein enhances phage survival in mouse circulatorysystem more than a 1000-fold. Virus Res., 2005; 114: 101-103
    Google Scholar
  • 96. Walmagh M., Boczkowska B., Grymonprez B., Briers Y., Drulis–Kawa Z., Lavigne R.: Characterization of five novel endolysins fromGram-negative infecting bacteriophages. Appl. Microbiol. Biotech.,2013; 97: 4369-4375
    Google Scholar
  • 97. Weinbauer M.G.: Ecology of prokaryotic viruses. FEMS Microbiol.Rev., 2004; 28: 127-181
    Google Scholar
  • 98. Yurewicz E.C., Ghalambor M. A., Duckworth D.H., Heath E.C.:Catalytic and molecular properties of a phage-induced capsularpolysaccharide depolymerase. J. Biol. Chem., 1971; 246: 5607-5616
    Google Scholar
  • 99. Zhang Y., Hu Z.: Combined treatment of Pseudomonas aeruginosabiofilms with bacteriophages and chlorine. Biotechnol. Bioeng.,2013; 110: 286-295
    Google Scholar

Full text

Skip to content