Bacteriophage endolysins as a response to emerging foodborne pathogens

Trends in Food Science and Technology

Volumn 28, Issue 2, 2012, Pages 103-115

  Oliveira, Hugo ^a   Azeredo, Joana ^a   Lavigne, Rob ^b   Kluskens, Leon D ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b LABORATORY OF GENE TECHNOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC-RESISTANT BACTERIA; FOOD-BORNE PATHOGENS; FUTURE APPLICATIONS; PEPTIDOGLYCANS; SAFETY OF FOOD;

FOOD PRESERVATION; FOOD PRESERVATIVES; FOOD PRODUCTS;

BACTERIOPHAGES;

BACTERIA (MICROORGANISMS);

EID: 84870728247     PISSN: 09242244     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tifs.2012.06.016     Document Type: Review

References (101)

1. Borysowski J., Weber-Dabrowska B., Gorski A. Bacteriophage endolysins as a novel class of antibacterial agents. Experimental Biology Medicine (Maywood) 2006, 231:366-377.
2. Briers Y., Cornelissen A., Aertsen A., Hertveldt K., Michiels C.W., Volckaert G., et al. Analysis of outer membrane permeability of Pseudomonas aeruginosa and bactericidal activity of endolysins KZ144 and EL188 under high hydrostatic pressure. FEMS Microbiology Letters 2008, 280:113-119.
3. Briers Y., Schmelcher M., Loessner M.J., Hendrix J., Engelborghs Y., Volckaert G., et al. The high-affinity peptidoglycan binding domain of Pseudomonas phage endolysin KZ144. Biochemical and Biophysical Research Communications 2009, 383:187-191.
4. Briers Y., Volckaert G., Cornelissen A., Lagaert S., Michiels C.W., Hertveldt K., et al. Muralytic activity and modular structure of the endolysins of Pseudomonas aeruginosa bacteriophages phiKZ and EL. Molecular Microbiology 2007, 65:1334-1344.
5. Briers Y., Volckaert G., Lavigne R. Bacteriophage encoded murein hydrolases. Contemporary trends in bacteriophage research 2009, 119-149. Nova Publishers, New York, (Adams, Ed.). H.T. Adams (Ed.).
6. Callewaert L., Walmagh M., Michiels C.W., Lavigne R. Food applications of bacterial cell wall hydrolases. Current Opinion in Biotechnology 2011, 22:164-171.
7. CDC Retrieved from. http://www.cdc.gov/ncidod/eid/vol5no5/mead.htm.
8. Celia L.K., Nelson D., Kerr D.E. Characterization of a bacteriophage lysin (Ply700) from Streptococcus uberis. Veterinary Microbiology 2008, 130:107-117.
9. Cheng Q., Fischetti V.A. Mutagenesis of a bacteriophage lytic enzyme PlyGBS significantly increases its antibacterial activity against group B streptococci. Applied Microbiology and Biotechnology 2007, 74:1284-1291.
10. Cheng Q., Nelson D., Zhu S., Fischetti V.A. Removal of group B streptococci colonizing the vagina and oropharynx of mice with a bacteriophage lytic enzyme. Antimicrobial Agents and Chemotherapy 2005, 49:111-117.
11. Cornelissen A., Hardies S.C., Shaburova O.V., Krylov V.N., Mattheus W., Kropinski A.M., et al. Complete genome sequence of the giant virus OBP and comparitive genome analysis of the diverse {varphi}KZ-related phages. Journal of Virology 2011, 86:1844-1852.
12. Deloitte FDA food survey on genetically modified foods 2010, Retrieved from. http://www.deloitte.com/assets/Dcom-UnitedStates/Local%2520Assets/Documents/Consumer%2520Business/us_cp_2010FoodSurveyFactSheetGeneticallyModifiedFoods_05022010.pdf.
13. Deutsch S.M., Guezenec S., Piot M., Foster S., Lortal S. Mur-LH, the broad-spectrum endolysin of Lactobacillus helveticus temperate bacteriophage phi-0303. Applied and Environmental Microbiology 2004, 70:96-103.
14. Diaz E., Lopez R., Garcia J.L. Chimeric phage-bacterial enzymes: a clue to the modular evolution of genes. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:8125-8129.
15. Djurkovic S., Loeffler J.M., Fischetti V.A. Synergistic killing of Streptococcus pneumoniae with the bacteriophage lytic enzyme Cpl-1 and penicillin or gentamicin depends on the level of penicillin resistance. Antimicrobial Agents and Chemotherapy 2005, 49:1225-1228.
16. Donovan D.M., Dong S., Garrett W., Rousseau G.M., Moineau S., Pritchard D.G. Peptidoglycan hydrolase fusions maintain their parental specificities. Applied and Environmental Microbiology 2006, 72:2988-2996.
