Evolutionarily distinct bacteriophage endolysins featuring conserved peptidoglycan cleavage sites protect mice from MRSA infection

Journal of Antimicrobial Chemotherapy

Volumn 70, Issue 5, 2014, Pages 1453-1465

  Schmelcher, Mathias ^a,b   Shen, Yang ^b,c   Nelson, Daniel C ^c,d   Eugster, Marcel R ^b   Eichenseher, Fritz ^b   Hanke, Daniela C ^b   Loessner, Martin J ^b   Dong, Shengli ^e   Pritchard, David G ^e   Lee, Jean C ^f   Becker, Stephen C ^a   Foster Frey, Juli ^a   Donovan, David M ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Antibiotic resistance; Antimicrobial; Biofilm; Peptidoglycan hydrolase

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL ENZYME; ENDOLYSIN DERIVATIVE; HYDROLASE; LYSOSTAPHIN; OXACILLIN; PEPTIDOGLYCAN HYDROLASE; PEPTIDOGLYCAN HYDROLASE 2638A; PEPTIDOGLYCAN HYDROLASE 80ALPHA; PEPTIDOGLYCAN HYDROLASE LYSK; PEPTIDOGLYCAN HYDROLASE P68; PEPTIDOGLYCAN HYDROLASE PHI11; PEPTIDOGLYCAN HYDROLASE PHISH2; PEPTIDOGLYCAN HYDROLASE TWORT; PEPTIDOGLYCAN HYDROLASE WMY; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT; ENDOLYSIN; PEPTIDOGLYCAN; PROTEINASE; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL CLEARANCE; BACTERIOPHAGE; BIOFILM; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; IN VITRO STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOUSE; NONHUMAN; PROTEIN DOMAIN; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS HAEMOLYTICUS; STAPHYLOCOCCUS WARNERI; TURBIDITY; ZYMOGRAPHY; ANIMAL; BACTEREMIA; BAGG ALBINO MOUSE; BIOLOGICAL THERAPY; CELL WALL; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HYDROLYSIS; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PROCEDURES; STAPHYLOCOCCAL INFECTIONS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTEREMIA; BACTERIOPHAGES; BIOLOGICAL THERAPY; CELL WALL; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; FEMALE; HYDROLYSIS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; PEPTIDOGLYCAN; RECOMBINANT PROTEINS; STAPHYLOCOCCAL INFECTIONS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84929474892     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dku552     Document Type: Article

References (63)

