Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses

PLoS Pathogens

Volumn 3, Issue 4, 2007, Pages 526-540

  Begun, Jakob ^a,b   Gaiani, Jessica M ^c   Rohde, Holger ^d   Mack, Dietrich ^e   Calderwood, Stephen B ^a,b   Ausubel, Frederick M ^a,b   Sifri, Costi D ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; EXOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSCRIPTION FACTOR; TRASCRIPTION FACTOR DAF 2; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; CAENORHABDITIS ELEGANS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PMK 1 PROTEIN, C ELEGANS; PMK-1 PROTEIN, C ELEGANS; POLYSACCHARIDE INTERCELLULAR ADHESIN; SEK1 PROTEIN, C ELEGANS;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOFILM; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DISEASE PREDISPOSITION; GENE LOCUS; GENE MUTATION; GENE OVEREXPRESSION; INNATE IMMUNITY; NONHUMAN; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS; STAPHYLOCOCCUS INFECTION; ANIMAL; DISEASE MODEL; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; STAPHYLOCOCCUS EPIDERMIDIS; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; NEMATODA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE MODELS, ANIMAL; IMMUNITY, NATURAL; INTESTINES; MAP KINASE KINASE 4; MITOGEN-ACTIVATED PROTEIN KINASES; POLYSACCHARIDES, BACTERIAL; SIGNAL TRANSDUCTION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS EPIDERMIDIS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 34247645197     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0030057     Document Type: Article

References (86)

1. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: A common cause of persistent infections. Science 284: 1318-1322.
2. Mah TF, O'Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9: 34-39.
3. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, et al. (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: Purification and structural analysis. J Bacteriol 178: 175-183.
4. Mack D, Nedelmann M, Krokotsch A, Schwarzkopf A, Heesemann J, et al. (1994) Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: Genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 62: 3244-3253.
5. Götz F (2002) Staphylococcus and biofilms. Mol Microbiol 43: 1367-1378.
6. Maira-Litrán T, Kropec A, Goldmann D, Pier GB (2004) Biologic properties and vaccine potential of the staphylococcal poly-N-acetyl glucosamine surface polysaccharide. Vaccine 22: 872-879.
7. Mack D, Rohde H, Harris LG, Davies AP, Horstkotte MA, et al. (2006) Biofilm formation in medical device-related infection. Int J Artif Organs 29: 343-359.
8. Heilmann C, Gerke C, Perdreau-Remington F, Götz F (1996) Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 64: 277-282.
9. Conlon KM, Humphreys H, O'Gara JP (2002) icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J Bacteriol 184: 4400-4408.
10. Rupp ME, Ulphani JS, Fey PD, Bartscht K, Mack D (1999) Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 67: 2627-2632.
11. Shiro H, Muller E, Gutierrez N, Boisot S, Grout M, et al. (1994) Transposon mutants of Staphylococcus epidermidis deficient in elaboration of capsular polysaccharide/adhesin and slime are avirulent in a rabbit model of endocarditis. J Infect Dis 169: 1042-1049.
12. Johnson GM, Lee DA, Regelmann WE, Gray ED, Peters G, et al. (1986) Interference with granulocyte function by Staphylococcus epidermidis slime. Infect Immun 54: 13-20.
13. Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR, et al. (2004) Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6: 269-275.
14. Galdbart JO, Allignet J, Tung HS, Ryden C, El Solh N (2000) Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J Infect Dis 182: 351-355.
15. Frebourg NB, Lefebvre S, Baert S, Lemeland JF (2000) PCR-Based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J Clin Microbiol 38: 877-880.
16. Ziebuhr W, Heilmann C, Götz F, Meyer P, Wilms K, et al. (1997) Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 65: 890-896.
17. McKenney D, Pouliot KL, Wang Y, Murthy V, Ulrich M, et al. (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284: 1523-1527.
18. Fluckiger U, Ulrich M, Steinhuber A, Doring G, Mack D, et al. (2005) Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 73: 1811-1819.
19. Knobloch JK, Horstkotte MA, Rohde H, Mack D (2002) Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol (Berl) 191: 101-106.
20. Cramton SE, Ulrich M, Götz F, Doring G (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69: 4079-4085.
21. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67: 5427-5433.
22. Martín-Loacute;pez JV, Pérez-Roth E, Claverie-Martin F, Díez Gil O, Batista N, et al. (2002) Detection of Staphylococcus aureus clinical isolates harboring the ica gene cluster needed for biofilm establishment. J Clin Microbiol 40: 1569-1570.
23. Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L, et al. (2002) Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70: 4987-4996.
24. Jefferson KK, Cramton SE, Götz F, Pier GB (2003) Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol Microbiol 48: 889-899.
25. Kropec A, Maira-Litrán T, Jefferson KK, Grout M, Cramton SE, et al. (2005) Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun 73: 6868-6876.
26. Rupp ME, Fey PD, Heilmann C, Götz F (2001) Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis 183: 1038-1042.
27. Francois P, Tu Quoc PH, Bisognano C, Kelley WL, Lew DP, et al. (2003) Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol Med Microbiol 35: 135-140.
28. Kristian SA, Golda T, Ferracin F, Cramton SE, Neumeister B, et al. (2004) The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb Pathog 36: 237-245.
29. Sifri CD, Begun J, Ausubel FM (2005) The worm has turned - Microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13: 119-127.
30. Kim DH, Ausubel FM (2005) Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr Opin Immunol 17: 4-10.
31. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, et al. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98: 10892-10897.
32. Sifri CD, Begun J, Ausubel FM, Calderwood SB (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71: 2208-2217.
33. Sifri CD, Mylonakis E, Singh KV, Qin X, Garsin DA, et al. (2002) Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70: 5647-5650.
34. Sifri CD, Baresch-Bernal A, Calderwood SB, von Eiff C (2006) Virulence of Staphylococcus aureus small colony variants in the Caenorhabditis elegans infection model. Infect Immun 74: 1091-1096.
35. Darby C, Hsu JW, Ghori N, Falkow S (2002) Caenorhabditis elegans: Plague bacteria biofilm blocks food intake. Nature 417: 243-244.
36. Joshua GW, Karlyshev AV, Smith MP, Isherwood KE, Titball RW, et al. (2003) A Caenorhabditis elegans model of Yersinia infection: Biofilm formation on a biotic surface. Microbiology 149: 3221-3229.
37. Kurz CL, Ewbank JJ (2003) Caenorhabditis elegans: An emerging genetic model for the study of innate immunity. Nat Rev Genet 4: 380-390.
38. Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, et al. (2001) A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 11: 809-821.
39. Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, et al. (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300: 1921.
40. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, et al. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12: 1209-1214.
41. Tan MW (2001) Genetic and genomic dissection of host-pathogen interactions using a P. aeruginosa-C. elegans pathogenesis model. Pediatr Pulmonol 32: 96-97.
42. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, et al. (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623-626.
43. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322.
44. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, et al. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994-999.
45. Paradis S, Ailion M, Toker A, Thomas JH, Ruvkun G (1999) A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev 13: 1438-1452.
46. Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28: 139-145.
47. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
48. Wolkow CA, Kimura KD, Lee MS, Ruvkun G (2000) Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290: 147-150.
49. Honda Y, Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13: 1385-1393.
50. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, et al. (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2: e183. doi:10.1371/journal.pgen.0020183
51. Riddle DL, Blumenthal T, Meyer BJ, Priess JR (1997) Introduction to C. elegans. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C elegans II. Plainview (New York): Cold Spring Harbor Laboratory Press. pp. 1-22.
52. Alegado RA, Campbell MC, Chen WC, Slutz SS, Tan MW (2003) Characterization of mediators of microbial virulence and innate immunity using the Caenorhabditis elegans host-pathogen model. Cell Microbiol 5: 435-444.
53. Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720.
54. Mack D, Riedewald J, Rohde H, Magnus T, Feucht HH, et al. (1999) Essential functional role of the polysaccharide intercellular adhesin of Staphylococcus epidermidis in hemagglutination. Infect Immun 67: 1004-1008.
55. Gerke C, Kraft A, Süßmuth R, Schweitzer O, Götz F (1998) Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273: 18586-18593.
56. Mack D, Bartscht K, Fischer C, Rohde H, de Grahl C, et al. (2001) Genetic and biochemical analysis of Staphylococcus epidermidis biofilm accumulation. Methods Enzymol 336: 215-239.
57. Höflich J, Berninsone P, Göbel C, Gravato-Nobre MJ, Libby BJ, et al. (2004) Loss of srf-3-encoded nucleotide sugar transporter activity in Caenorhabditis elegans alters surface antigenicity and prevents bacterial adherence. J Biol Chem 279: 30440-30448.
58. Aballay A, Yorgey P, Ausubel FM (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10: 1539-1542.
59. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, et al. (2003) Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 49: 1577-1593.
60. Thomas VL, Sanford BA, Moreno R, Ramsay MA (1997) Enzyme-linked lectinsorbent assay measures N-acetyl-D-glucosamine in matrix of biofilm produced by Staphylococcus epidermidis. Curr Microbiol 35: 249-254.
61. Tan L, Darby C (2004) A movable surface: Formation of Yersinia sp. biofilms on motile Caenorhabditis elegans. J Bacteriol 186: 5087-5092.
62. Miller DM, Shakes DC (1995) Immunofluorescence microscopy. Methods Cell Biol 48: 365-394.
63. Rupp ME, Fey PD (2001) In vivo models to evaluate adhesion and biofilm formation by Staphylococcus epidermidis. Methods Enzymol 336: 206-215.
64. Millet AC, Ewbank JJ (2004) Immunity in Caenorhabditis elegans. Curr Opin Immunol 16: 4-9.
65. Begun J, Sifri CD, Goldman S, Calderwood SB, Ausubel FM (2005) Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans-killing model. Infect Immun 73: 872-877.
66. Bae T, Banger AK, Wallace A, Glass EM, Aslund F, et al. (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci U S A 101: 12312-12317.
67. Blevins JS, Beenken KE, Elasri MO, Hurlburt BK, Smeltzer MS (2002) Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect Immun 70: 470-480.
68. Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, et al. (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186: 4665-4684.
69. Lazazzera BA (2005) Lessons from DNA microarray analysis: The gene expression profile of biofilms. Curr Opin Microbiol 8: 222-227.
70. Vuong C, Kocianova S, Yao Y, Carmody AB, Otto M (2004) Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J Infect Dis 190: 1498-1505.
71. Schulenburg H, Kurz CL, Ewbank JJ (2004) Evolution of the innate immune system: The worm perspective. Immunol Rev 198: 36-58.
72. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, et al. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279: 54881-54886.
73. Wang X, Preston JF 3rd, Romeo T (2004) The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186: 2724-2734.
74. Matz C, Kjelleberg S (2005) Off the hook - How bacteria survive protozoan grazing. Trends Microbiol 13: 302-307.
75. Matz C, McDougald D, Moreno AM, Yung PY, Yildiz FH, et al. (2005) Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc Natl Acad Sci U S A 102: 16819-16824.
76. Tanaka-Hino M, Sagasti A, Hisamoto N, Kawasaki M, Nakano S, et al. (2002) SEK-1 MAPKK mediates Ca2+ signaling to determine neuronal asymmetric development in Caenorhabditis elegans. EMBO Rep 3: 56-62.
77. Mizuno T, Hisamoto N, Terada T, Kondo T, Adachi M, et al. (2004) The Caenorhabditis elegans MAPK phosphatase VHP-1 mediates a novel JNK-like signaling pathway in stress response. EMBO J 23: 2226-2234.
78. Lewis JA, Fleming JT (1995) Basic culture methods. Methods Cell Biol 48: 3-29.
79. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
80. Sulston J, Hodgkin J (1988) Methods. In: Wood WB, editor. The nematode Caenorhabditis elegans. Cold Spring Harbor (New York): Cold Spring Harbor Laboratory. pp. 587-606.
81. Mack D, Siemssen N, Laufs R (1992) Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: Evidence for functional relation to intercellular adhesion. Infect Immun 60: 2048-2057.
82. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
83. Hawiger J, Niewiarowski S, Gurewich V, Thomas DP (1970) Measurement of fibrinogen and fibrin degradation products in serum by staphylococcal clumping test. J Lab Clin Med 75: 93-108.
84. Fawcett P, Eichenberger P, Losick R, Youngman P (2000) The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci U S A 97: 8063-8068.
85. Kim DH, Liberati NT, Mizuno T, Inoue H, Hisamoto N, et al. (2004) Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc Natl Acad Sci U S A 101: 10990-10994.
86. Hodgkin J, Kuwabara PE, Corneliussen B (2000) A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 10: 1615-1618.