Synergistic streptococcal phage λSA2 and B30 endolysins kill streptococci in cow milk and in a mouse model of mastitis

Applied Microbiology and Biotechnology

Volumn 99, Issue 20, 2015, Pages 8475-8486

  Schmelcher, Mathias ^a,b   Powell, Anne M ^a   Camp, Mary J ^a   Pohl, Calvin S ^a,c   Donovan, David M ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b ETH ZURICH   (Switzerland)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Antimicrobial; Bacteriophage; Endolysin; Mastitis; Peptidoglycan hydrolase; Streptococcus

Indexed keywords

ANTIBIOTICS; BACTERIOPHAGES; DISEASES; ENZYMES; IONIC STRENGTH;

ANTIMICROBIAL; ENDOLYSIN; MASTITIS; PEPTIDOGLYCAN HYDROLASE; STREPTOCOCCUS;

MAMMALS;

ANTIBIOTIC AGENT; HYDROLASE; LYSOSTAPHIN; STREPTOCOCCAL PHAGE B30 ENDOLYSIN; STREPTOCOCCUS PHAGE DELTA SA2 ENDOLYSIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CALCIUM; ENDOLYSIN; PROTEINASE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOTECHNOLOGY; CATTLE; DISEASE VECTOR; ENZYME ACTIVITY; MILK; RODENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERICIDAL ACTIVITY; BOVINE MASTITIS; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; IN VITRO STUDY; INTRAMAMMARY DRUG ADMINISTRATION; MILK; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STREPTOCOCCAL PHAGE B30; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS PHAGE; STREPTOCOCCUS UBERIS; ANIMAL; BACTERIAL LOAD; BOVINE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; HUMAN; ISOLATION AND PURIFICATION; MAMMARY GLAND; MASTITIS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; OSMOLARITY; PH; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS; TREATMENT OUTCOME;

UNITED STATES;

BOVINAE; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS UBERIS;

ANIMALS; BACTERIAL LOAD; CALCIUM; CATTLE; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; ENDOPEPTIDASES; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; MAMMARY GLANDS, HUMAN; MASTITIS; MICE; MICROBIAL VIABILITY; MILK; OSMOLAR CONCENTRATION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS; STREPTOCOCCUS PHAGES; TREATMENT OUTCOME;

EID: 84941994476     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6579-0     Document Type: Article

References (70)