17. Donovan D.M., Foster-Frey J. LambdaSa2 prophage endolysin requires Cpl-7-binding domains and amidase-5 domain for antimicrobial lysis of streptococci. FEMS Microbiology Letters 2008, 287:22-33.
18. Donovan D.M., Lardeo M., Foster-Frey J. Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiology Letters 2006, 265:133-139.
19. During K., Porsch P., Fladung M., Lorz H. Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia carotovora. Plant Journal 1993, 3:587-598.
20. EFSA Retrieved from. http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1211902031795.htm.
21. FDA What you should know about government response to foodborne illness outbreaks 2009, Retrieved from. http://www.fda.gov/downloads/Food/ResourcesForYou/Consumers/UCM180355.pdf.
22. Fernandez-Tornero C., Garcia E., de Pascual-Teresa B., Lopez R., Gimenez-Gallego G., Romero A. Ofloxacin-like antibiotics inhibit pneumococcal cell wall-degrading virulence factors. Journal of Biological Chemistry 2005, 280:19948-19957.
23. Fischetti V.A. Novel method to control pathogenic bacteria on human mucous membranes. Annals of the New York Academy of Sciences 2003, 987:207-214.
24. Fischetti V.A. The use of phage lytic enzymes to control bacterial infections. Bacteriophages: Biology and applications 2004, 321-334. Boca Raton - Florida. E.S. Kutter (Ed.).
25. Fischetti V.A. Bacteriophage lytic enzymes: novel anti-infectives. Trends in Microbiology 2005, 13:491-496.
26. Fischetti V.A. Use of phage lytic enzymes for the treatment and control of bacterial pathogens. Shock 2005, 23:31-32.
27. Fischetti V.A. Bacteriophage lysins as effective antibacterials. Current Opinion in Microbiology 2008, 11:393-400.
28. Fischetti V.A. Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. International Journal of Medical Microbiology 2010, 300:357-362.
29. Fokine A., Miroshnikov K.A., Shneider M.M., Mesyanzhinov V.V., Rossmann M.G. Structure of the bacteriophage phi KZ lytic transglycosylase gp144. Journal of Biological Chemistry 2008, 283:7242-7250.
30. Fujinami Y., Hirai Y., Sakai I., Yoshino M., Yasuda J. Sensitive detection of Bacillus anthracis using a binding protein originating from gamma-phage. Microbiology and Immunology 2007, 51:163-169.
31. Gaeng S., Scherer S., Neve H., Loessner M.J. Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Applied and Environmental Microbiology 2000, 66:2951-2958.
32. Garcia P., Garcia J.L., Garcia E., Sanchez-Puelles J.M., Lopez R. Modular organization of the lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Gene 1990, 86:81-88.
33. Garcia P., Martinez B., Rodriguez L., Rodriguez A. Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. International Journal of Food Microbiology 2010, 141:151-155.
34. Gasson M.J. European patent EP0510907 1992.
35. Hermoso J.A., Garcia J.L., Garcia P. Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Current Opinion in Microbiology 2007, 10:461-472.
36. Hermoso J.A., Monterroso B., Albert A., Galan B., Ahrazem O., Garcia P., et al. Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 2003, 11:1239-1249.
37. Hoopes J.T., Stark C.J., Kim H.A., Sussman D.J., Donovan D.M., Nelson D.C. Use of a bacteriophage lysin, PlyC, as an enzyme disinfectant against Streptococcus equi. Applied and Environmental Microbiology 2009, 75:1388-1394.
38. Horgan M., O'Flynn G., Garry J., Cooney J., Coffey A., Fitzgerald G.F., et al. Phage lysin LysK can be truncated to its CHAP domain and retain lytic activity against live antibiotic-resistant staphylococci. Applied and Environmental Microbiology 2009, 75:872-874.
39. Jado I., Lopez R., Garcia E., Fenoll A., Casal J., Garcia P. Phage lytic enzymes as therapy for antibiotic-resistant Streptococcus pneumoniae infection in a murine sepsis model. Journal of Antimicrobial Chemotherapy 2003, 52:967-973.
