1,903
Views
0
CrossRef citations to date
0
Altmetric
Review article

Potential of phage depolymerase for the treatment of bacterial biofilms

ORCID Icon, &
Article: 2273567 | Received 07 Mar 2023, Accepted 30 Aug 2023, Published online: 31 Oct 2023

References

  • No authors listed. United Nations meeting on antimicrobial resistance. Bull World Health Organ. 2016;94(9):638–19. doi: 10.2471/BLT.16.020916
  • Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–1322. doi: 10.1126/science.284.5418.1318
  • Wang S, Ding Q, Zhang Y, et al. Evolution of virulence, fitness, and carbapenem resistance transmission in ST23 hypervirulent Klebsiella pneumoniae with the capsular polysaccharide synthesis gene wcaJ Inserted via insertion sequence elements. Microbiol Spectr. 2022;10(6):e0240022. doi: 10.1128/spectrum.02400-22
  • Caldara M, Belgiovine C, Secchi E, et al. Environmental, microbiological, and immunological features of bacterial biofilms associated with implanted medical devices. Clin Microbiol Rev. 2022;35(2):e0022120. doi: 10.1128/cmr.00221-20
  • Singh A, Amod A, Pandey P, et al. Bacterial biofilm infections, their resistance to antibiotics therapy and current treatment strategies. Biomed Mater. 2022;17(2):17. doi: 10.1088/1748-605X/ac50f6
  • Rasool FN, Saavedra MA, Pamba S, et al. Isolation and characterization of human pathogenic multidrug resistant bacteria associated with plastic litter collected in Zanzibar. J Hazard Mater. 2021;405:124591. doi: 10.1016/j.jhazmat.2020.124591
  • Shahed-Al-Mahmud M, Roy R, Sugiokto FG, et al. Phage φAB6-borne depolymerase combats Acinetobacter baumannii biofilm formation and infection. Antibiotics. 2021;10(3):10. doi: 10.3390/antibiotics10030279
  • Li M, Wang H, Chen L, et al. Identification of a phage-derived depolymerase specific for KL47 capsule of Klebsiella pneumoniae and its therapeutic potential in mice. Virol Sin. 2022;37(4):538–546. doi: 10.1016/j.virs.2022.04.005
  • Timoshina OY, Kasimova AA, Shneider MM, et al. Loss of a branch sugar in the Acinetobacter baumannii K3-type capsular polysaccharide due to Frameshifts in the gtr6 glycosyltransferase gene leads to susceptibility to phage APK37.1. Microbiol Spectr. 2023;11(1):e0363122. doi: 10.1128/spectrum.03631-22
  • Pires DP, Oliveira H, Melo LD, et al. Bacteriophage-encoded depolymerases: their diversity and biotechnological applications. Appl Microbiol Biotechnol. 2016;100(5):2141–2151. doi: 10.1007/s00253-015-7247-0
  • Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B. Bacteriophages and phage-derived proteins–application approaches. Curr Med Chem. 2015;22(14):1757–1773. doi: 10.2174/0929867322666150209152851
  • Topka-Bielecka G, Dydecka A, Necel A, et al. Bacteriophage-derived depolymerases against bacterial biofilm. Antibiotics. 2021;10(2):10. doi: 10.3390/antibiotics10020175
  • Majkowska-Skrobek G, Latka A, Berisio R, et al. Capsule-Targeting Depolymerase, derived from Klebsiella KP36 phage, as a tool for the development of anti-virulent strategy. Viruses. 2016;8(12):324. doi: 10.3390/v8120324
  • Abdelkader K, Gutierrez D, Latka A, et al. The specific capsule depolymerase of phage PMK34 sensitizes Acinetobacter baumannii to serum killing. Antibiotics. 2022;11(5):11. doi: 10.3390/antibiotics11050677
  • Wu Y, Wang R, Xu M, et al. A novel polysaccharide depolymerase encoded by the phage SH-KP152226 confers specific activity against multidrug-resistant Klebsiella pneumoniae via biofilm degradation. Front Microbiol. 2019;10:2768. doi: 10.3389/fmicb.2019.02768
