Inhibition of Staphylococcus aureus by lysostaphin-expressing Lactobacillus plantarum WCFS1 in a modified genital tract secretion medium

Applied and Environmental Microbiology

Volumn 77, Issue 24, 2011, Pages 8500-8508

  Liu, Huanli ^a   Gao, Yuan ^a   Yu, Li Rong ^a   Jones, Richard C ^b   Elkins, Christopher A ^c   Hart, Mark E ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b MS BIOWORKS   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFERED MEDIUM; CELL WALLS; COCULTURE; LACTOBACILLUS PLANTARUM; LACTOBACILLUS SPECIES; LACTOBACILLUS STRAINS; LYSOSTAPHIN; MICROFLORA; PROMOTER SEQUENCES; S. AUREUS; SIGNAL PEPTIDE; SIGNAL SEQUENCE; STAPHYLOCOCCUS AUREUS; TOXIC SHOCKS;

BACTERIA; MASS SPECTROMETRY; PH; PHYSIOLOGY; PROTEINS;

ECOLOGY;

LYSOSTAPHIN; RECOMBINANT PROTEIN; SIGNAL PEPTIDE;

BACTERIAL DISEASE; BACTERIUM; CHROMOSOME; CYTOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH RATE; INHIBITION; MASS SPECTROMETRY; PH; PLASMID; SECRETION; TOXIN;

ANTIBIOSIS; ARTICLE; CHEMISTRY; CULTURE MEDIUM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LACTOBACILLUS PLANTARUM; METABOLISM; PLASMID; PROMOTER REGION; SECRETION; STAPHYLOCOCCUS AUREUS; TRANSGENIC ORGANISM;

ANTIBIOSIS; CULTURE MEDIA; GENE EXPRESSION; HUMANS; LACTOBACILLUS PLANTARUM; LYSOSTAPHIN; ORGANISMS, GENETICALLY MODIFIED; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN SORTING SIGNALS; RECOMBINANT PROTEINS; STAPHYLOCOCCUS AUREUS;

EID: 83155188291     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06755-11     Document Type: Article

References (80)