1. Götz F, Bannerman T, Schleifer KH. The genera Staphylococcus and Macrococcus. In: Falkow S, Rosenberg E, Schleifer KH et al., eds. The Prokaryotes. New York: Springer, 2006; 5-75.
2. Sordillo LM, Streicher KL. Mammary gland immunity and mastitis susceptibility. J Mammary Gland Biol Neoplasia 2002; 7: 135-46.
3. Götz F. Staphylococcus and biofilms. Mol Microbiol 2002; 43: 1367-78.
4. Nelson DC, Schmelcher M, Rodriguez-Rubio L et al. Endolysins as antimicrobials. Adv Virus Res 2012; 83: 299-365.
5. Fox LK, Zadoks RN, Gaskins CT. Biofilmproduction by Staphylococcus aureus associated with intramammary infection. Vet Microbiol 2005; 107: 295-9.
6. Klevens RM, Morrison MA, Nadle J et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007; 298:1763-71.
7. De Oliveira AP, Watts JL, Salmon SA et al. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Europe and the United States. J Dairy Sci 2000; 83: 855-62.
8. Klevens RM, Edwards JR, Tenover FC et al. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003. Clin Infect Dis 2006; 42: 389-91.
9. Moran GJ, Amii RN, Abrahamian FM et al. Methicillin-resistant Staphylococcus aureus in community-acquired skin infections. Emerg Infect Dis 2005; 11: 928-30.
10. Fischetti VA. Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int J Med Microbiol 2010; 300: 357-62.
11. Schmelcher M, Donovan DM, Loessner MJ. Bacteriophage endolysins as novel antimicrobials. Future Microbiol 2012; 7: 1147-71.
12. Spratt BG. Resistance to antibiotics mediated by target alterations. Science 1994; 264: 388-93.
13. Schindler CA, Schuhardt VT. Lysostaphin: a new bacteriolytic agent for the Staphylococcus. Proc Natl Acad Sci USA 1964; 51: 414-21.
14. Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972; 36: 407-77.
15. Gründling A, Missiakas DM, Schneewind O. Staphylococcus aureus mutants with increased lysostaphin resistance. J Bacteriol 2006; 188:6286-97.
16. Loessner MJ. Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol 2005; 8: 480-7.
17. Whisstock JC, Lesk AM. SH3 domains in prokaryotes. Trends Biochem Sci 1999; 24: 132-3.
18. Becker SC, Foster-Frey J, Stodola AJ et al. Differentially conserved staphylococcal SH3b_5 cellwall binding domains confer increased staphylolytic and streptolytic activity to a streptococcal prophage endolysin domain. Gene 2009; 443: 32-41.
19. Becker SC, Dong S, Baker JR et al. LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells. FEMS Microbiol Lett 2009; 294: 52-60.
20. Navarre WW, Ton-That H, Faull KF et al. Multiple enzymatic activities of the murein hydrolase from staphylococcal phage f11. Identification of a D-alanyl-glycine endopeptidase activity. J Biol Chem 1999; 274:15847-56.
21. Schindler CA, Schuhardt VT. Purification and properties of lysostaphin-a lytic agent for Staphylococcus aureus. Biochim Biophys Acta 1965; 97: 242-50.
22. Abaev I, Foster-Frey J, Korobova O et al. Staphylococcal phage 2638A endolysin is lytic for Staphylococcus aureus and harbors an inter-lyticdomain secondary translational start site. Appl Microbiol Biotechnol 2013; 97: 3449-56.
23. Schmelcher M, Korobova O, Schischkova N et al. Staphylococcus haemolyticus prophage PhiSH2 endolysin relies on cysteine, histidinedependent amidohydrolases/peptidases activity for lysis 'from without'. J Biotechnol 2012; 162: 289-98.
24. Yokoi KJ, Kawahigashi N, Uchida M et al. The two-component cell lysis genes holWMY and lysWMY of the Staphylococcus warneri M phage varphiWMY: cloning, sequencing, expression, and mutational analysis in Escherichia coli. Gene 2005; 351: 97-108.
25. Loessner MJ, Gaeng S, Wendlinger G et al. The two-component lysis system of Staphylococcus aureus bacteriophage Twort: a large TTG-start holin and an associated amidase endolysin. FEMS Microbiol Lett 1998; 162: 265-74.
26. Christie GE, Matthews AM, King DG et al. The complete genomes of Staphylococcus aureus bacteriophages 80 and 80a-implications for the specificity of SaPI mobilization. Virology 2010; 407: 381-90.
27. Jayaswal RK, Lee YI, Wilkinson BJ. Cloning and expression of a Staphylococcus aureus gene encoding a peptidoglycan hydrolase activity. J Bacteriol 1990; 172: 5783-8.
28. O'Flaherty S, Coffey A, Meaney W et al. The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J Bacteriol 2005; 187: 7161-4.
29. Manoharadas S, Witte A, Bläsi U. Antimicrobial activity of a chimeric enzybiotic towards Staphylococcus aureus. J Biotechnol 2009; 139:118-23.
30. Kerr DE, Plaut K, Bramley AJ et al. Lysostaphin expression in mammary glands confers protection against staphylococcal infection in transgenic mice. Nat Biotechnol 2001; 19: 66-70.
31. Donovan DM, Foster-Frey J. LambdaSa2 prophage endolysin requires Cpl-7-binding domains and amidase-5 domain for antimicrobial lysis of streptococci. FEMS Microbiol Lett 2008; 287: 22-33.
