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Bacteriophage Polysaccharide Depolymerases and Biomedical Applications

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An Erratum to this article was published on 18 March 2014

Abstract

Polysaccharide depolymerase, a polysaccharide hydrolase encoded by bacteriophages (or ‘phages’), can specifically degrade the macromolecule carbohydrates of the host bacterial envelope. This enzyme assists the bacteriophage in adsorbing, invading, and disintegrating the host bacteria. Polysaccharide depolymerase activity continues even within biofilms. This effectiveness means phages are promising candidates for novel antibiotic scaffolds. A comprehensive compendium of bacteriophage polysaccharide depolymerases has been compiled, together with their potential biomedical applications, such as novel antibiotics, adjuvants for antibiotics, bacterial biofilm disruptants, and diagnostic kits.

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References

  1. Whitfield C, Roberts IS. Structure, assembly and regulation of expression of capsules in Escherichia coli. Molecular Microbiol. 1999;31(5):1307–19. doi:10.1046/j.1365-2958.1999.01276.x.

    Article  CAS  Google Scholar 

  2. Bayer AS, Park S, Ramos MC, Nast CC, Eftekhar F, Schiller NL. Effects of alginase on the natural history and antibiotic therapy of experimental endocarditis caused by mucoid Pseudomonas aeruginosa. Infect Immun. 1992;60(10):3979–85. http://iai.asm.org/content/60/10/3979.short.

  3. Bayer AS, Speert DP, Park S, Tu J, Witt M, Nast CC, Norman DC. Functional role of mucoid exopolysaccharide (alginate) in antibiotic-induced and polymorphonuclear leukocyte-mediated killing of Pseudomonas aeruginosa. Infect Immun. 1991;59(1):302–8. http://europepmc.org/articles/PMC257741.

  4. Stiver HG, Zachidniak K, Speert DP. Inhibition of polymorphonuclear leukocyte chemotaxis by the mucoid exopolysaccharide of Pseudomonas aeruginosa. Clin Invest Med. 1988;11(4):247. http://www.ncbi.nlm.nih.gov/pubmed/2971496.

    Google Scholar 

  5. Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. J Immunol. 2005;175(11):7512–8. http://europepmc.org/abstract/MED/16301659.

    Google Scholar 

  6. Mrsny RJ, Lazazzera BA, Daugherty AL, Schiller NL, Patapoff TW. Addition of a bacterial alginate lyase to purulent CF sputum in vitro can result in the disruption of alginate and modification of sputum viscoelasticity. Pulm Pharmacol. 1994;7(6):357–66. http://www.ncbi.nlm.nih.gov/pubmed/7549223/.

  7. Ackermann H-W. Bacteriophage taxonomy. Viruses of prokaryotes. Tom I. 2011. http://microbiology.publish.csiro.au/paper/MA11090.htm.

  8. Casjens SR. Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol. 2005;8(4):451–8. http://dx.doi.org/10.1016/j.mib.2005.06.014.

    Google Scholar 

  9. Bradley DE. Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev. 1967;31(4):230. http://mmbr.asm.org/content/31/4/230.short.

    Google Scholar 

  10. Ackermann H-W. Tailed bacteriophages: the order caudovirales. Adv Virus Res. 1998;51:135–201. http://dx.doi.org/10.1016/S0065-3527(08)60785-X.

  11. Ackermann H-W. Classification of bacteriophages. Bacteriophages. 2006;2:8–16.

    Google Scholar 

  12. Ackermann H-W. 5500 Phages examined in the electron microscope. Archives Virol. 2007;152(2):227–43. doi:10.1007/s00705-006-0849-1.

    Article  CAS  Google Scholar 

  13. Barbirz S, Becker M, Freiberg A, Seckler R. Phage tailspike proteins with beta-solenoid fold as thermostable carbohydrate binding materials. Macromol Biosci. 2009;9(2):169–73. doi:10.1002/mabi.200800278.

    Article  CAS  PubMed  Google Scholar 

  14. Müller JJ, Barbirz S, Heinle K, Freiberg A, Seckler R, Heinemann U. An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri Phage Sf6. Structure. 2008;16(5):766–75. doi:10.1016/j.str.2008.01.019.