1. Antikainen, J., V. Kuparinen, K. Lahteenmaki, and T. K. Korhonen. 2007. Enolases from gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol. Med. Microbiol. 51:526-534.
2. Antikainen, J., V. Kuparinen, K. Lahteenmaki, and T. K. Korhonen. 2007. pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J. Bacteriol. 189:4539-4543.
3. Antonio, M. A., S. E. Hawes, and S. L. Hillier. 1999. The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J. Infect. Dis. 180:1950-1956.
4. Aslim, B., and E. Kilic. 2006. Some probiotic properties of vaginal lactobacilli isolated from healthy women. Jpn. J. Infect. Dis. 59:249-253.
5. Bateman, A., and M. Bycroft. 2000. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299:1113-1119.
6. Beller, F. K., and K. W. Schweppe. 1979. Review on the biology of menstrual blood, p. 231-245. In F. K. Beller and G. G. B. Schumacher (ed.), The biology of the fluids of the female genital tract. North-Holland, New York, NY.
7. Bendtsen, J. D., L. J. Jensen, N. Blom, G. von Heijne, and S. Brunak. 2004. Feature-based prediction of non-classical and leaderless protein secretion. Protein. Eng. Des. Sel. 17:349-356.
8. Bendtsen, J. D., L. Kiemer, A. Fausboll, and S. Brunak. 2005. Non-classical protein secretion in bacteria. BMC Microbiol. 5:58.
9. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
10. Bergdoll, M. S., B. A. Crass, R. F. Reiser, R. N. Robbins, and J. P. Davis. 1981. A new staphylococcal enterotoxin, enterotoxin-F, associated with toxicshock syndrome Staphylococcus aureus isolates. Lancet i:1017-1021.
11. Bergmann, S., M. Rohde, and S. Hammerschmidt. 2004. Glyceraldehyde-3- phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect. Immun. 72:2416-2419.
12. Biswas, I., A. Gruss, S. D. Ehrlich, and E. Maguin. 1993. High-efficiency gene inactivation and replacement system for gram-positive bacteria. J. Bacteriol. 175:3628-3635.
13. Boekhorst, J., M. Wels, M. Kleerebezem, and R. J. Siezen. 2006. The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 152:3175-3183.
14. Boskey, E. R., R. A. Cone, K. J. Whaley, and T. R. Moench. 2001. Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum. Reprod. 16:1809-1813.
15. Boskey, E. R., K. M. Telsch, K. J. Whaley, T. R. Moench, and R. A. Cone. 1999. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect. Immun. 67:5170-5175.
16. Chesney, P. J. 1997. Toxic shock syndrome, p. 509-525. In K. B. Crossley and G. L. Archer (ed.), The staphylococci in human disease. Churchill Livingston, New York, NY.
17. Dajcs, J. J., et al. 2000. Lysostaphin treatment of methicillin-resistant Staphylococcus aureus keratitis in the rabbit. Invest. Ophthal. Vis. Sci. 41:1432-1437.
18. Dajcs, J. J., et al. 2001. Lysostaphin is effective in treating methicillinresistant Staphylococcus aureus endophthalmitis in the rabbit. Curr. Eye Res. 22:451-457.
19. Dinges, M. M., P. M. Orwin, and P. M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13:16-34.
20. Elkins, C. A., M. E. Munoz, L. B. Mullis, R. L. Stingley, and M. E. Hart. 2008. Lactobacillus-mediated inhibition of clinical toxic shock syndrome Staphylococcus aureus strains and its relation to acid and peroxide production. Anaerobe 14:261-267.
21. Eschenbach, D. 1993. Toxic shock syndrome-menstrual vs nonmenstrual. Clin. Infect. Dis. 17:292.
22. Falagas, M. E., G. I. Betsi, and S. Athanasiou. 2007. Probiotics for the treatment of women with bacterial vaginosis. Clin. Microbiol. Infect. 13:657-664.
23. Gaventa, S., et al. 1989. Active surveillance for toxic shock syndrome in the United States, 1986. Rev. Infect. Dis. 11:S28-S34.
24. Geshnizgani, A. M., and A. B. Onderdonk. 1992. Defined medium simulating genital tract secretions for growth of vaginal microflora. J. Clin. Microbiol. 30:1323-1326.
25. Harris, R. I., A. W. Nunnery, and H. D. Riley. 1967. Effects of lysostaphin on staphylococcal carriage in infants and children. Antimicrob. Agents Chemother. 7:110-112.
26. Heinrich, P., R. Rosenstein, M. Bohmer, P. Sonner, and F. Gotz. 1987. The molecular organization of the lysostaphin gene and its sequences repeated in tandem. Mol. Gen. Genet. 209:563-569.
27. Hill, D. R., et al. 2005. In vivo assessment of human vaginal oxygen and carbon dioxide levels during and post menses. J. Appl. Physiol. 99:1582-1591.
28. Hols, P., T. Ferain, D. Garmyn, N. Bernard, and J. Delcour. 1994. Use of homologous expression-secretion signals and vector-free stable chromosomal integration in engineering of Lactobacillus plantarum for alpha-amylase and levanase expression. Appl. Environ. Microbiol. 60:1401-1413.