1. Anderson JC, Craven N (1984) Assessment in the mouse of cefoperazone as a treatment for mastitis. Vet Rec 114:607–612
2. Apparao MD, Ruegg PL, Lago A, Godden S, Bey R, Leslie K (2009) Relationship between in vitro susceptibility test results and treatment outcomes for gram-positive mastitis pathogens following treatment with cephapirin sodium. J Dairy Sci 92:2589–2597. doi:10.3168/jds.2008-1693
3. Bateman A, Rawlings ND (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends BiochemSci 28:234–237
4. Becker SC, Foster-Frey J, Donovan DM (2008) The phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol Lett 287:185–191
5. 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
6. Blowey RW, Edmondson P (2010) Mastitis control in dairy herds. CABI, Cambridge
7. Borysowski J, Weber-Dabrowska B, Gorski A (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med(Maywood) 231:366–377
8. Bramley AJ, Foster R (1990) Effects of lysostaphin on Staphylococcus aureus infections of the mouse mammary gland. Res Vet Sci 49:120–121
9. Brouillette E, Malouin F (2005) The pathogenesis and control of Staphylococcus aureus-induced mastitis: study models in the mouse. Microbes Infect 7:560–568
10. Brouillette E, Grondin G, Lefebvre C, Talbot BG, Malouin F (2004) Mouse mastitis model of infection for antimicrobial compound efficacy studies against intracellular and extracellular forms of Staphylococcus aureus. Vet Microbiol 101:253–262
11. Calvinho LF, Almeida RA, Oliver SP (1998) Potential virulence factors of Streptococcus dysgalactiae associated with bovine mastitis. Vet Microbiol 61:93–110
12. Cattell MB, Dinsmore RP, Belschner AP, Carmen J, Goodell G (2001) Environmental gram-positive mastitis treatment: in vitro sensitivity and bacteriologic cure. J Dairy Sci 84:2036–2043
13. Celia LK, Nelson D, Kerr DE (2008) Characterization of a bacteriophage lysin (Ply700) from Streptococcus uberis. Vet Microbiol 130:107–117
14. Chandler RL (1970a) Experimental bacterial mastitis in the mouse. J Med Microbiol 3:273–282
15. Chandler RL (1970b) Ultrastructural pathology of mastitis in the mouse. A study of experimental staphylococcal and streptococcal infections. Br J Exp Pathol 51:639–645
16. Chandler RL (1971) Studies on experimental mouse mastitis relative to the assessment of pharmaceutical substances. J Comp Pathol 81:507–514
17. Deluyker HA, Van Oye SN, Boucher JF (2005) Factors affecting cure and somatic cell count after pirlimycin treatment of subclinical mastitis in lactating cows. J Dairy Sci 88:604–614
18. Demon D, Ludwig C, Breyne K, Guede D, Dorner JC, Froyman R, Meyer E (2012) The intramammary efficacy of first generation cephalosporins against Staphylococcus aureus mastitis in mice. Vet Microbiol 160:141–150. doi:10.1016/j.vetmic.2012.05.017
19. Demon D, Breyne K, Schiffer G, Meyer E (2013) Short communication: Antimicrobial efficacy of intramammary treatment with a novel biphenomycin compound against Staphylococcus aureus, Streptococcus uberis, and Escherichia coli-induced mouse mastitis. J Dairy Sci 96:7082–7087. doi:10.3168/jds.2013-7011
20. Diarra MS, Petitclerc D, Deschenes E, Lessard N, Grondin G, Talbot BG, Lacasse P (2003) Lactoferrin against Staphylococcus aureus mastitis. Lactoferrin alone or in combination with penicillin G on bovine polymorphonuclear function and mammary epithelial cells colonisation by Staphylococcus aureus. Vet Immunol and Immunopathol 95:33–42
21. Donovan DM (2007) Bacteriophage and peptidoglycan degrading enzymes with antimicrobial applications. Recent Pat Biotechnol 1:113–122
22. Donovan DM, Foster-Frey J (2008) LambdaSa2 prophage endolysin requires Cpl-7-binding domains and amidase-5 domain for antimicrobial lysis of streptococci. FEMS Microbiol Lett 287:22–33
23. Donovan DM, Dong S, Garrett W, Rousseau GM, Moineau S, Pritchard DG (2006a) Peptidoglycan hydrolase fusions maintain their parental specificities. Appl Environ Microbiol 72:2988–2996
24. Donovan DM, Foster-Frey J, Dong S, Rousseau GM, Moineau S, Pritchard DG (2006b) The cell lysis activity of the Streptococcus agalactiae bacteriophage B30 endolysin relies on the cysteine, histidine-dependent amidohydrolase/peptidase domain. Appl Environ Microbiol 72:5108–5112
25. Donovan DM, Lardeo M, Foster-Frey J (2006c) Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiol Lett 265:133–139
26. Donovan DM, Becker SC, Dong S, Baker JR, Foster-Frey J, Pritchard DG (2009) Peptidoglycan hydrolase enzyme fusions for treating multi-drug resistant pathogens. Biotech International 21:6–10
27. Fischetti VA (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13:491–496
28. Gao J, Yu FQ, Luo LP, He JZ, Hou RG, Zhang HQ, Li SM, Su JL, Han B (2012) Antibiotic resistance of Streptococcus agalactiae from cows with mastitis. Vet J 194:423–424. doi:10.1016/j.tvjl.2012.04.020
29. Garcia P, Garcia JL, Garcia E, Sanchez-Puelles JM, Lopez R (1990) Modular organization of the lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Gene 86:81–88
30. Gaucheron F (2005) The minerals of milk. Reprod Nutr Dev 45:473–483. doi:10.1051/rnd:2005030
31. Gehring R, Smith GW (2006) An overview of factors affecting the disposition of intramammary preparations used to treat bovine mastitis. J Vet Pharmacol Ther 29:237–241
32. 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. doi:10.1128/AAC.02526-12
33. Gruet P, Maincent P, Berthelot X, Kaltsatos V (2001) Bovine mastitis and intramammary drug delivery: review and perspectives. Adv Drug Deliv Rev 50:245–259
34. Hermoso JA, Garcia JL, Garcia P (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol 10:461–472
