Murine immune response to a chronic Staphylococcus aureus biofilm infection

Infection and Immunity

Volumn 79, Issue 4, 2011, Pages 1789-1796

  Prabhakara, Ranjani ^a,b   Harro, Janette M ^a   Leid, Jeff G ^c   Harris, Megan ^a,b   Shirtliff, Mark E ^a,b  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; HERMES ANTIGEN; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL VIABILITY; BACTERIUM CULTURE; BIOFILM; C57BL 6 MOUSE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DOWN REGULATION; IMMUNE RESPONSE; IMPLANTATION; INFLAMMATION; MOUSE; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TH1 CELL; TH17 CELL; TIBIA; TISSUE LEVEL; UPREGULATION;

ANIMALS; BIOFILMS; BONE NAILS; CHRONIC DISEASE; CYTOKINES; FLOW CYTOMETRY; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; PROSTHESIS-RELATED INFECTIONS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTES;

EID: 79953309287     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01386-10     Document Type: Article

References (48)

1. Arciola, C. R., M. Cervellati, V. Pirini, S. Gamberini, and L. Montanaro. 2001. Staphylococci in orthopaedic surgical wounds. New Microbiol. 24:365-369.
2. Assenmacher, M., et al. 1998. Sequential production of IL-2, IFN-gamma and IL-10 by individual staphylococcal enterotoxin B-activated T helper lymphocytes. Eur. J. Immunol. 28:1534-1543.
3. Aujla, S. J., P. J. Dubin, and J. K. Kolls. 2007. Th17 cells and mucosal host defense. Semin. Immunol. 19:377-382.
4. Beenken, K. E., et al. 2004. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186:4665-4684.
5. Benton, B. M., et al. 2004. Large-scale identification of genes required for full virulence of Staphylococcus aureus. J. Bacteriol. 186:8478-8489.
6. Brady, R. A., J. G. Leid, A. K. Camper, J. W. Costerton, and M. E. Shirtliff. 2006. Identification of Staphylococcus aureus proteins recognized by the antibody-mediated immune response to a biofilm infection. Infect. Immun. 74:3415-3426.
7. Breuer, K., et al. 2005. Alpha-toxin is produced by skin colonizing Staphylococcus aureus and induces a T helper type 1 response in atopic dermatitis. Clin. Exp. Allergy 35:1088-1095.
8. Cardona, I. D., E. Goleva, L. S. Ou, and D. Y. Leung. 2006. Staphylococcal enterotoxin B inhibits regulatory T cells by inducing glucocorticoid-induced TNF receptor-related protein ligand on monocytes. J. Allergy Clin. Immunol. 117:688-695.
9. Carper, H. T., G. W. Sullivan, and G. L. Mandell. 1987. Teicoplanin, vancomycin, rifampicin: in-vivo and in-vitro studies with Staphylococcus aureus. J. Antimicrob. Chemother. 19:659-662.
10. Cassat, J., et al. 2006. Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology 152: 3075-3090.
11. Cassat, J. E., et al. 2005. Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J. Bacteriol. 187:576-592.
12. Cassat, J. E., C. Y. Lee, and M. S. Smeltzer. 2007. Investigation of biofilm formation in clinical isolates of Staphylococcus aureus. Methods Mol. Biol. 391:127-144.
13. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
14. Dauwalder, O., et al. 2006. Comparative inflammatory properties of staphylococcal superantigenic enterotoxins SEA and SEG: implications for septic shock. J. Leukoc. Biol. 80:753-758.
15. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
16. Fedtke, I., F. Gotz, and A. Peschel. 2004. Bacterial evasion of innate host defenses-the Staphylococcus aureus lesson. Int. J. Med. Microbiol. 294: 189-194.
17. Gillaspy, A. F., et al. 1995. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 63:3373-3380.
