Bacteriophage Polysaccharide Depolymerases and Biomedical Applications

doi:10.1007/S40259-013-0081-Y

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Bacteriophage Polysaccharide Depolymerases and Biomedical Applications

Journal Article•DOI•

Bacteriophage Polysaccharide Depolymerases and Biomedical Applications

Jianlong Yan¹, Jiaoxiao Mao¹, Jianping Xie¹•Institutions (1)

Southwest University¹

01 Jun 2014-BioDrugs (Springer International Publishing)-Vol. 28, Iss: 3, pp 265-274

TL;DR: 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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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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Journal Article•DOI•

Bacteriophage-encoded depolymerases: their diversity and biotechnological applications

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Diana Priscila Penso Pires¹, Hugo Alexandre Mendes Oliveira¹, Luís Daniel Rodrigues Melo¹, Sanna Sillankorva¹, Joana Azeredo¹ - Show less +1 more•Institutions (1)

University of Minho¹

15 Jan 2016-Applied Microbiology and Biotechnology

TL;DR: This is the first review gathering information about all the depolymerases encoded by fully sequenced phages, which can comprise areas as diverse as medical, chemical, or food-processing industry.

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Abstract: Bacteriophages (phages), natural enemies of bacteria, can encode enzymes able to degrade polymeric substances. These substances can be found in the bacterial cell surface, such as polysaccharides, or are produced by bacteria when they are living in biofilm communities, the most common bacterial lifestyle. Consequently, phages with depolymerase activity have a facilitated access to the host receptors, by degrading the capsular polysaccharides, and are believed to have a better performance against bacterial biofilms, since the degradation of extracellular polymeric substances by depolymerases might facilitate the access of phages to the cells within different biofilm layers. Since the diversity of phage depolymerases is not yet fully explored, this is the first review gathering information about all the depolymerases encoded by fully sequenced phages. Overall, in this study, 160 putative depolymerases, including sialidases, levanases, xylosidases, dextranases, hyaluronidases, peptidases as well as pectate/pectin lyases, were found in 143 phages (43 Myoviridae, 47 Siphoviridae, 37 Podoviridae, and 16 unclassified) infecting 24 genera of bacteria. We further provide information about the main applications of phage depolymerases, which can comprise areas as diverse as medical, chemical, or food-processing industry.

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285 citations

Cites background from "Bacteriophage Polysaccharide Depoly..."

...The presence of depolymerases in phage genomes may act as an adjuvant for phage infection, since they degrade polymers either present in the bacterial surface, such as structural or capsular polysaccharides, or EPSs present in bacterial biofilms (Cornelissen et al. 2011; Yan et al. 2014)....
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...…depolymerases Overall, phages with depolymerase activity have an improved performance against their target bacteria since these enzymes help phages in many important processes such as adsorption, invasion, and disintegration of host bacterial cell as well as biofilm disruption (Yan et al. 2014)....
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...It is believed that phages encoding depolymerases might have a better performance against bacterial biofilms (Hughes et al. 1998b; Yan et al. 2014)....
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...To date, some Azobacter and Pseudomonas spp. phages were found to encode alginate lyases (Bartell et al. 1966; Davidson et al. 1977; Glonti et al. 2010), which help phages to penetrate through the acetylated poly(M)-rich EPSs produced by their bacterial hosts (Wong et al. 2000; Yan et al. 2014)....
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Journal Article•DOI•

Bacteriophages and Biofilms

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David R Harper, Helena M. R. T. Parracho, James T. Walker¹, Richard Sharp, Gavin Hughes, Maria Werthén², Susan M. Lehman, Sandra Morales - Show less +4 more•Institutions (2)

Public Health England¹, University of Gothenburg²

25 Jun 2014-Antibiotics

TL;DR: It is perhaps unsurprising that bacteriophages, as the natural predators of bacteria, have the ability to target this common form of bacterial life.

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Abstract: Biofilms are an extremely common adaptation, allowing bacteria to colonize hostile environments. They present unique problems for antibiotics and biocides, both due to the nature of the extracellular matrix and to the presence within the biofilm of metabolically inactive persister cells. Such chemicals can be highly effective against planktonic bacterial cells, while being essentially ineffective against biofilms. By contrast, bacteriophages seem to have a greater ability to target this common form of bacterial growth. The high numbers of bacteria present within biofilms actually facilitate the action of bacteriophages by allowing rapid and efficient infection of the host and consequent amplification of the bacteriophage. Bacteriophages also have a number of properties that make biofilms susceptible to their action. They are known to produce (or to be able to induce) enzymes that degrade the extracellular matrix. They are also able to infect persister cells, remaining dormant within them, but re-activating when they become metabolically active. Some cultured biofilms also seem better able to support the replication of bacteriophages than comparable planktonic systems. It is perhaps unsurprising that bacteriophages, as the natural predators of bacteria, have the ability to target this common form of bacterial life.