40. Kim W.S., Salm H., Geider K. Expression of bacteriophage phiEa1h lysozyme in Escherichia coli and its activity in growth inhibition of Erwinia amylovora. Microbiology 2004, 150:2707-2714.
41. Kretzer J.W., Lehmann R., Schmelcher M., Banz M., Kim K.P., Korn C., et al. Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Applied and Environmental Microbiology 2007, 73:1992-2000.
42. Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nature Reviews Microbiology 2010, 8:317-327.
43. Lai M.J., Lin N.T., Hu A., Soo P.C., Chen L.K., Chen L.H., et al. Antibacterial activity of Acinetobacter baumannii phage varphiAB2 endolysin (LysAB2) against both gram-positive and gram-negative bacteria. Applied Microbiology and Biotechnology 2011, 90:529-539.
44. Lavigne R., Briers Y., Hertveldt K., Robben J., Volckaert G. Identification and characterization of a highly thermostable bacteriophage lysozyme. Cellular and Molecular Life Sciences 2004, 61:2753-2759.
45. Law B.A. The nature of enzymes and their action in foods. Enzymes in food technology 2002, 1-18. Sheffield Academic Press, Sheffield, UK. B.A.L. Robert, J. Whitehurst (Eds.).
46. Liu B., Wu S., Song Q., Zhang X., Xie L. Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Current Microbiology 2006, 53:163-166.
47. Loeffler J.M., Djurkovic S., Fischetti V.A. Phage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia. Infection and Immunity 2003, 71:6199-6204.
48. Loeffler J.M., Fischetti V.A. Synergistic lethal effect of a combination of phage lytic enzymes with different activities on penicillin-sensitive and -resistant Streptococcus pneumoniae strains. Antimicrobial Agents and Chemotherapy 2003, 47:375-377.
49. Loeffler J.M., Nelson D., Fischetti V.A. Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 2001, 294:2170-2172.
50. Loessner M.J. Bacteriophage endolysins - current state of research and applications. Current Opinion in Microbiology 2005, 8:480-487.
51. Loessner M.J., Gaeng S., Scherer S. Evidence for a holin-like protein gene fully embedded out of frame in the endolysin gene of Staphylococcus aureus bacteriophage 187. Journal of Bacteriology 1999, 181:4452-4460.
52. Loessner M.J., Gaeng S., Wendlinger G., Maier S.K., Scherer S. The two-component lysis system of Staphylococcus aureus bacteriophage Twort: a large TTG-start holin and an associated amidase endolysin. FEMS Microbiology Letters 1998, 162:265-274.
53. Loessner M.J., Kramer K., Ebel F., Scherer S. C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Molecular Microbiology 2002, 44:335-349.
54. Loessner M.J., Wendlinger G., Scherer S. Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Molecular Microbiology 1995, 16:1231-1241.
55. Low L.Y., Yang C., Perego M., Osterman A., Liddington R.C. Structure and lytic activity of a Bacillus anthracis prophage endolysin. Journal of Biological Chemistry 2005, 280:35433-35439.
56. Manoharadas S., Witte A., Blasi U. Antimicrobial activity of a chimeric enzybiotic towards Staphylococcus aureus. Journal of Biotechnology 2009, 139:118-123.
57. Masschalck B., Deckers D., Michiels C.W. Lytic and nonlytic mechanism of inactivation of gram-positive bacteria by lysozyme under atmospheric and high hydrostatic pressure. Journal of Food Protection 2002, 65:1916-1923.
58. Masschalck B., Van Houdt R., Van Haver E.G., Michiels C.W. Inactivation of gram-negative bacteria by lysozyme, denatured lysozyme, and lysozyme-derived peptides under high hydrostatic pressure. Applied and Environmental Microbiology 2001, 67:339-344.
59. Matsushita I., Yanase H. A novel thermophilic lysozyme from bacteriophage phiIN93. Biochemical and Biophysical Research Communications 2008, 377:89-92.
60. Matthews B.W., Remington S.J. The three dimensional structure of the lysozyme from bacteriophage T4. Proceedings of the National Academy of Sciences of the United States of America 1974, 71:4178-4182.
61. Mayer M.J., Payne J., Gasson M.J., Narbad A. Genomic sequence and characterization of the virulent bacteriophage phiCTP1 from Clostridium tyrobutyricum and heterologous expression of its endolysin. Applied and Environmental Microbiology 2010, 76:5415-5422.