    Article  PubMed  Google Scholar 

  15. Israel V. A model for the adsorption of phage P22 to Salmonella typhimurium. J Gen Virol. 1978;40(3):669–73. doi:10.1099/0022-1317-40-3-669.

    Article  CAS  PubMed  Google Scholar 

  16. Baxa U, Steinbacher S, Miller S, Weintraub A, Huber R, Seckler R. Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J. 1996;71(4):2040–8. doi:10.1016/S0006-3495(96)79402-X.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Andres D, Hanke C, Baxa U, Seul A, Barbirz S, Seckler R. Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J Biol Chem. 2010;285(47):36768–75. doi:10.1074/jbc.M110.169003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R. Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Nat Acad Sci. 1996;93(20): 10584–8. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC38196/.

  19. Rashel M, Uchiyama J, Takemura I, Hoshiba H, Ujihara T, Takatsuji H, Honke K, Matsuzaki S. Tail-associated structural protein gp61 of Staphylococcus aureus phage φMR11 has bifunctional lytic activity. Fems Microbiol Lett. 2008;284(1):9–16. doi:10.1111/j.1574-6968.2008.01152.x.

    Article  CAS  PubMed  Google Scholar 

  20. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol. 2010;59:145–155. http://www.pjm.microbiology.pl/archive/vol5932010145.pdf.

    Google Scholar 

  21. Barbirz S, Müller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R. Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Molecular Microbiol. 2008;69(2):303–16. doi:10.1111/j.1365-2958.2008.06311.x.

    Article  CAS  Google Scholar 

  22. Chang JT, Schmid MF, Haase-Pettingell C, Weigele PR, King JA, Chiu W. Visualizing the structural changes of bacteriophage Epsilon15 and its Salmonella host during infection. J Molecular Biol. 2010;402(4):731–40. doi:10.1016/j.jmb.2010.07.058.

    Article  CAS  Google Scholar 

  23. Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, Hermo-Parrado XL, Llamas-Saiz AL, Seckler R, Miller S, van Raaij MJ. Structure of the receptor-binding protein of bacteriophage det7: a podoviral tail spike in a myovirus. J Virol. 2008;82(5):2265–73. doi:10.1128/JVI.01641-07.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Chua JE, Manning PA, Morona R. The Shigella flexneri bacteriophage Sf6 tailspike protein (TSP)/endorhamnosidase is related to the bacteriophage P22 TSP and has a motif common to exo-and endoglycanases, and C-5 epimerases. Microbiology. 1999;145(7):1649–59. doi:10.1099/13500872-145-7-1649.

    Article  CAS  PubMed  Google Scholar 

  25. Chaby R, Girard R. Adsorption and endo-glycosidase activity of phage phi 1 (40) on Salmonella johannesbureg O-polysaccharide. Virology. 1980;105(1):136–47.

    Article  CAS  PubMed  Google Scholar 

  26. Prehm P, Jann K. Enzymatic action of coliphage omega8 and its possible role in infection. J Virol. 1976;19(3):940–9. http://www.ncbi.nlm.nih.gov/pubmed/9521.

  27. Wong TY, Preston LA, Schiller NL. ALGINATE LYASE: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Ann Rev Microbiol. 2000;54:289–340. doi:10.1146/annurev.micro.54.1.289.

    Article  CAS  Google Scholar 

  28. Bartell PF, Orr TE, Lam GK. Polysaccharide depolymerase associated with bacteriophage infection. J Bacteriol. 1966;92(1):56–62. http://www.ncbi.nlm.nih.gov/pubmed/4957437.

    Google Scholar 

  29. Glonti T, Chanishvili N, Taylor PW. Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J Appl Microbiol. 2010;108(2):695–702. doi:10.1111/j.1365-2672.2009.04469.x.

    Article  CAS  PubMed  Google Scholar 

  30. Davidson IW, Lawson CJ, Sutherland IW. An alginate lysate from Azotobacter vinelandii phage. J Gen Microbiol. 1977;98(1):223–9. doi:10.1099/00221287-98-1-223.

