Prophage lysin Ply30 protects mice from Streptococcus suis and Streptococcus equi subsp. zooepidemicus infections

Applied and Environmental Microbiology

Volumn 81, Issue 21, 2015, Pages 7377-7384

  Tang, Fang ^a   Li, Dezhi ^a   Wang, Haojin ^a   Ma, Zhe ^a   Lu, Chengping ^a   Dai, Jianjun ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOPHAGES; CELL DEATH;

ANTIBIOTIC RESISTANCE; BACTERIAL INFECTIONS; BACTERIAL LOAD; HIGH ACTIVITY; LYSOSOMAL ENZYMES; OPTIMAL CONCENTRATION; PATHOGENIC BACTERIUM; ZOOEPIDEMICUS;

MAMMALS;

ANTIMICROBIAL ACTIVITY; BACTERIOPHAGE; BACTERIUM; BLOOD; CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; GENE EXPRESSION; INFECTIVITY; MICROBIAL ACTIVITY; PATHOGEN; PH; RODENT;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS; STREPTOCOCCUS EQUI SUBSP. ZOOEPIDEMICUS; STREPTOCOCCUS SUIS; SUIDAE;

ANTIINFECTIVE AGENT; ENDOLYSIN; PROTEINASE;

ANIMAL; ANIMAL STRUCTURES; BACTERIAL COUNT; BACTERIOLYSIS; BLOOD; DISEASE MODEL; DRUG EFFECTS; ENZYME STABILITY; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MICROBIOLOGY; MOUSE; PH; PHYSIOLOGY; PROPHAGE; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS EQUI; STREPTOCOCCUS SUIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ANIMAL STRUCTURES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOLYSIS; BLOOD; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; ENZYME STABILITY; HYDROGEN-ION CONCENTRATION; MICE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; PROPHAGES; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS EQUI; STREPTOCOCCUS SUIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84944396611     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02300-15     Document Type: Article

References (49)