29. Horton, R. M., et al. 1993. Gene-splicing by overlap extension. Methods Enzymol. 217:270-279.
30. Iversen, O. J., and A. Grov. 1973. Studies on lysostaphin. Separation and characterization of three enzymes. Eur. J. Biochem. 38:293-300.
31. Jankovic, I., et al. 2003. Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. J. Bacteriol. 185:3288-3296.
32. Jones, R. C., J. Deck, R. D. Edmondson, and M. E. Hart. 2008. Relative quantitative comparisons of the extracellular protein profiles of Staphylococcus aureus UAMS-1 and its sarA, agr, and sarA agr regulatory mutants using one-dimensional polyacrylamide gel electrophoresis and nanocapillary liquid chromatography coupled with tandem mass spectrometry. J. Bacteriol. 190:5265-5278.
33. Kim, Y. H., K. S. Han, S. Oh, S. You, and S. H. Kim. 2005. Optimization of technical conditions for the transformation of Lactobacillus acidophilus strains by electroporation. J. Appl. Microbiol. 99:167-174.
34. Kleerebezem, M., et al. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. U. S. A. 100:1990-1995.
35. Kokai-Kun, J. F., T. Chanturiya, and J. J. Mond. 2007. Lysostaphin as a treatment for systemic Staphylococcus aureus infection in a mouse model. J. Antimicrob. Chemother. 60:1051-1059.
36. Kokai-Kun, J. F., S. M. Walsh, T. Chanturiya, and J. J. Mond. 2003. Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob. Agents Chemother. 47:1589-1597.
37. Kumar, J. K. 2008. Lysostaphin: an antistaphylococcal agent. Appl. Microbiol. Biotechnol. 80:555-561.
38. Laughton, J. M., E. Devillard, D. E. Heinrichs, G. Reid, and J. K. McCormick. 2006. Inhibition of expression of a staphylococcal superantigen-like protein by a soluble factor from Lactobacillus reuteri. Microbiology 152:1155-1167.
39. Leer, R. J., et al. 1993. Gene disruption in Lactobacillus plantarum strain 80 by site-specific recombination: isolation of a mutant strain deficient in conjugated bile salt hydrolase activity. Mol. Gen. Genet. 239:269-272.
40. Leloup, L., S. D. Ehrlich, M. Zagorec, and F. Morel-Deville. 1997. Singlecrossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes. Appl. Environ. Microbiol. 63:2117-2123.
41. MacPhee, R. A., R. Hummelen, J. E. Bisanz, W. L. Miller, and G. Reid. 2010. Probiotic strategies for the treatment and prevention of bacterial vaginosis. Exp. Opin. Pharmacother. 11:2985-2995.
42. Maguin, E., H. Prevost, S. D. Ehrlich, and A. Gruss. 1996. Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J. Bacteriol. 178:931-935.
43. McCormick, J. K., J. M. Yarwood, and P. M. Schlievert. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol. 55:77-104.
44. Modun, B., and P. Williams. 1999. The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect. Immun. 67:1086-1092.
45. Moller, B., and P. Kaspersen. 1991. The acidity of the vagina, p. 63-68. In B. Horowitz and P. A. Marc (ed.), Vaginitis and vaginosis. Wiley-Liss, New York, NY.
46. Musser, J. M., et al. 1990. A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome. Proc. Natl. Acad. Sci. U. S. A. 87:225-229.
47. Nelson, D., et al. 2001. pH-regulated secretion of a glyceraldehyde-3-phosphate dehydrogenase from Streptococcus gordonii FSS2: purification, characterization, and cloning of the gene encoding this enzyme. J. Dent. Res. 80:371-377.
48. Ocana, V. S., A. A. P. D. Holgado, and M. E. Nader-Macias. 1999. Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain. Appl. Environ. Microbiol. 65:5631-5635.
49. Osset, J., R. M. Bartolome, E. Garcia, and A. Andreu. 2001. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J. Infect. Dis. 183:485-491.
50. Otero, M. C., and M. E. Nader-Macias. 2006. Inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus gasseri isolated from the vaginal tract of cattle. Anim. Reprod. Sci. 96:35-46.
51. Pancholi, V., and V. A. Fischetti. 1998. Alpha-enolase, a novel strong plasmin( ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515.
52. Parsonnet, J., et al. 2008. Prevalence of toxic shock syndrome toxin 1 (TSST-1)-producing strains of Staphylococcus aureus and antibody to TSST-1 among healthy Japanese women. J. Clin. Microbiol. 46:2731-2738.
53. Polak, J., P. Della Latta, and P. Blackburn. 1993. In vitro activity of recombinant lysostaphin-antibiotic combinations toward methicillin-resistant Staphylococcus aureus. Diagn. Microbiol. Infect. Dis. 17:265-270.
54. Pybus, V., and A. B. Onderdonk. 1999. Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect. 1:285-292.