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235 citations

Cites background or methods from "Bacteriophage Polysaccharide Depoly..."

...The presence of such enzymes within the tail seems to be a common feature of bacteriophage infection, noted by Yan et al. [12] as the ―general model of tailed bacteriophage infection‖....
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...While they could theoretically play a role in degrading the biofilm matrix, they are often masked until the tail reconfigures during infection and, thus, have a very localized action [11,12]....
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...Bacteriophage polysaccharide depolymerases have been classified by Yan [12] as endorhamnosidases, alginate lyases, endosialidases and hyaluronidases (glycoside hydrolases)....
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...It is known that many bacteriophage genomes contain genes for enzymes capable of breaking down elements of the biofilm matrix [1,11,12]....
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...[12] further notes that ―polysaccharide depolymerase protein is a common constituent of the tail structure of a bacteriophage‖ and that ―many tailspike proteins have endoglycosidase activity,...
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Journal Article•DOI•

Bacteriophage-encoded virion-associated enzymes to overcome the carbohydrate barriers during the infection process.

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Agnieszka Latka¹, Barbara Maciejewska¹, Grazyna Majkowska-Skrobek¹, Yves Briers², Zuzanna Drulis-Kawa¹ - Show less +1 more•Institutions (2)

University of Wrocław¹, Ghent University²

23 Mar 2017-Applied Microbiology and Biotechnology

TL;DR: The existing diversity in structural locations, variable architectures, enzymatic specificities, and evolutionary aspects of polysaccharide depolymerases and virion-associated lysins (VALs) are discussed and illustrated how these aspects can correlate with the host spectrum.

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Abstract: Bacteriophages are bacterial viruses that infect the host after successful receptor recognition and adsorption to the cell surface. The irreversible adherence followed by genome material ejection into host cell cytoplasm must be preceded by the passage of diverse carbohydrate barriers such as capsule polysaccharides (CPSs), O-polysaccharide chains of lipopolysaccharide (LPS) molecules, extracellular polysaccharides (EPSs) forming biofilm matrix, and peptidoglycan (PG) layers. For that purpose, bacteriophages are equipped with various virion-associated carbohydrate active enzymes, termed polysaccharide depolymerases and lysins, that recognize, bind, and degrade the polysaccharide compounds. We discuss the existing diversity in structural locations, variable architectures, enzymatic specificities, and evolutionary aspects of polysaccharide depolymerases and virion-associated lysins (VALs) and illustrate how these aspects can correlate with the host spectrum. In addition, we present methods that can be used for activity determination and the application potential of these enzymes as antibacterials, antivirulence agents, and diagnostic tools.

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206 citations

Cites background from "Bacteriophage Polysaccharide Depoly..."

...Some reviews dealing with these phage-encoded, virion-associated enzymes have been published recently, particularly focusing on general characteristics and biomedical applications (Drulis-Kawa et al. 2012, 2015; Yan et al. 2014) or on virion-associated peptidoglycan hydrolases (VAPGHs) (Rodríguez-Rubio et al....
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...The Cterminal domain seems to be responsible for protein trimerization and mainly works as an intra-molecular chaperone, while others also assign a function of receptor recognition to this domain (Weigele et al. 2003; Cornelissen et al. 2011; Schwarzer et al. 2012; Yan et al. 2014)....
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...…with these phage-encoded, virion-associated enzymes have been published recently, particularly focusing on general characteristics and biomedical applications (Drulis-Kawa et al. 2012, 2015; Yan et al. 2014) or on virion-associated peptidoglycan hydrolases (VAPGHs) (Rodríguez-Rubio et al. 2013a)....
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...This high stability corresponds to the harsh external conditions these proteins have to withstand in different environments such as the presence of proteases and denaturing conditions (Yan et al. 2014; Majkowska-Skrobek et al. 2016)....
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Journal Article•DOI•

Viruses of prokaryotes: Ackermann, H.W. & Dubow, M.S. 2 vol. (18.5×26 cm), 444 pages. CRC Press. Inc. West Palm Beach, 1987

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J. Rocourt

01 Jul 1988-Annales De L'institut Pasteur. Microbiologie

202 citations

Journal Article•DOI•

Antimicrobial bacteriophage-derived proteins and therapeutic applications.

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Dwayne R. Roach¹, David M. Donovan²•Institutions (2)

Pasteur Institute¹, United States Department of Agriculture²

23 Jun 2015

TL;DR: The current preclinical state of using phage-derived endolysins, virion-associated peptidoglycan hydrolases, polysaccharide depolymerases, and holins for the treatment of bacterial infection is reviewed.