    Article  CAS  PubMed  Google Scholar 

  31. Suda K, Tanji Y, Hori K, Unno H. Evidence for a novel Chlorella virus-encoded alginate lyase. Fems Microbiol Lett. 1999;180(1):45–53. doi:10.1111/j.1574-6968.1999.tb08776.x.

    Article  CAS  PubMed  Google Scholar 

  32. Osawa T, Matsubara Y, Muramatsu T, Kimura M, Kakuta Y. Crystal structure of the alginate (poly alpha-l-guluronate) lyase from Corynebacterium sp. at 1.2 A resolution. J Mol Biol. 2005;345(5):1111–8. http://dx.doi.org/10.1016/j.jmb.2004.10.081.

  33. Jakobsson E, Schwarzer D, Jokilammi A, Finne J. Endosialidases: versatile tools for the study of polysialic acid. Top Curr Chem. 2012. http://www.ncbi.nlm.nih.gov/pubmed/22851159.

  34. Amaya MF, Watts AG, Damager I, Wehenkel A, Nguyen T, Buschiazzo A, Paris G, Frasch AC, Withers SG, Alzari PM. Structural insights into the catalytic mechanism of Trypanosoma cruzi trans-sialidase. Structure. 2004;12(5):775–784. http://dx.doi.org/10.1016/j.str.2004.02.036.

  35. Watts AG, Oppezzo P, Withers SG, Alzari PM, Buschiazzo A. Structural and kinetic analysis of two covalent sialosyl-enzyme intermediates on Trypanosoma rangeli sialidase. J Biol Chem. 2006;281(7):4149–55. doi:10.1074/jbc.M510677200.

    Article  CAS  PubMed  Google Scholar 

  36. Li YT, Nakagawa H, Ross SA, Hansson GC, Li SC. A novel sialidase which releases 2,7-anhydro-alpha-N-acetylneuraminic acid from sialoglycoconjugates. J Biol Chem. 1990;265(35):21629–33. http://www.jbc.org/content/265/35/21629.short.

    Google Scholar 

  37. Morley TJ, Willis LM, Whitfield C, Wakarchuk WW, Withers SG. A new sialidase mechanism: bacteriophage K1F endo-sialidase is an inverting glycosidase. J Biol Chem. 2009;284(26):17404–10. doi:10.1074/jbc.M109.003970.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Kitajima K, Inoue S, Inoue Y, Troy FA. Use of a bacteriophage-derived endo-N-acetylneuraminidase and an equine antipolysialyl antibody to characterize the polysialyl residues in salmonid fish egg polysialoglycoproteins. Substrate and immunospecificity studies. J Biol Chem. 1988;263(34):18269–76. http://www.jbc.org/content/263/34/18269.short.

  39. Mühlenhoff M, Stummeyer K, Grove M, Sauerborn M, Gerardy-Schahn R. Proteolytic processing and oligomerization of bacteriophage-derived endosialidases. J Biol Chem. 2003;278(15):12634–44. doi:10.1074/jbc.M212048200.

    Article  PubMed  Google Scholar 

  40. Stummeyer K, Schwarzer D, Claus H, Vogel U, Gerardy-Schahn R, Mühlenhoff M. Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Molecular Microbiol. 2006;60(5):1123–35. doi:10.1111/j.1365-2958.2006.05173.x.

    Article  CAS  Google Scholar 

  41. Schwarzer D, Stummeyer K, Gerardy-Schahn R, Mühlenhoff M. Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem. 2007;282(5):2821–31. doi:10.1074/jbc.M609543200.

    Article  CAS  PubMed  Google Scholar 

  42. Jakobsson E, Jokilammi A, Aalto J, Ollikka P, Lehtonen JV, Hirvonen H, Finne J. Identification of amino acid residues at the active site of endosialidase that dissociate the polysialic acid binding and cleaving activities in Escherichia coli K1 bacteriophages. Biochem J. 2007;405(3):465. http://www.ncbi.nlm.nih.gov/pubmed/17394421.