  • Chen X, Liu M, Zhang P, et al. Phage-Derived Depolymerase as an antibiotic adjuvant against Multidrug-Resistant Acinetobacter baumannii. Front Microbiol. 2022;13:845500. doi: 10.3389/fmicb.2022.845500
  • Sutherland IW. The biofilm matrix–an immobilized but dynamic microbial environment. Trends Microbiol. 2001;9(5):222–227. doi: 10.1016/S0966-842X(01)02012-1
  • Belfield K, Bayston R, Birchall JP, et al. Do orally administered antibiotics reach concentrations in the middle ear sufficient to eradicate planktonic and biofilm bacteria? A review. Int J Pediatr Otorhinolaryngol. 2015;79(3):296–300. doi: 10.1016/j.ijporl.2015.01.003
  • Hoiby N, Bjarnsholt T, Givskov M, et al. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35(4):322–332. doi: 10.1016/j.ijantimicag.2009.12.011
  • Kostakioti M, Hadjifrangiskou M, Hultgren SJ. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med. 2013;3(4):a010306. doi: 10.1101/cshperspect.a010306
  • Jang H, Rusconi R, Stocker R. Biofilm disruption by an air bubble reveals heterogeneous age-dependent detachment patterns dictated by initial extracellular matrix distribution. NPJ Biofilms Microbiomes. 2017;3(1):6. doi: 10.1038/s41522-017-0014-5
  • Abebe GM. The role of bacterial biofilm in antibiotic resistance and food contamination. Int J Microbiol. 2020;2020:1705814. doi: 10.1155/2020/1705814
  • Petrova OE, Sauer K. Sticky situations: key components that control bacterial surface attachment. J Bacteriol. 2012;194(10):2413–2425. doi: 10.1128/JB.00003-12
  • Jamal M, Ahmad W, Andleeb S, et al. Bacterial biofilm and associated infections. J Chin Med Assoc. 2018;81(1):7–11. doi: 10.1016/j.jcma.2017.07.012
  • Habash M, Reid G. Microbial biofilms: their development and significance for medical device-related infections. J Clin Pharmacol. 1999;39(9):887–898. doi: 10.1177/00912709922008506
  • Legoux R, Lelong P, Jourde C, et al. N-acetyl-heparosan lyase of Escherichia coli K5: gene cloning and expression. J Bacteriol. 1996;178(24):7260–7264. doi: 10.1128/jb.178.24.7260-7264.1996
  • Blanco-Cabra N, Paetzold B, Ferrar T, et al. Characterization of different alginate lyases for dissolving Pseudomonas aeruginosa biofilms. Sci Rep. 2020;10(1):9390. doi: 10.1038/s41598-020-66293-2
  • Lahiri D, Nag M, Dey A, et al. Immobilized enzymes as potent antibiofilm agent. Biotechnol Prog. 2022;38(5):e3281. doi: 10.1002/btpr.3281
  • Woolcock JB. The capsule of Streptococcus equi. J Gen Microbiol. 1974;85(2):372–375. doi: 10.1099/00221287-85-2-372
  • Latka A, Maciejewska B, Majkowska-Skrobek G, et al. Bacteriophage-encoded virion-associated enzymes to overcome the carbohydrate barriers during the infection process. Appl Microbiol Biotechnol. 2017;101(8):3103–3119. doi: 10.1007/s00253-017-8224-6
  • Singh R, Sahore S, Kaur P, et al. Penetration barrier contributes to bacterial biofilm-associated resistance against only select antibiotics, and exhibits genus-, strain- and antibiotic-specific differences. Pathog Dis. 2016;74(6):ftw056. doi: 10.1093/femspd/ftw056
  • Singh R, Ray P, Das A, et al. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother. 2010;65(9):1955–1958. doi: 10.1093/jac/dkq257
  • Nguyen H, Nguyen TH, Otto M. The staphylococcal exopolysaccharide PIA - Biosynthesis and role in biofilm formation, colonization, and infection. Comput Struct Biotechnol J. 2020;18:3324–3334. doi: 10.1016/j.csbj.2020.10.027