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Abstract: Antibiotics have the remarkable power to control bacterial infections. Unfortunately, widespread use, whether regarded as prudent or not, has favored the emergence and persistence of antibiotic resistant strains of human pathogenic bacteria, resulting in a global health threat. Bacteriophages (phages) are parasites that invade the cells of virtually all known bacteria. Phages reproduce by utilizing the host cell's machinery to replicate viral proteins and genomic material, generally damaging and killing the cell in the process. Thus, phage can be exploited therapeutically as bacteriolytic agents against bacteria. Furthermore, understanding of the molecular processes involved in the viral life cycle, particularly the entry and cell lysis steps, has led to the development of viral proteins as antibacterial agents. Here we review the current preclinical state of using phage-derived endolysins, virion-associated peptidoglycan hydrolases, polysaccharide depolymerases, and holins for the treatment of bacterial infection. The scope of this review is a focus on the viral proteins that have been assessed for protective effects against human pathogenic bacteria in animal models of infection and disease.

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165 citations

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References

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Open Access

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Journal Article•DOI•

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics

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Brandi L. Cantarel¹, Pedro M. Coutinho², Corinne Rancurel², Thomas Bernard², Vincent Lombard², Bernard Henrissat² - Show less +2 more•Institutions (2)

University of Provence¹, Aix-Marseille University²

01 Jan 2009-Nucleic Acids Research

TL;DR: The Carbohydrate-Active Enzyme (CAZy) database is a knowledge-based resource specialized in the enzymes that build and breakdown complex carbohydrates and glycoconjugates and has been used to improve the quality of functional predictions of a number genome projects by providing expert annotation.

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Abstract: The Carbohydrate-Active Enzyme (CAZy) database is a knowledge-based resource specialized in the enzymes that build and breakdown complex carbohydrates and glycoconjugates. As of September 2008, the database describes the present knowledge on 113 glycoside hydrolase, 91 glycosyltransferase, 19 polysaccharide lyase, 15 carbohydrate esterase and 52 carbohydrate-binding module families. These families are created based on experimentally characterized proteins and are populated by sequences from public databases with significant similarity. Protein biochemical information is continuously curated based on the available literature and structural information. Over 6400 proteins have assigned EC numbers and 700 proteins have a PDB structure. The classification (i) reflects the structural features of these enzymes better than their sole substrate specificity, (ii) helps to reveal the evolutionary relationships between these enzymes and (iii) provides a convenient framework to understand mechanistic properties. This resource has been available for over 10 years to the scientific community, contributing to information dissemination and providing a transversal nomenclature to glycobiologists. More recently, this resource has been used to improve the quality of functional predictions of a number genome projects by providing expert annotation. The CAZy resource resides at URL: http://www.cazy.org/.

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6,028 citations

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J. Virol. Methods: Corrigendum to “Detection of stylet-borne and circulative potato viruses in aphids by duplex reverse transcription polymerase chain reaction” [59 (1996) 189]

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"Bacteriophage Polysaccharide Depoly..." refers background in this paper

...Bradley groups A, B, and C, respectively [9, 10]....
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Journal Article•DOI•

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Jukka Finne¹, Maija Leinonen¹, P. Helena Mäkelä¹•Institutions (1)

University of Helsinki¹

13 Aug 1983-The Lancet

TL;DR: Glycopeptides containing polysialic acid units were isolated from human and rat brain and tested for reactivity with antibodies against meningococcal capsules.

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Journal Article•DOI•

Dispersing biofilms with engineered enzymatic bacteriophage

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Timothy K. Lu¹, James J. Collins•Institutions (1)

Massachusetts Institute of Technology¹

03 Jul 2007-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: This work demonstrates the feasibility and benefits of using engineered enzymatic bacteriophage to reduce bacterial biofilms and the applicability of synthetic biology to an important medical and industrial problem.

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Abstract: Synthetic biology involves the engineering of biological organisms by using modular and generalizable designs with the ultimate goal of developing useful solutions to real-world problems. One such problem involves bacterial biofilms, which are crucial in the pathogenesis of many clinically important infections and are difficult to eradicate because they exhibit resistance to antimicrobial treatments and removal by host immune systems. To address this issue, we engineered bacteriophage to express a biofilm-degrading enzyme during infection to simultaneously attack the bacterial cells in the biofilm and the biofilm matrix, which is composed of extracellular polymeric substances. We show that the efficacy of biofilm removal by this two-pronged enzymatic bacteriophage strategy is significantly greater than that of nonenzymatic bacteriophage treatment. Our engineered enzymatic phage substantially reduced bacterial biofilm cell counts by ≈4.5 orders of magnitude (≈99.997% removal), which was about two orders of magnitude better than that of nonenzymatic phage. This work demonstrates the feasibility and benefits of using engineered enzymatic bacteriophage to reduce bacterial biofilms and the applicability of synthetic biology to an important medical and industrial problem.

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767 citations