62. McCullers J.A., Karlstrom A., Iverson A.R., Loeffler J.M., Fischetti V.A. Novel strategy to prevent otitis media caused by colonizing Streptococcus pneumoniae. PLoS Pathogens 2007, 3:e28.
63. Morita M., Tanji Y., Orito Y., Mizoguchi K., Soejima A., Unno H. Functional analysis of antibacterial activity of Bacillus amyloliquefaciens phage endolysin against Gram-negative bacteria. FEBS Letters 2001, 500:56-59.
64. Nakagawa H., Arisaka F., Ishii S. Isolation and characterization of the bacteriophage T4 tail-associated lysozyme. Journal of Virology 1985, 54:460-466.
65. Nakimbugwe D., Masschalck B., Atanassova M., Zewdie-Bosuner A., Michiels C.W. Comparison of bactericidal activity of six lysozymes at atmospheric pressure and under high hydrostatic pressure. International Journal of Food Microbiology 2006, 108:355-363.
66. Navarre W.W., Ton-That H., Faull K.F., Schneewind O. Multiple enzymatic activities of the murein hydrolase from staphylococcal phage phi11. Identification of a d-alanyl-glycine endopeptidase activity. Journal of Biological Chemistry 1999, 274:15847-15856.
67. Nelson D., Loomis L., Fischetti V.A. Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:4107-4112.
68. Nelson D., Schuch R., Chahales P., Zhu S., Fischetti V.A. PlyC: a multimeric bacteriophage lysin. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:10765-10770.
69. Obeso J.M., Martinez B., Rodriguez A., Garcia P. Lytic activity of the recombinant staphylococcal bacteriophage PhiH5 endolysin active against Staphylococcus aureus in milk. International Journal of Food Microbiology 2008, 128:212-218.
70. O'Flaherty S., Coffey A., Meaney W., Fitzgerald G.F., Ross R.P. The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. Journal of Bacteriology 2005, 187:7161-7164.
71. Orito Y., Morita M., Hori K., Unno H., Tanji Y. Bacillus amyloliquefaciens phage endolysin can enhance permeability of Pseudomonas aeruginosa outer membrane and induce cell lysis. Applied Microbiology and Biotechnology 2004, 65:105-109.
72. Perez-Dorado I., Campillo N.E., Monterroso B., Hesek D., Lee M., Paez J.A., et al. Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. Journal of Biological Chemistry 2007, 282:24990-24999.
73. Pritchard D.G., Dong S., Baker J.R., Engler J.A. The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 2004, 150:2079-2087.
74. Pritchard D.G., Dong S., Kirk M.C., Cartee R.T., Baker J.R. LambdaSa1 and LambdaSa2 prophage lysins of Streptococcus agalactiae. Applied and Environmental Microbiology 2007, 73:7150-7154.
75. Rashel M., Uchiyama J., Ujihara T., Uehara Y., Kuramoto S., Sugihara S., et al. Efficient elimination of multidrug-resistant Staphylococcus aureus by cloned lysin derived from bacteriophage phi MR11. Journal of Infectious Diseases 2007, 196:1237-1247.
76. de Ruyter P.G., Kuipers O.P., Meijer W.C., de Vos W.M. Food-grade controlled lysis of Lactococcus lactis for accelerated cheese ripening. Nature Biotechnology 1997, 15:976-979.
77. Sainathrao S., Mohan K.V., Atreya C. Gamma-phage lysin PlyG sequence-based synthetic peptides coupled with Qdot-nanocrystals are useful for developing detection methods for Bacillus anthracis by using its surrogates, B. anthracis-Sterne and B. cereus-4342. BMC Biotechnology 2009, 9:67.
78. Santos S.B., Kropinski A.M., Ceyssens P.J., Ackermann H.W., Villegas A., Lavigne R., et al. Genomic and proteomic characterization of the broad-host-range Salmonella Phage PVP-SE1: creation of a new phage genus. Journal of Virology 2011, 85:11265-11273.
79. Sass P., Bierbaum G. Lytic activity of recombinant bacteriophage phi11 and phi12 endolysins on whole cells and biofilms of Staphylococcus aureus. Applied and Environmental Microbiology 2007, 73:347-352.
80. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., et al. Foodborne illness acquired in the United States - major pathogens. Emerging Infectious Diseases 2011, 17:7-15.