  • Nuryastuti T, Krom BP. Ica-status of clinical Staphylococcus epidermidis strains affects adhesion and aggregation: a thermodynamic analysis. Antonie Van Leeuwenhoek. 2017;110(11):1467–1474. doi: 10.1007/s10482-017-0899-2
  • Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother. 2000;44(7):1818–1824. doi: 10.1128/AAC.44.7.1818-1824.2000
  • Hoyle BD, Alcantara J, Costerton JW. Pseudomonas aeruginosa biofilm as a diffusion barrier to piperacillin. Antimicrob Agents Chemother. 1992;36(9):2054–2056. doi: 10.1128/AAC.36.9.2054
  • Abdi-Ali A, Mohammadi-Mehr M, Agha AY. Bactericidal activity of various antibiotics against biofilm-producing Pseudomonas aeruginosa. Int J Antimicrob Agents. 2006;27(3):196–200. doi: 10.1016/j.ijantimicag.2005.10.007
  • Wu Y, Klapper I, Stewart PS. Hypoxia arising from concerted oxygen consumption by neutrophils and microorganisms in biofilms. Pathog Dis. 2018;76(4). doi: 10.1093/femspd/fty043
  • Pabst B, Pitts B, Lauchnor E, et al. Gel-entrapped Staphylococcus aureus bacteria as models of biofilm infection exhibit growth in dense aggregates, oxygen limitation, antibiotic tolerance, and heterogeneous gene expression. Antimicrob Agents Chemother. 2016;60(10):6294–6301. doi: 10.1128/AAC.01336-16
  • Uribe-Alvarez C, Chiquete-Felix N, Contreras-Zentella M, et al. Staphylococcus epidermidis: metabolic adaptation and biofilm formation in response to different oxygen concentrations. Pathog Dis. 2016;74(1):ftv111. doi: 10.1093/femspd/ftv111
  • Pulukkody AC, Yung YP, Donnarumma F, et al. Spatially resolved analysis of Pseudomonas aeruginosa biofilm proteomes measured by laser ablation sample transfer. PLoS One. 2021;16(7):e0250911. doi: 10.1371/journal.pone.0250911
  • Ramos-Gonzalez MI, Travieso ML, Soriano MI, et al. Genetic dissection of the regulatory network associated with high c-di-GMP levels in Pseudomonas putida KT2440. Front Microbiol. 2016;7:1093. doi: 10.3389/fmicb.2016.01093
  • Mills E, Petersen E, Kulasekara BR, et al. A direct screen for c-di-GMP modulators reveals a salmonella typhimurium periplasmic ʟ-arginine–sensing pathway. Sci Signal. 2015;8(380):ra57. doi: 10.1126/scisignal.aaa1796
  • Anderl JN, Zahller J, Roe F, et al. Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother. 2003;47(4):1251–1256. doi: 10.1128/AAC.47.4.1251-1256.2003
  • Hunter RC, Beveridge TJ. Application of a pH-sensitive fluoroprobe (C-SNARF-4) for pH microenvironment analysis in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 2005;71(5):2501–2510. doi: 10.1128/AEM.71.5.2501-2510.2005
  • Venglarcik JR, Blair LL, Dunkle LM. pH-dependent oxacillin tolerance of Staphylococcus aureus. Antimicrob Agents Chemother. 1983;23(2):232–235. doi: 10.1128/AAC.23.2.232
  • Xu KD, McFeters GA, Stewart PS. Biofilm resistance to antimicrobial agents. Microbiology (Reading). 2000;146(Pt 3):547–549. doi: 10.1099/00221287-146-3-547
  • Zheng Z, Stewart PS. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother. 2002;46(3):900–903. doi: 10.1128/AAC.46.3.900-903.2002
  • Schierholz JM, Beuth J, Pulverer G. Killing effects of antibiotics and two-fold antimicrobial combinations on proliferating and non growing staphylococci. Zentralbl Bakteriol. 1998;288(4):527–539. doi: 10.1016/S0934-8840(98)80072-8
  • Zimmerli W, Frei R, Widmer AF, et al. Microbiological tests to predict treatment outcome in experimental device-related infections due to Staphylococcus aureus. J Antimicrob Chemother. 1994;33:959–967.
  • Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis. 2015;34(5):877–886. doi: 10.1007/s10096-015-2323-z
  • Savage VJ, Chopra I, O’Neill AJ. Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrob Agents Chemother. 2013;57(4):1968–1970. doi: 10.1128/AAC.02008-12
  • Kouzel N, Oldewurtel ER, Maier B, et al. Gene transfer efficiency in gonococcal biofilms: role of biofilm Age, architecture, and pilin antigenic variation. J Bacteriol. 2015;197(14):2422–2431. doi: 10.1128/JB.00171-15
  • Tanner WD, Atkinson RM, Goel RK, et al. Horizontal transfer of the blaNDM-1 gene to Pseudomonas aeruginosa and Acinetobacter baumannii in biofilms. FEMS Microbiol Lett. 2017;364(8). doi: 10.1093/femsle/fnx048
  • Fisarova L, Botka T, Du X, et al. Staphylococcus epidermidis phages transduce antimicrobial resistance plasmids and mobilize chromosomal islands. mSphere. 2021;6(3):6. doi: 10.1128/mSphere.00223-21
  • Lattar SM, Wu X, Brophy J, et al. A mechanism of unidirectional Transformation, leading to antibiotic resistance, occurs within nasopharyngeal pneumococcal biofilm consortia. MBio. 2018;9(3). doi: 10.1128/mBio.00561-18
  • Uruen C, Chopo-Escuin G, Tommassen J, et al. Biofilms as promoters of bacterial antibiotic resistance and tolerance. Antibiotics. 2020;10(1):10. doi: 10.3390/antibiotics10010003
  • Driffield K, Miller K, Bostock JM, et al. Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother. 2008;61(5):1053–1056. doi: 10.1093/jac/dkn044
  • Sultan AM, Amer GF, Nabiel Y. Quinolone-resistant uropathogenic E. coli: is there a relation between qnr genes, gyrA gene target site mutation and biofilm formation? J Med Microbiol. 2021;70(10). doi: 10.1099/jmm.0.001432
  • Turkel I, Yildirim T, Yazgan B, et al. Relationship between antibiotic resistance, efflux pumps, and biofilm formation in extended-spectrum β-lactamase producing Klebsiella pneumoniae. J Chemother. 2018;30(6–8):354–363. doi: 10.1080/1120009X.2018.1521773
  • Knight DB, Rudin SD, Bonomo RA, et al. Acinetobacter nosocomialis: defining the role of efflux pumps in resistance to antimicrobial therapy, surface motility, and biofilm formation. Front Microbiol. 2018;9:1902. doi: 10.3389/fmicb.2018.01902
  • Li XF, Shi HQ, Liang Y, et al. Interaction of biofilm and efflux pump in clinical isolates of carbapenem resistant P. aeruginosa. Eur Rev Med Pharmacol Sci. 2022;26(5):1729–1737. doi: 10.26355/eurrev_202203_28242
  • Lin H, Paff ML, Molineux IJ, et al. Therapeutic application of phage capsule depolymerases against K1, K5, and K30 capsulated E. coli in mice. Front Microbiol. 2017;8:2257. doi: 10.3389/fmicb.2017.02257
  • Nimmich W, Schmidt G, Krallmann-Wenzel U. Two different Escherichia coli capsular polysaccharide depolymerases each associated with one of the coliphage φK5 and φK20. FEMS Microbiol Lett. 1991;66(2):137–141. doi: 10.1016/0378-1097(91)90322-2
  • Domingo-Calap P, Beamud B, Vienne J, et al. Isolation of four lytic phages infecting Klebsiella pneumoniae K22 clinical isolates from Spain. Int J Mol Sci. 2020;21(2):21. doi: 10.3390/ijms21020425
  • Gorodnichev RB, Volozhantsev NV, Krasilnikova VM, et al. Novel Klebsiella pneumoniae K23-specific bacteriophages from different families: similarity of depolymerases and their therapeutic potential. Front Microbiol. 2021;12:669618. doi: 10.3389/fmicb.2021.669618