32. Reichelt P, Schwarz C, Donzeau M. Single step protocol to purify recombinant proteins with low endotoxin contents. Protein Expr Purif 2006; 46: 483-8.
33. Donovan DM, Dong S, Garrett W et al. Peptidoglycan hydrolase fusions maintain their parental specificities. Appl Environ Microbiol 2006; 72:2988-96.
34. Eugster MR, Haug MC, Huwiler SG et al. The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid. Mol Microbiol 2011; 81: 1419-32.
35. Riordan JF, Vallee BL. Acetylation. In: Hirs CHW, ed. Methods in Enzymology. New York: Academic Press, 1967; 565-70.
36. Park JT, Johnson MJ. A submicrodetermination of glucose. J Biol Chem 1949; 181: 149-51.
37. Spiro RG. Analysis of sugars found in glycoproteins. In: Neufeld EF, Ginsburg V, eds. Methods in Enzymology. New York: Academic Press, 1966; 3-26.
38. Ghuysen JM, Tipper DJ, Strominger JL. Enzymes that degrade bacterial cell walls. Methods Enzymol 1966; 8: 685-99.
39. Pritchard DG, Dong S, Baker JR et al. The bifunctional peptidoglycan lysin of Streptococcus agalactieae bacteriophage B30. Microbiology 2004; 150: 2079-87.
40. Sass P, Bierbaum G. Lytic activity of recombinant bacteriophage phi11 and phi12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl Environ Microbiol 2007; 73: 347-52.
41. Christensen GD, Simpson WA, Younger JJ et al. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 1985; 22: 996-1006.
42. Daniel A, Euler C, Collin M et al. Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2010; 54: 1603-12.
43. Biswas B, Adhya S, Washart P et al. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect Immun 2002; 70: 204-10.
44. Synnott AJ, Kuang Y, Kurimoto M et al. Isolation from sewage influent and characterization of novel Staphylococcus aureus bacteriophages with wide host ranges and potent lytic capabilities. Appl Environ Microbiol 2009; 75: 4483-90.
45. Weidenmaier C, Kokai-Kun JF, Kristian SA et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 2004; 10: 243-5.
46. Peschel A, Vuong C, Otto M et al. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 2000; 44: 2845-7.
47. Kropec A, Maira-Litran T, Jefferson KK et al. Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun 2005; 73: 6868-76.
48. Weidenmaier C, Kokai-Kun JF, Kulauzovic E et al. Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int J Med Microbiol 2008; 298:505-13.
49. Watts A, Ke D,Wang Q et al. Staphylococcus aureus strains that express serotype 5 or serotype 8 capsular polysaccharides differ in virulence. Infect Immun 2005; 73: 3502-11.
50. Yokogawa K, Kawata S, Nishimura S et al. Mutanolysin, bacteriolytic agent for cariogenic streptococci: partial purification and properties. Antimicrob Agents Chemother 1974; 6: 156-65.
51. Fenton M, Casey PG, Hill C et al. The truncated phage lysin CHAP(k) eliminates Staphylococcus aureus in the nares of mice. Bioeng Bugs 2010; 1: 404-7.
52. Kusuma C, Kokai-Kun J. Comparison of four methods for determining lysostaphin susceptibility of various strains of Staphylococcus aureus. Antimicrob Agents Chemother 2005; 49: 3256-63.
53. Gaeng S, Scherer S, Neve H et al. Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl Environ Microbiol 2000; 66: 2951-8.
54. Cisani G, Varaldo PE, Grazi G et al. High-level potentiation of lysostaphin anti-staphyloccocal activity by lysozyme. Antimicrob Agents Chemother 1982; 21: 531-5.
55. Idelevich EA, von Eiff C, Friedrich AW et al. In vitro activity against Staphylococcus aureus of a novel antimicrobial agent, PRF-119, a recombinant chimeric bacteriophage endolysin. Antimicrob Agents Chemother 2011; 55: 4416-9.
56. Atilano ML, Pereira PM, Yates J et al. Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci USA 2010; 107: 18991-6.
57. Gründling A, Schneewind O. Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J Bacteriol 2006; 188: 2463-72.
58. Son JS, Lee SJ, Jun SY et al. Antibacterial and biofilm removal activity of a Podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl Microbiol Biotechnol 2010; 86: 1439-49.
59. Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001; 45: 999-1007.
60. Abee T, Kovacs AT, Kuipers OP et al. Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol 2011; 22: 172-9.
61. Borysowski J,Weber-Dabrowska B, Gorski A. Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med (Maywood) 2006; 231:366-77.
62. Entenza JM, Loeffler JM, Grandgirard D et al. Therapeutic effects of bacteriophage Cpl-1 lysin against Streptococcus pneumoniae endocarditis in rats. Antimicrob Agents Chemother 2005; 49: 4789-92.
63. Witzenrath M, Schmeck B, Doehn JM et al. Systemic use of the endolysin Cpl-1 rescues mice with fatal pneumococcal pneumonia. Crit Care Med 2009; 37: 642-9.