35. Kerr DE, Plaut K, Bramley AJ, Williamson CM, Lax AJ, Moore K, Wells KD, Wall RJ (2001) Lysostaphin expression in mammary glands confers protection against staphylococcal infection in transgenic mice. Nat Biotechnol 19:66–70
36. Kuang Y, Jia H, Miyanaga K, Tanji Y (2009) Effect of milk on antibacterial activity of tetracycline against Escherichia coli and Staphylococcus aureus isolated from bovine mastitis. Appl Microbiol Biotechnol 84:135–142
37. Lammers A, van Vorstenbosch CJ, Erkens JH, Smith HE (2001) The major bovine mastitis pathogens have different cell tropisms in cultures of bovine mammary gland cells. Vet Microbiol 80:255–265
38. Leigh JA (1999) Streptococcus uberis: a permanent barrier to the control of bovine mastitis? Vet J 157:225–238. doi:10.1053/tvjl.1998.0298
39. Lewis RE, Diekema DJ, Messer SA, Pfaller MA, Klepser ME (2002) Comparison of Etest, chequerboard dilution and time-kill studies for the detection of synergy or antagonism between antifungal agents tested against Candida species. J Antimicrob Chemother 49:345–351
40. Loeffler JM, Fischetti VA (2003) Synergistic lethal effect of a combination of phage lytic enzymes with different activities on penicillin-sensitive and -resistant Streptococcus pneumoniae strains. Antimicrob Agents Chemother 47:375–377
41. Loeffler JM, Nelson D, Fischetti VA (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294:2170–2172
42. Lonnerdal B, Keen CL, Hurley LS (1981) Iron, copper, zinc, and manganese in milk. Annu Rev Nutr 1:149–174. doi:10.1146/annurev.nu.01.070181.001053
43. Lopez R, Garcia E (2004) Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol Rev 28:553–580
44. Notebaert S, Meyer E (2006) Mouse models to study the pathogenesis and control of bovine mastitis. A review. Vet Q 28:2–13
45. Obeso JM, Martinez B, Rodriguez A, Garcia P (2008) Lytic activity of the recombinant staphylococcal bacteriophage PhiH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128:212–218
46. Odds FC (2003) Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52:1. doi:10.1093/jac/dkg301
47. O’Flaherty S, Coffey A, Meaney WJ, Fitzgerald GF, Ross RP (2005) Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Lett Appl Microbiol 41:274–279
48. 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. doi:10.1128/AAC.00890-10
49. Ponting CP, Aravind L, Schultz J, Bork P, Koonin EV (1999) Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol 289:729–745
50. Pritchard DG, Dong S, Baker JR, Engler JA (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactieae bacteriophage B30. Microbiology 150:2079–2087
51. Pritchard DG, Dong S, Kirk MC, Cartee RT, Baker JR (2007) LambdaSa1 and LambdaSa2 prophage lysins of Streptococcus agalactiae. Appl Environ Microbiol 73:7150–7154
52. Pyörälä S (2009) Treatment of mastitis during lactation. Ir Vet J 62(Suppl 4):S40–S44. doi:10.1186/2046-0481-62-S4-S40
53. Reichelt P, Schwarz C, Donzeau M (2006) Single step protocol to purify recombinant proteins with low endotoxin contents. Protein Expr Purif 46:483–488
54. Rowson AD, Wang YQ, Aalseth E, Forsberg NE, Puntenney SB (2011) Effects of an immunomodulatory feed additive on the development of mastitis in a mouse infection model using four bovine-origin isolates. Animal 5(2):220–229. doi:10.1017/S1751731110001850
55. Sanchez MS, Ford CW, Yancey RJ Jr (1994) Effect of tumor necrosis factor-alpha, interleukin-1 beta, and antibiotics on the killing of intracellular Staphylococcus aureus. J Dairy Sci 77:1251–1258
56. Schindler CA, Schuhardt VT (1964) Lysostaphin: a new bacteriolytic agent for the Staphylococcus. Proc Natl Acad Sci U S A 51:414–421
57. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477
58. Schmelcher M, Shabarova T, Eugster MR, Eichenseher F, Tchang VS, Banz M, Loessner MJ (2010) Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl Environ Microbiol 76:5745–5756
59. Schmelcher M, Donovan DM, Loessner MJ (2012a) Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7:1147–1171. doi:10.2217/fmb.12.97
60. Schmelcher M, Powell AM, Becker SC, Camp MJ, Donovan DM (2012b) Chimeric phage lysins act synergistically with lysostaphin to kill mastitis-causing Staphylococcus aureus in murine mammary glands. Appl Environ Microbiol 78:2297–2305. doi:10.1128/AEM.07050-11
61. Schuch R, Nelson D, Fischetti VA (2002) A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418:884–889
62. Sordillo LM, Streicher KL (2002) Mammary gland immunity and mastitis susceptibility. J Mammary Gland Biol Neoplasia 7:135–146
63. Tenhagen BA, Koster G, Wallmann J, Heuwieser W (2006) Prevalence of mastitis pathogens and their resistance against antimicrobial agents in dairy cows in Brandenburg, Germany. J Dairy Sci 89:2542–2551. doi:10.3168/jds.S0022-0302(06)72330-X
64. Wall RJ, Powell A, Paape MJ, Kerr DE, Bannerman DD, Pursel VG, Wells KD, Talbot N, Hawk HW (2005) Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat Biotechnol 23:445–451
65. Wall R, Powell A, Sohn E, Foster-Frey J, Bannerman D, Paape M (2009) Enhanced host immune recognition of mastitis causing Escherchia coli in CD-14 transgenic mice. Anim Biotechnol 20:1–14
66. Walsh C (2003) Where will new antibiotics come from? Nat Rev Microbiol 1:65–70
67. Webb BH, Johnson AH, Alford JA (1974) Fundamentals of dairy chemistry. AVI, Westport
68. Whisstock JC, Lesk AM (1999) SH3 domains in prokaryotes. Trends Biochem Sci 24:132–133
69. Wilson DJ, Gonzalez RN, Das HH (1997) Bovine mastitis pathogens in New York and Pennsylvania: prevalence and effects on somatic cell count and milk production. J Dairy Sci 80:2592–2598
70. Yancey RJ Jr (1999) Vaccines and diagnostic methods for bovine mastitis: fact and fiction. Adv Vet Med 41:257–273