1. Gruszynski K, Young A, Levine SJ, Garvin JP, Brown S, Turner L, Fritzinger A, Gertz RE, Jr, Murphy JM, Vogt M, Beall B. 2015. Streptococcus equi subsp. zooepidemicus infections associated with guinea pigs. Emerg Infect Dis 21:156-158. http://dx.doi.org/10.3201/eid2101.140640.
2. Fulde M, Valentin-Weigand P. 2013. Epidemiology and pathogenicity of zoonotic streptococci. Curr Top Microbiol Immunol 368:49-81. http://dx.doi.org/10.1007/82_2012_277.
3. Devriese LA, Cruz Colque JI, De Herdt P, Haesebrouck F. 1992. Identification and composition of the tonsillar and anal enterococcal and streptococcal flora of dogs and cats. J Appl Bacteriol 73:421-425. http://dx.doi.org/10.1111/j.1365-2672.1992.tb04998.x.
4. Staats JJ, Feder I, Okwumabua O, Chengappa MM. 1997. Streptococcus suis: past and present. Vet Res Commun 21:381-407. http://dx.doi.org/10.1023/A:1005870317757.
5. Liu Z, Zheng H, Gottschalk M, Bai X, Lan R, Ji S, Liu H, Xu J. 2013. Development of multiplex PCR assays for the identification of the 33 serotypes of Streptococcus suis. PLoS One 8:e72070. http://dx.doi.org/10.1371/journal.pone.0072070.
6. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ. 2007. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7:201-209. http://dx.doi.org/10.1016/S1473-3099(07)70001-4.
7. Harel J, Martinez G, Nassar A, Dezfulian H, Labrie SJ, Brousseau R, Moineau S, Gottschalk M. 2003. Identification of an inducible bacteriophage in a virulent strain of Streptococcus suis serotype 2. Infect Immun 71:6104-6108. http://dx.doi.org/10.1128/IAI.71.10.6104-6108.2003.
8. Hu P, Yang M, Zhang A, Wu J, Chen B, Hua Y, Yu J, Xiao J, Jin M. 2011. Complete genome sequence of Streptococcus suis serotype 14 strain JS14. J Bacteriol 193:2375-2376. http://dx.doi.org/10.1128/JB.00083-11.
9. Hu X, Zhu F, Wang H, Chen S, Wang G, Sun J, Hua C, Yang H. 2000. Studies on human streptococcal infectious syndrome caused by infected pigs. Zhonghua Yu Fang Yi Xue Za Zhi 34:150-152.
10. Huong VT, Ha N, Huy NT, Horby P, Nghia HD, Thiem VD, Zhu X, Hoa NT, Hien TT, Zamora J, Schultsz C, Wertheim HF, Hirayama K. 2014. Epidemiology, clinical manifestations, and outcomes of Streptococcus suis infection in humans. Emerg Infect Dis 20:1105-1114. http://dx.doi.org/10.3201/eid2007.131594.
11. Lindahl SB, Aspan A, Baverud V, Paillot R, Pringle J, Rash NL, Soderlund R, Waller AS. 2013. Outbreak of upper respiratory disease in horses caused by Streptococcus equi subsp. zooepidemicus ST-24. Vet Microbiol 166:281-285. http://dx.doi.org/10.1016/j.vetmic.2013.05.006.
12. Pelkonen S, Lindahl SB, Suomala P, Karhukorpi J, Vuorinen S, Koivula I, Vaisanen T, Pentikainen J, Autio T, Tuuminen T. 2013. Transmission of Streptococcus equi subspecies zooepidemicus infection from horses to humans. Emerg Infect Dis 19:1041-1048. http://dx.doi.org/10.3201/eid1907.121365.
13. Holden MT, Heather Z, Paillot R, Steward KF, Webb K, Ainslie F, Jourdan T, Bason NC, Holroyd NE, Mungall K, Quail MA, Sanders M, Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley KA, Maiden MC, Kehoe M, Chanter N, Bentley SD, Robinson C, Maskell DJ, Parkhill J, Waller AS. 2009. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 5:e1000346. http://dx.doi.org/10.1371/journal.ppat.1000346.
14. Bordes-Benitez A, Sanchez-Onoro M, Suarez-Bordon P, GarciaRojas AJ, Saez-Nieto JA, Gonzalez-Garcia A, Alamo-Antunez I, Sanchez-Maroto A, Bolanos-Rivero M. 2006. Outbreak of Streptococcus equi subsp. zooepidemicus infections on the island of Gran Canaria associated with the consumption of inadequately pasteurized cheese. Eur J Clin Microbiol Infect Dis 25:242-246. http://dx.doi.org/10.1007/s10096-006-0119-x.
15. Blum S, Elad D, Zukin N, Lysnyansky I, Weisblith L, Perl S, Netanel O, David D. 2010. Outbreak of Streptococcus equi subsp. zooepidemicus infections in cats. Vet Microbiol 144:236-239. http://dx.doi.org/10.1016/j.vetmic.2009.12.040.