  • Eckstein S, Stender J, Mzoughi S, et al. Isolation and characterization of lytic phage TUN1 specific for Klebsiella pneumoniae K64 clinical isolates from Tunisia. BMC Microbiol. 2021;21(1):186. doi: 10.1186/s12866-021-02251-w
  • Kasimova AA, Arbatsky NP, Timoshina OY, et al. The K26 capsular polysaccharide from Acinetobacter baumannii KZ-1098: structure and cleavage by a specific phage depolymerase. Int j biol macromol. 2021;191:182–191. doi: 10.1016/j.ijbiomac.2021.09.073
  • Drobiazko AY, Kasimova AA, Evseev PV, et al. Capsule-targeting depolymerases derived from Acinetobacter baumannii prophage regions. Int J Mol Sci. 2022;23(9):23. doi: 10.3390/ijms23094971
  • Squeglia F, Maciejewska B, Latka A, et al. Structural and functional studies of a Klebsiella phage capsule Depolymerase Tailspike: mechanistic insights into capsular degradation. Structure. 2020;28(6):613–624.e4. doi: 10.1016/j.str.2020.04.015
  • Tu IF, Lin TL, Yang FL, et al. Structural and biological insights into Klebsiella pneumoniae surface polysaccharide degradation by a bacteriophage K1 lyase: implications for clinical use. J Biomed Sci. 2022;29(1):9. doi: 10.1186/s12929-022-00792-4
  • Mushtaq N, Redpath MB, Luzio JP, et al. Treatment of experimental Escherichia coli infection with recombinant bacteriophage-derived capsule depolymerase. J Antimicrob Chemother. 2005;56(1):160–165. doi: 10.1093/jac/dki177
  • Kimura K, Itoh Y. Characterization of poly-γ-glutamate hydrolase encoded by a bacteriophage genome: possible role in phage infection of Bacillus subtilis encapsulated with poly-γ-glutamate. Appl Environ Microbiol. 2003;69(5):2491–2497. doi: 10.1128/AEM.69.5.2491-2497.2003
  • Ely B, Gibbs W, Diez S, et al. The caulobacter crescentus transducing phage Cr30 is a unique member of the T4-like family of myophages. Curr Microbiol. 2015;70(6):854–858. doi: 10.1007/s00284-015-0799-5
  • Yoon BH, Chang HI. Complete genomic sequence of the lactobacillus temperate phage LF1. Arch Virol. 2011;156(10):1909–1912. doi: 10.1007/s00705-011-1082-0
  • Maaroufi H, Levesque RC. Glycoside hydrolase family 32 is present in Bacillus subtilis phages. Virol J. 2015;12(1):157. doi: 10.1186/s12985-015-0373-6
  • Chua J, 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 (Reading). 1999;145(7):1649–1659. doi: 10.1099/13500872-145-7-1649
  • Mushtaq N, Redpath MB, Luzio JP, et al. Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob Agents Chemother. 2004;48(5):1503–1508. doi: 10.1128/AAC.48.5.1503-1508.2004
  • Smith NL, Taylor EJ, Lindsay AM, et al. Structure of a group a streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded β-helix. Proc Natl Acad Sci U S A. 2005;102(49):17652–17657. doi: 10.1073/pnas.0504782102
  • Baker JR, Dong S, Pritchard DG. The hyaluronan lyase of Streptococcus pyogenes bacteriophage H4489A. Biochem J. 2002;365(1):317–322. doi: 10.1042/bj20020149
  • 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
  • Cornelissen A, Ceyssens PJ, T’Syen J, et al. The T7-related Pseudomonas putida phage phi15 displays virion-associated biofilm degradation properties. PLoS One. 2011;6:e18597. doi: 10.1371/journal.pone.0018597
  • Liu Y, Mi Z, Mi L, et al. Identification and characterization of capsule depolymerase Dpo48 from Acinetobacter baumannii phage IME200. PeerJ. 2019;7:e6173. doi: 10.7717/peerj.6173
  • Rice CJ, Kelly SA, O’Brien SC, et al. Novel phage-derived depolymerase with activity against Proteus mirabilis biofilms. Microorganisms. 2021;9(10):2172. doi: 10.3390/microorganisms9102172