  43. Gerardy-Schahn R, Bethe A, Brennecke T, Mühlenhoff M, Eckhardt M, Ziesing S, Lottspeich F, Frosch M. Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Molecular Microbiol. 1995;16(3):441–50. doi:10.1111/j.1365-2958.1995.tb02409.x.

    Article  CAS  Google Scholar 

  44. Petter JG, Vimr ER. Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol. 1993;175(14):4354–63. http://www.ncbi.nlm.nih.gov/pubmed/8331067.

  45. Scholl D, Merril C. The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli. J Bacteriol. 2005;187(24):8499–503. doi:10.1128/JB.187.24.8499-8503.2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Machida Y, Hattori K, Miyake K, Kawase Y, Kawase M, Iijima S. Molecular cloning and characterization of a novel bacteriophage-associated sialidase. J Biosci Bioeng. 2000;90(1):62–68. http://dx.doi.org/10.1016/S1389-1723(00)80035-3.

    Google Scholar 

  47. Scholl D, Rogers S, Adhya S, Merril CR. Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol. 2001;75(6):2509–15. doi:10.1128/JVI.75.6.2509-2515.2001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Mishra P, Prem Kumar R, Ethayathulla AS, Singh N, Sharma S, Perbandt M, Betzel C, Kaur P, Srinivasan A, Bhakuni V, Singh TP. Polysaccharide binding sites in hyaluronate lyase-crystal structures of native phage-encoded hyaluronate lyase and its complexes with ascorbic acid and lactose. FEBS J. 2009;276(12):3392–402. doi:10.1111/j.1742-4658.2009.07065.x.

    Article  CAS  PubMed  Google Scholar 

  49. Marković-Housley Z, Miglierini G, Soldatova L, Rizkallah PJ, Müller U, Schirmer T. Crystal structure of hyaluronidase, a major allergen of bee venom. Structure. 2000;8(10):1025–35. http://dx.doi.org/10.1016/S0969-2126(00)00511-6.

    Google Scholar 

  50. Jedrzejas MJ, Mello LV, de Groot BL, Li S. Mechanism of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. Structures of complexes with the substrate. J Biol Chem. 2002;277(31):28287–97. doi:10.1074/jbc.M112009200.

    Article  CAS  PubMed  Google Scholar 

  51. Meyer K. 11 Hyaluronidases. Enzymes. 1971;5:307–20.

    Article  CAS  Google Scholar 

  52. Niemann H, Birch-Andersen A, Kjems E, Mansa B, Stirm S. Streptococcal bacteriophage 12/12-borne hyaluronidase and its characterization as a lyase (EC 4.2.99.1) by means of streptococcal hyaluronic acid and purified bacteriophage suspensions. Acta Pathologica Microbiologica Scandinavica Section B. Microbiology. 1976;84(3):145–53. doi:10.1111/j.1699-0463.1976.tb01917.x.

    CAS  PubMed  Google Scholar 

  53. Hynes WL, Hancock L, Ferretti JJ. Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immun. 1995;63(8):3015–20. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC173410/.

  54. Smith NL, Taylor EJ, Lindsay AM, Charnock SJ, Turkenburg JP, Dodson EJ, Davies GJ, Black GW. Structure of a group A streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded beta-helix. Proc Natl Acad Sci USA. 2005;102(49):17652–7. doi:10.1073/pnas.0504782102.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Lindsay AM, Zhang M, Mitchell Z, Holden MT, Waller AS, Sutcliffe IC, Black GW. The Streptococcus equi prophage-encoded protein SEQ2045 is a hyaluronan-specific hyaluronate lyase that is produced during equine infection. Microbiology. 2009;155(Pt 2):443–9. doi:10.1099/mic.0.020826-0.

    Article  CAS  PubMed  Google Scholar 

  56. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009;37(suppl 1):D233–8. doi:10.1093/nar/gkn663.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Hynes WL, Ferretti JJ. Sequence analysis and expression in Escherichia coli of the hyaluronidase gene of Streptococcus pyogenes bacteriophage H4489A. Infection and Immunity. 1989;57(2):533–9. http://www.ncbi.nlm.nih.gov/pubmed/2643574.