16. Wisselink HJ, Veldman KT, Van den Eede C, Salmon SA, Mevius DJ. 2006. Quantitative susceptibility of Streptococcus suis strains isolated from diseased pigs in seven European countries to antimicrobial agents licensed in veterinary medicine. Vet Microbiol 113:73-82. http://dx.doi.org/10.1016/j.vetmic.2005.10.035.
17. Hendriksen RS, Mevius DJ, Schroeter A, Teale C, Jouy E, Butaye P, Franco A, Utinane A, Amado A, Moreno M, Greko C, Stark KD, Berghold C, Myllyniemi AL, Hoszowski A, Sunde M, Aarestrup FM. 2008. Occurrence of antimicrobial resistance among bacterial pathogens and indicator bacteria in pigs in different European countries from year 2002-2004: the ARBAO-II study. Acta Vet Scand 50:19. http://dx.doi.org/10.1186/1751-0147-50-19.
18. Palmieri C, Varaldo PE, Facinelli B. 2011. Streptococcus suis, an emerging drug-resistant animal and human pathogen. Front Microbiol 2:235. http://dx.doi.org/10.3389/fmicb.2011.00235.
19. Chalker VJ, Waller A, Webb K, Spearing E, Crosse P, Brownlie J, Erles K. 2012. Genetic diversity of Streptococcus equi subsp. zooepidemicus and doxycycline resistance in kennelled dogs. J Clin Microbiol 50:2134-2136. http://dx.doi.org/10.1128/JCM.00719-12.
20. Reardon S. 2014. Phage therapy gets revitalized. Nature 510:15-16. http://dx.doi.org/10.1038/510015a.
21. Qadir MI. 2015. Review: phage therapy: a modern tool to control bacterial infections. Pak J Pharm Sci 28:265-270.
22. Nilsson AS. 2014. Phage therapy-constraints and possibilities. Ups J Med Sci 119:192-198. http://dx.doi.org/10.3109/03009734.2014.902878.
23. Ma YL, Lu CP. 2008. Isolation and identification of a bacteriophage capable of infecting Streptococcus suis type 2 strains. Vet Microbiol 132: 340-347. http://dx.doi.org/10.1016/j.vetmic.2008.05.013.
24. Gilmer DB, Schmitz JE, Euler CW, Fischetti VA. 2013. Novel bacteriophage lysin with broad lytic activity protects against mixed infection by Streptococcus pyogenes and methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 57:2743-2750. http://dx.doi.org/10.1128/AAC.02526-12.
25. Gu J, Xu W, Lei L, Huang J, Feng X, Sun C, Du C, Zuo J, Li Y, Du T, Li L, Han W. 2011. LysGH15, a novel bacteriophage lysin, protects a murine bacteremia model efficiently against lethal methicillin-resistant Staphylococcus aureus infection. J Clin Microbiol 49:111-117. http://dx.doi.org/10.1128/JCM.01144-10.
26. Wang Y, Sun JH, Lu CP. 2009. Purified recombinant phage lysin LySMP: an extensive spectrum of lytic activity for swine streptococci. Curr Microbiol 58:609-615. http://dx.doi.org/10.1007/s00284-009-9379-x.
27. Schmitz JE. 2011. Expanding the horizons of enzybiotic identification. Ph.D. thesis. Rockefeller University, New York, NY.
28. Tang F, Bossers A, Harders F, Lu C, Smith H. 2013. Comparative genomic analysis of twelve Streptococcus suis (pro)phages. Genomics 101: 336-344. http://dx.doi.org/10.1016/j.ygeno.2013.04.005.
29. LaVallie ER, DiBlasio EA, Kovacic S, Grant KL, Schendel PF, McCoy JM. 1993. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (N Y) 11:187-193. http://dx.doi.org/10.1038/nbt0293-187.
30. Oechslin F, Daraspe J, Giddey M, Moreillon P, Resch G. 2013. In vitro characterization of PlySK1249, a novel phage lysin, and assessment of its antibacterial activity in a mouse model of Streptococcus agalactiae bacteremia. Antimicrob Agents Chemother 57:6276-6283. http://dx.doi.org/10.1128/AAC.01701-13.
31. Lood R, Raz A, Molina H, Euler CW, Fischetti VA. 2014. A highly active and negatively charged Streptococcus pyogenes lysin with a rare D-alanyl-Lalanine endopeptidase activity protects mice against streptococcal bacteremia. Antimicrob Agents Chemother58:3073-3084. http://dx.doi.org/10.1128/AAC.00115-14.
32. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 2014. Pfam: the protein families database. Nucleic Acids Res 42:D222-D230. http://dx.doi.org/10.1093/nar/gkt1223.