  • Wang C, Li P, Zhu Y, et al. Identification of a novel Acinetobacter baumannii phage-derived depolymerase and its therapeutic application in mice. Front Microbiol. 2020;11:1407. doi: 10.3389/fmicb.2020.01407
  • Oliveira H, Pinto G, Mendes B, et al. A tailspike with exopolysaccharide depolymerase activity from a New Providencia stuartii phage makes multidrug-resistant bacteria susceptible to serum-mediated killing. Appl Environ Microbiol. 2020;86(13). doi: 10.1128/AEM.00073-20
  • Oliveira H, Mendes A, Fraga AG, et al. K2 capsule depolymerase is highly stable, is refractory to resistance, and protects larvae and mice from Acinetobacter baumannii sepsis. Appl Environ Microbiol. 2019;85(17). doi: 10.1128/AEM.00934-19
  • Oliveira H, Costa AR, Ferreira A, et al. Functional analysis and antivirulence properties of a New depolymerase from a myovirus that infects Acinetobacter baumannii capsule K45. J Virol. 2019;93(4). doi: 10.1128/JVI.01163-18
  • Pertics BZ, Cox A, Nyul A, et al. Isolation and characterization of a novel lytic bacteriophage against the K2 capsule-Expressing Hypervirulent Klebsiella pneumoniae strain 52145, and Identification of its functional depolymerase. Microorganisms. 2021;9(3):650. doi: 10.3390/microorganisms9030650
  • Hernandez-Morales AC, Lessor LL, Wood TL, et al. Genomic and biochemical characterization of Acinetobacter podophage petty reveals a novel lysis mechanism and tail-associated depolymerase activity. J Virol. 2018;92(6). doi: 10.1128/JVI.01064-17
  • Hsu CR, Lin TL, Pan YJ, et al. Isolation of a bacteriophage specific for a new capsular type of Klebsiella pneumoniae and characterization of its polysaccharide depolymerase. PLoS One. 2013;8(8):e70092. doi: 10.1371/journal.pone.0070092
  • Liu Y, Leung S, Huang Y, et al. Identification of two depolymerases from phage IME205 and their antivirulent functions on K47 capsule of Klebsiella pneumoniae. Front Microbiol. 2020;11:218. doi: 10.3389/fmicb.2020.00218
  • Pan YJ, Lin TL, Chen CC, et al. Klebsiella phage PhiK64-1 encodes multiple depolymerases for multiple host capsular types. J Virol. 2017;91(6):e02457–16. doi: 10.1128/JVI.02457-16
  • Pan YJ, Lin TL, Chen YY, et al. Identification of three podoviruses infecting Klebsiella encoding capsule depolymerases that digest specific capsular types. Microbiol Biotechnol. 2019;12(3):472–486. doi: 10.1111/1751-7915.13370
  • Hsieh PF, Lin HH, Lin TL, et al. Two T7-like Bacteriophages, K5-2 and K5-4, each encodes two capsule depolymerases: isolation and functional characterization. Sci Rep. 2017;7(1):4624. doi: 10.1038/s41598-017-04644-2
  • Broudy TB, Pancholi V, Fischetti VA, et al. Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect Immun. 2001;69(3):1440–1443. doi: 10.1128/IAI.69.3.1440-1443.2001
  • Wong TY, Preston LA, Schiller NL. ALGINATE LYASE: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol. 2000;54(1):289–340. doi: 10.1146/annurev.micro.54.1.289
  • Davidson IW, Lawson CJ, Sutherland IW. An alginate lysate from Azotobacter vinelandii phage. Journal Of General Microbiology. 1977;98(1):223–229. doi: 10.1099/00221287-98-1-223
  • Chen Y, Li X, Wang S, et al. A novel tail-associated O91-specific polysaccharide depolymerase from a podophage reveals lytic efficacy of Shiga toxin-producing Escherichia coli. Appl Environ Microbiol. 2020;86(9). doi: 10.1128/AEM.00145-20