  58. Baker JR, Dong S, Pritchard DG. Pritchard, the hyaluronan lyase of Streptococcus pyogenes bacteriophage H4489A. Biochem J. 2002;365(Pt 1):317–22. doi:10.1042/BJ20020149.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Martinez-Fleites C, Smith NL, Turkenburg JP, Black GW, Taylor EJ. Structures of two truncated phage-tail hyaluronate lyases from Streptococcus pyogenes serotype M1. Acta Crystallogr Section F Struct Biol Cryst Commun. 2009;65(10):963–6. doi:10.1107/S1744309109032813.

    Article  CAS  Google Scholar 

  60. Thompson JE, Pourhossein M, Waterhouse A, Hudson T, Goldrick M, Derrick JP, Roberts IS. The K5 lyase KflA combines a viral tail spike structure with a bacterial polysaccharide lyase mechanism. J Biol Chem. 2010;285(31):23963–9. doi:10.1074/jbc.M110.127571.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Yurewicz EC, Ghalambor MA, Duckworth DH, Heath EC. Catalytic and molecular properties of a phage-induced capsular polysaccharide depolymerase. J Biol Chem. 1971;246(18):5607–16. http://www.ncbi.nlm.nih.gov/pubmed/5096084.

    Google Scholar 

  62. Flachowsky H, Richter K, Kim WS, Geider K, Hanke MV. Transgenic expression of a viral EPS-depolymerase is potentially useful to induce fire blight resistance in apple. Annals Appl Biol. 2008;153(3):345–55. doi:10.1111/j.1744-7348.2008.00264.x.

    Article  CAS  Google Scholar 

  63. Scholl D, Cooley M, Williams SR, Gebhart D, Martin D, Bates A, Mandrell R. An engineered R-type pyocin is a highly specific and sensitive bactericidal agent for the food-borne pathogen Escherichia coli O157: H7. Antimicrob Agents Chemother. 2009;53(7):3074–80. doi:10.1128/AAC.01660-08.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Tenke P, Riedl CR, Jones GL, Williams GJ, Stickler D, Nagy E. Bacterial biofilm formation on urologic devices and heparin coating as preventive strategy. Int J Antimicrob Agents. 2004;23:67–74. http://www.ncbi.nlm.nih.gov/pubmed/15037330.

    Google Scholar 

  65. Lu TK, Collins JJ. Dispersing biofilms with engineered enzymatic bacteriophage. Proc Nat Acad Sci. 2007;104(27):11197–202. http://www.pnas.org/content/104/27/11197.long.

    Google Scholar 

  66. Donlan RM. Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol. 2009;17(2):66–72. doi:10.1016/j.tim.2008.11.002.

    Article  CAS  PubMed  Google Scholar 

  67. Hughes KA, Sutherland IW, Jones MV. Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology. 1998;144(11):3039–47. doi:10.1099/00221287-144-11-3039.

    Article  CAS  PubMed  Google Scholar 

  68. Carson L, Gorman SP, Gilmore BF. The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis and Escherichia coli. FEMS Immunol Med Microbiol. 2010;59(3):447–55. doi:10.1111/j.1574-695X.2010.00696.x.

    CAS  PubMed  Google Scholar 

  69. Meng X, Shi Y, Ji W, Meng X, Zhang J, Wang H, Lu C, Sun J, Yan Y. Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl Environ Microbiol. 2011;77(23):8272–9. doi:10.1128/AEM.05151-11.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Chibeu A, Lingohr EJ, Masson L, Manges A, Harel J, Ackermann HW, Kropinski AM, Boerlin P. Bacteriophages with the ability to degrade uropathogenic Escherichia coli biofilms. Viruses. 2012;4(4):471–87. doi:10.3390/v4040471.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Doolittle MM, Cooney JJ, Caldwell DE. Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can J Microbiol. 1995;41(1):12–18. http://europepmc.org/abstract/MED/7728652.

    Google Scholar 

  72. Verma V, Harjai K, Chhibber S. Structural changes induced by a lytic bacteriophage make ciprofloxacin effective against older biofilm of Klebsiella pneumoniae. Biofouling. 2010;26(6):729–37. doi:10.1080/08927014.2010.511196.