81. Schmelcher M., Shabarova T., Eugster M.R., Eichenseher F., Tchang V.S., Banz M., et al. Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Applied and Environmental Microbiology 2010, 76:5745-5756.
82. Schmelcher M., Waldherr F., Loessner M.J. Listeria bacteriophage peptidoglycan hydrolases feature high thermoresistance and reveal increased activity after divalent metal cation substitution. Applied Microbiology and Biotechnology 2011, 93:633-643.
83. Schuch R., Nelson D., Fischetti V.A. A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 2002, 418:884-889.
84. Shuren J. Federal Register. US food and Drug Administration 2006, Vol. 71:47729-47732. Natl Arch and Records Admin, Washington, DC.
85. Son J.S., Lee S.J., Jun S.Y., Yoon S.J., Kang S.H., Paik H.R., et al. Antibacterial and biofilm removal activity of a podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Applied Microbiology and Biotechnology 2010, 86:1439-1449.
86. Sonstein S.A., Hammel J.M., Bondi A. Staphylococcal bacteriophage-associated lysin: a lytic agent active against Staphylococcus aureus. Journal of Bacteriology 1971, 107:499-504.
87. Tamakoshi M., Murakami A., Sugisawa M., Tsuneizumi K., Takeda S., Saheki T., et al. Genomic and proteomic characterization of the large Myoviridae bacteriophage varphiTMA of the extreme thermophile Thermus thermophilus. Bacteriophage 2011, 1:152-164.
88. Teufer T., Von Jagow C. Which path to go? On how to find a passage for innovations through the jungle of EU-food law - Discussed by the example of bacteriophages 2007, Vol. 3. 136-145.
89. Thomas J.A., Rolando M.R., Carroll C.A., Shen P.S., Belnap D.M., Weintraub S.T., et al. Characterization of Pseudomonas chlororaphis myovirus 201varphi2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 2008, 376:330-338.
90. Vaara M. Agents that increase the permeability of the outer membrane. Microbiological Reviews 1992, 56:395-411.
91. Varzakas T.H., Arvanitoyannis I.S., Baltas H. The politics and science behind GMO acceptance. Critical Reviews in Food Science and Nutrition 2007, 47:335-361.
92. Vasala A., Valkkila M., Caldentey J., Alatossava T. Genetic and biochemical characterization of the Lactobacillus delbrueckii subsp. lactis bacteriophage LL-H lysin. Applied and Environmental Microbiology 1995, 61:4004-4011.
93. Visweswaran G.R., Dijkstra B.W., Kok J. Two major archaeal pseudomurein endoisopeptidases: PeiW and PeiP. Archaea 2010, 2010. 480492.
94. Vollmer W., Joris B., Charlier P., Foster S. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiology Reviews 2008, 32:259-286.
95. Walmagh M., Briers Y., Dos Santos S.B., Azeredo J., Lavigne R. Characterization of modular bacteriophage endolysins from Myoviridae phages OBP, 201varphi2-1 and PVP-SE1. PLoS ONE 2012, 7:e36991.
96. Wang S., Kong J., Zhang X. Identification and characterization of the two-component cell lysis cassette encoded by temperate bacteriophage phiPYB5 of Lactobacillus fermentum. Journal of Applied Microbiology 2008, 105:1939-1944.
97. Wang I.N., Smith D.L., Young R. Holins: the protein clocks of bacteriophage infections. Annual Review of Microbiology 2000, 54:799-825.
98. Yoong P., Schuch R., Nelson D., Fischetti V.A. Identification of a broadly active phage lytic enzyme with lethal activity against antibiotic-resistant Enterococcus faecalis and Enterococcus faecium. Journal of Bacteriology 2004, 186:4808-4812.
99. Yoong P., Schuch R., Nelson D., Fischetti V.A. PlyPH, a bacteriolytic enzyme with a broad pH range of activity and lytic action against Bacillus anthracis. Journal of Bacteriology 2006, 188:2711-2714.
100. Zhang H., Bao H., Billington C., Hudson J.A., Wang R. Isolation and lytic activity of the Listeria bacteriophage endolysin LysZ5 against Listeria monocytogenes in soya milk. Food Microbiology 2012, 31:133-136.
101. Zimmer M., Vukov N., Scherer S., Loessner M.J. The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Applied and Environmental Microbiology 2002, 68:5311-5317.