33. Pan Z, Ma J, Dong W, Song W, Wang K, Lu C, Yao H. 2015. Novel variant serotype of Streptococcus suis isolated from piglets with meningitis. Appl Environ Microbiol 81:976-985. http://dx.doi.org/10.1128/AEM.02962-14.
34. Nelson DC, Schmelcher M, Rodriguez-Rubio L, Klumpp J, Pritchard DG, Dong S, Donovan DM. 2012. Endolysins as antimicrobials. Adv Virus Res 83:299-365. http://dx.doi.org/10.1016/B978-0-12-394438-2.00007-4.
35. Schmelcher M, Donovan DM, Loessner MJ. 2012. Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7:1147-1171. http://dx.doi.org/10.2217/fmb.12.97.
36. Herpers B. 2015. Endolysins: redefining antibacterial therapy. Future Microbiol 10:309-311. http://dx.doi.org/10.2217/fmb.14.142.
37. Tang F, Zhang W, Lu C. 2013. Lysogenic Streptococcus suis isolate SS2-4 containing prophage SMP showed increased mortality in zebra fish compared to the wild-type isolate. PLoS One 8:e54227. http://dx.doi.org/10.1371/journal.pone.0054227.
38. Mishra AK, Rawat M, Viswas KN, Abhishek Kumar S, Reddy M. 2013. Expression and lytic efficacy assessment of the Staphylococcus aureus phage SA4 lysin gene. J Vet Sci 14:37-43. http://dx.doi.org/10.4142/jvs.2013.14.1.37.
39. Diez-Martinez R, De Paz HD, Garcia-Fernandez E, Bustamante N, Euler CW, Fischetti VA, Menendez M, Garcia P. 2015. A novel chimeric phage lysin with high in vitro and in vivo bactericidal activity against Streptococcus pneumoniae. J Antimicrob Chemother 70:1763-1773. http://dx.doi.org/10.1093/jac/dkv038.
40. Pastagia M, Euler C, Chahales P, Fuentes-Duculan J, Krueger JG, Fischetti VA. 2011. A novel chimeric lysin shows superiority to mupirocin for skin decolonization of methicillin-resistant and-sensitive Staphylococcus aureus strains. Antimicrob Agents Chemother 55:738-744. http://dx.doi.org/10.1128/AAC.00890-10.
41. Hoopes JT, Stark CJ, Kim HA, Sussman DJ, Donovan DM, Nelson DC. 2009. Use of a bacteriophage lysin, PlyC, as an enzyme disinfectant against Streptococcus equi. Appl Environ Microbiol 75:1388-1394. http://dx.doi.org/10.1128/AEM.02195-08.
42. Yao HC, Chen G, Lu CP. 1999. Identification of isolates of S. suis in Jiangsu Province during 1998. J Nanjing Agric Univ 22:67-70.
43. Ma Z, Geng J, Yi L, Xu B, Jia R, Li Y, Meng Q, Fan H, Hu S. 2013. Insight into the specific virulence related genes and toxin-antitoxin virulent pathogenicity islands in swine streptococcosis pathogen Streptococcus equi ssp. zooepidemicus strain ATCC35246. BMC Genomics 14:377. http://dx.doi.org/10.1186/1471-2164-14-377.
44. Zhao Z, Wang J, Liu P, Zhang S, Gong J, Huang X, Li B, Xue F. 2009. Cultivation, LD(50) determination and experimental model of Streptococcus suis serotype 2 strain HA9801. Res Vet Sci 86:200-205. http://dx.doi.org/10.1016/j.rvsc.2008.07.012.
45. Loessner MJ. 2005. Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol 8:480-487. http://dx.doi.org/10.1016/j.mib.2005.06.002.
46. Loessner MJ, Wendlinger G, Scherer S. 1995. Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol Microbiol 16:1231-1241. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02345.x.
47. Hermoso JA, Monterroso B, Albert A, Galan B, Ahrazem O, Garcia P, Martinez-Ripoll M, Garcia JL, Menendez M. 2003. Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure11:1239-1249. http://dx.doi.org/10.1016/j.str.2003.09.005.
48. Becker SC, Foster-Frey J, Stodola AJ, Anacker D, Donovan DM. 2009. Differentially conserved staphylococcal SH3b_5 cell wall binding domains confer increased staphylolytic and streptolytic activity to a streptococcal prophage endolysin domain. Gene 443:32-41. http://dx.doi.org/10.1016/j.gene.2009.04.023.
49. Porter CJ, Schuch R, Pelzek AJ, Buckle AM, McGowan S, Wilce MC, Rossjohn J, Russell R, Nelson D, Fischetti VA, Whisstock JC. 2007. The 1.6 A crystal structure of the catalytic domain of PlyB, a bacteriophage lysin active against Bacillus anthracis. J Mol Biol 366:540-550. http://dx.doi.org/10.1016/j.jmb.2006.11.056.