    Article  CAS  PubMed  Google Scholar 

  73. Kassa T, Chhibber S. Thermal treatment of the bacteriophage lysate of Klebsiella pneumoniae B5055 as a step for the purification of capsular depolymerase enzyme. J Virol Methods. 2012;179(1):135–41. doi:10.1016/j.jviromet.2011.10.011.

    Article  CAS  PubMed  Google Scholar 

  74. Kumon H, Tomochika K, Matunaga T, Ogawa M, Ohmori H. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol Immunol. 1994;38(8):615–9. http://www.ncbi.nlm.nih.gov/pubmed/7799834.

  75. Hatch RA, Schiller NL. Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1998;42(4):974–7. http://aac.asm.org/content/42/4/974.short.

  76. Hay ID, Gatland K, Campisano A, Jordens JZ, Rehm BH. Impact of alginate overproduction on attachment and biofilm architecture of a supermucoid Pseudomonas aeruginosa strain. Appl Environ Microbiol. 2009;75(18):6022–5. doi:10.1128/AEM.01078-09.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Alkawash MA, Soothill JS, Schiller NL. Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS. 2006;114(2):131–8. doi:10.1111/j.1600-0463.2006.apm_356.x.

    Article  CAS  PubMed  Google Scholar 

  78. Lamppa JW, Griswold KE. Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother. 2013;57(1):137–45. doi:10.1128/AAC.01789-12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Roth J, Zuber C, Wagner P, Taatjes DJ, Weisgerber C, Heitz PU, Goridis C, Bitter-Suermann D. Reexpression of poly (sialic acid) units of the neural cell adhesion molecule in Wilms tumor. Proc Nat Acad Sci. 1988;85(9):2999–3003. http://www.pnas.org/content/85/9/2999.short.

  80. Miettinen M, Cupo W. Neural cell adhesion molecule distribution in soft tissue tumors. Hum Pathol. 1993;24(1):62–6. http://dx.doi.org/10.1016/0046-8177(93)90064-N.

  81. Seidenfaden R, Krauter A, Schertzinger F, Gerardy-Schahn R, Hildebrandt H. Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol Cell Biol. 2003;23(16):5908–18. doi:10.1128/MCB.23.16.5908- 5918.2003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Finne J, Leinonen M, Mäkelä PH. Antigenic similarities between brain components and bacteria causing meningitis: implications for vaccine development and pathogenesis. Lancet. 1983;322(8346):355–7. http://dx.doi.org/10.1016/S0140-6736(83)90340-9.

  83. Vimr E, Steenbergen S, Cieslewicz M. Biosynthesis of the polysialic acid capsule in Escherichia coli K1. J Ind Microbiol. 1995;15(4):352–60. http://www.ncbi.nlm.nih.gov/pubmed/8605072.

  84. Jokilammi A, Ollikka P, Korja M, Jakobsson E, Loimaranta V, Haataja S, Hirvonen H, Finne J. Construction of antibody mimics from a noncatalytic enzyme-detection of polysialic acid. J Immunol Methods. 2004;295(1):149–60. http://dx.doi.org/10.1016/j.jim.2004.10.006.

    Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation (grant numbers 81371851,81071316, 81271882), the National Megaprojects for Key Infectious Diseases (grant numbers 2008ZX10003-006), New Century Excellent Talents in Universities (grant number NCET-11-0703), Excellent PhD thesis fellowship of Southwest University (grant numbers kb2010017, ky2011003), the Fundamental Research Funds for the Central Universities (grant numbers XDJK2011D006, XDJK2012D011, XDJK2012D007, and XDJK2013D003), Natural Science Foundation Project of CQ CSTC (grant number CSTC 2010BB5002), The Chongqing Municipal Committee of Education for Postgraduates Excellence Program (grant numbers YJG123104), The Undergraduates Teaching Reform Program (grant numbers 2011JY052).

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Yan, J., Mao, J. & Xie, J. Bacteriophage Polysaccharide Depolymerases and Biomedical Applications. BioDrugs 28, 265–274 (2014). https://doi.org/10.1007/s40259-013-0081-y

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