  • Olszak T, Shneider MM, Latka A, et al. The O-specific polysaccharide lyase from the phage LKA1 tailspike reduces Pseudomonas virulence. Sci Rep. 2017;7(1):16302. doi: 10.1038/s41598-017-16411-4
  • Kaszowska M, Majkowska-Skrobek G, Markwitz P, et al. The mutation in wbaP cps gene cluster selected by phage-borne depolymerase abolishes capsule production and diminishes the virulence of Klebsiella pneumoniae. Int J Mol Sci. 2021;22(21):22. doi: 10.3390/ijms222111562
  • Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75(1):39–68. doi: 10.1146/annurev.biochem.75.103004.142545
  • Majkowska-Skrobek G, Latka A, Berisio R, et al. Phage-borne depolymerases decrease Klebsiella pneumoniae resistance to innate defense mechanisms. Front Microbiol. 2018;9:2517. doi: 10.3389/fmicb.2018.02517
  • Guerrero-Bustamante CA, Dedrick RM, Garlena RA, et al. Toward a phage cocktail for tuberculosis: susceptibility and tuberculocidal action of mycobacteriophages against diverse mycobacterium tuberculosis strains. MBio. 2021;12(3):12. doi: 10.1128/mBio.00973-21
  • Li M, Chang R, Lin Y, et al. Phage cocktail powder for Pseudomonas aeruginosa respiratory infections. Int J Pharm. 2021;596:120200. doi: 10.1016/j.ijpharm.2021.120200
  • Mijbel AB, Gatea KS, Al-Bayati MA, et al. A novel phage cocktail therapy of the urinary tract infection in a mouse model. Arch Razi Inst. 2021;76(5):1229–1236. doi: 10.22092/ari.2021.356004.1762
  • Jault P, Leclerc T, Jennes S, et al. Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): a randomised, controlled, double-blind phase 1/2 trial. Lancet Infect Dis. 2019;19(1):35–45. doi: 10.1016/S1473-3099(18)30482-1
  • Sarker SA, Sultana S, Reuteler G, et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBioMedicine. 2016;4:124–137. doi: 10.1016/j.ebiom.2015.12.023
  • Golembo M, Puttagunta S, Rappo U, et al. Development of a topical bacteriophage gel targeting Cutibacterium acnes for acne prone skin and results of a phase 1 cosmetic randomized clinical trial. Skin Health Dis. 2022;2(2):e93. doi: 10.1002/ski2.93
  • 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):729–737. doi: 10.1080/08927014.2010.511196
  • Latka A, Drulis-Kawa Z. Advantages and limitations of microtiter biofilm assays in the model of antibiofilm activity of Klebsiella phage KP34 and its depolymerase. Sci Rep. 2020;10(1):20338. doi: 10.1038/s41598-020-77198-5
  • Luo CH, Hsu YH, Wu WJ, et al. Phage digestion of a bacterial capsule imparts resistance to two antibiotic Agents. Microorganisms. 2021;9(4):794. doi: 10.3390/microorganisms9040794
  • Dunne MW, Aronin SI, Das AF, et al. Sulopenem or ciprofloxacin for the treatment of uncomplicated urinary tract infections in women: a phase 3, randomized trial. Clin Infect Dis. 2023;76(1):66–77. doi: 10.1093/cid/ciac738
  • Chen Y, Sun E, Yang L, et al. Therapeutic application of bacteriophage PHB02 and its putative depolymerase against Pasteurella multocida capsular type a in mice. Front Microbiol. 2018;9:1678. doi: 10.3389/fmicb.2018.01678
  • Mi L, Liu Y, Wang C, et al. Identification of a lytic Pseudomonas aeruginosa phage depolymerase and its anti-biofilm effect and bactericidal contribution to serum. Vir Gen. 2019;55(3):394–405. doi: 10.1007/s11262-019-01660-4
  • Russo A, Gavaruzzi F, Ceccarelli G, et al. Multidrug-resistant Acinetobacter baumannii infections in COVID-19 patients hospitalized in intensive care unit. Infection. 2022;50(1):83–92. doi: 10.1007/s15010-021-01643-4