55. Quickel, K. E., Jr., R. Selden, J. R. Caldwell, N. F. Nora, and W. Schaffner. 1971. Efficacy and safety of topical lysostaphin treatment of persistent nasal carriage of Staphylococcus aureus. Appl. Microbiol. 22:446-450.
56. Ravel, J., et al. 2011. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 108:4680-4687.
57. Recsei, P. A., A. D. Gruss, and R. P. Novick. 1987. Cloning, sequence, and expression of the lysostaphin gene from Staphylococcus simulans. Proc. Natl. Acad. Sci. U. S. A. 84:1127-1131.
58. Redondo-Lopez, V., R. L. Cook, and J. D. Sobel. 1990. Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial microflora. Rev. Infect. Dis. 12:856-872.
59. Reid, G., J. Dols, and W. Miller. 2009. Targeting the vaginal microbiota with probiotics as a means to counteract infections. Curr. Opin. Clin. Nutr. Metab. Care 12:583-587.
60. Reid, G., J. Jass, M. T. Sebulsky, and J. K. McCormick. 2003. Potential uses of probiotics in clinical practice. Clin. Microbiol. Rev. 16:658-672.
61. Reniero, R., P. Cocconcelli, V. Bottazzi, and L. Morelli. 1992. High-frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J. Gen. Microbiol. 138:763-768.
62. Russell, W. M., and T. R. Klaenhammer. 2001. Efficient system for directed integration into the Lactobacillus acidophilus and Lactobacillus gasseri chromosomes via homologous recombination. Appl. Environ. Microbiol. 67:4361-4364.
63. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
64. Schindler, C. A., and V. T. Schuhardt. 1965. Purification and properties of lysostaphin-a lytic agent for Staphylococcus aureus. Biochim. Biophys. Acta 97:242-250.
65. Schlievert, P. M., K. N. Shands, B. B. Dan, G. P. Schmid, and R. D. Nishimura. 1981. Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic shock syndrome. J. Infect. Dis. 143:509-516.
66. Schlievert, P. M., T. J. Tripp, and M. L. Peterson. 2004. Reemergence of staphylococcal toxic shock syndrome in Minneapolis-St. Paul, Minnesota, during the 2000-2003 surveillance period. J. Clin. Microbiol. 42:2875-2876.
67. Shah, A., J. Mond, and S. Walsh. 2004. Lysostaphin-coated catheters eradicate Staphylococcus aureus challenge and block surface colonization. Antimicrob. Agents Chemother. 48:2704-2707.
68. Shands, K. N., et al. 1980. Toxic shock syndrome in menstruating women: association with tampon use and Staphylococcus aureus and clinical features in 52 cases. N. Engl. J. Med. 303:1436-1442.
69. Sloan, G. L., J. M. Robinson, and W. E. Kloos. 1982. Identification of Staphylococcus staphylolyticus NRRL B-2628 as a biovar of Staphylococcus simulans. Int. J. Syst. Bacteriol. 32:170-174.
70. Stark, F. R., C. Thornsvard, E. P. Flannery, and M. S. Artenstein. 1974. Systemic lysostaphin in man-apparent antimicrobial activity in a neutropenic patient. N. Engl. J. Med. 291:239-241.
71. Thumm, G., and F. Gotz. 1997. Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. Mol. Microbiol. 23:1251-1265.
72. Todd, J., M. Fishaut, F. Kapral, and T. Welch. 1978. Toxic-shock syndrome associated with phage-group-1 staphylococci. Lancet ii:1116-1118.
73. Turner, M. S., L. M. Hafner, T. Walsh, and P. M. Giffard. 2004. Identification and characterization of the novel LysM domain-containing surface protein Sep from Lactobacillus fermentum BR11 and its use as a peptide fusion partner in Lactobacillus and Lactococcus. Appl. Environ. Microbiol. 70:3673-3680.
74. Turner, M. S., F. Waldherr, M. J. Loessner, and P. M. Giffard. 2007. Antimicrobial activity of lysostaphin and a Listeria monocytogenes bacteriophage endolysin produced and secreted by lactic acid bacteria. Syst. Appl. Microbiol. 30:58-67.
75. Valore, E. V., C. H. Park, S. L. Igreti, and T. Ganz. 2002. Antimicrobial components of vaginal fluid. Am. J. Obstet. Gynecol. 187:561-568.
76. Ventura, M., I. Jankovic, D. C. Walker, R. D. Pridmore, and R. Zink. 2002. Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl. Environ. Microbiol. 68:6172-6181.
77. Vergeront, J. M., et al. 1983. Prevalence of serum antibody to staphylococcal enterotoxin F among Wisconsin residents: implications for toxic shock syndrome. J. Infect. Dis. 148:692-698.
78. Yarwood, J. M., and P. M. Schlievert. 2000. Oxygen and carbon dioxide regulation of toxic shock syndrome toxin 1 production by Staphylococcus aureus MN8. J. Clin. Microbiol. 38:1797-1803.
79. Yu, L. R., et al. 2007. Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J. Proteome Res. 6:4150-4162.
80. Zozaya-Hinchliffe, M., R. Lillis, D. H. Martin, and M. J. Ferris. 2010. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J. Clin. Microbiol. 48:1812-1819.