18. Grundmann, H., M. ires-de-Sousa, J. Boyce, and E. Tiemersma. 2006. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368:874-885.
19. Halabi-Tawil, M., et al. 2009. Cutaneous manifestations of immune dysregulation, polyendocrinopathy, enteropathy, X-linked (IPEX) syndrome. Br. J. Dermatol. 160:645-651.
20. Hekiert, A. M., et al. 2009. Biofilms correlate with TH1 inflammation in the sinonasal tissue of patients with chronic rhinosinusitis. Otolaryngol. Head Neck Surg. 141:448-453.
21. Heriazon, A., et al. 2009. Regulatory T cells modulate staphylococcal enterotoxin B-induced effector T-cell activation and acceleration of colitis. Infect. Immun. 77:707-713.
22. Horan, T. C., et al. 1993. Nosocomial infections in surgical patients in the United States, January 1986-June 1992. National Nosocomial Infections Surveillance (NNIS) System. Infect. Control Hosp. Epidemiol. 14:73-80.
23. Klevens, R. M., et al. 2007. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763-1771.
24. Knudsen, J. D., K. Fuursted, S. Raber, F. Espersen, and N. Frimodt-Moller. 2000. Pharmacodynamics of glycopeptides in the mouse peritonitis model of Streptococcus pneumoniae or Staphylococcus aureus infection. Antimicrob. Agents Chemother. 44:1247-1254.
25. Kristian, S. A., et al. 2008. Biofilm formation induces C3a release and protects Staphylococcus epidermidis from IgG and complement deposition and from neutrophil-dependent killing. J. Infect. Dis. 197:1028-1035.
26. Leid, J. G., M. E. Shirtliff, J. W. Costerton, and A. P. Stoodley. 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect. Immun. 70:6339-6345.
27. Leijh, P. C., M. T. van den Barselaar, M. R. Daha, and R. van Furth. 1981. Participation of immunoglobulins and complement components in the intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Infect. Immun. 33:714-724.
28. Li, D., et al. 2008. Quantitative mouse model of implant-associated osteo-myelitis and the kinetics of microbial growth, osteolysis, and humoral immunity. J. Orthop. Res. 26:96-105.
29. Lindsay, J. A., and M. T. Holden. 2004. Staphylococcus aureus: superbug, super genome? Trends Microbiol. 12:378-385.
30. Mader, J. T., D. Mohan, and J. Calhoun. 1997. A practical guide to the diagnosis and management of bone and joint infections. Drugs 54:253-264.
31. Mader, J. T., M. Shirtliff, and J. H. Calhoun. 1997. Staging and staging application in osteomyelitis. Clin. Infect. Dis. 25:1303-1309.
32. Mader, J. T., and M. E. Shirtliff. 1999. The rabbit model of bacterial osteomyelitis of the tibia. Academic Press Ltd., London, England.
33. Megyeri, K., Y. Mandi, M. Degre, and I. Rosztoczy. 2002. Induction of cytokine production by different Staphylococcal strains. Cytokine 19:206-212.
34. Nayak, D. K., A. Asha, K. M. Shankar, and C. V. Mohan. 2004. Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of Clarias batrachus- a carnivore model. Fish Shellfish Immunol. 16:613-619.
35. Nishimura, S., T. Tsurumoto, A. Yonekura, K. Adachi, and H. Shindo. 2006. Antimicrobial susceptibility of Staphylococcus aureus and Staphylococcus epidermidis biofilms isolated from infected total hip arthroplasty cases. J. Orthop. Sci. 11:46-50.
36. Raad, I. I., R. Darouiche, R. Hachem, M. Sacilowski, and G. P. Bodey. 1995. Antibiotics and prevention of microbial colonization of catheters. Antimicrob. Agents Chemother. 39:2397-2400.
37. Rice, K. C., et al. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 104(19):8113-8118.
38. Sanderson, P. J. 1991. Infection in orthopaedic implants. J. Hosp. Infect. 18(Suppl. A):367-375.
39. Shirtliff, M. E., J. H. Calhoun, and J. T. Mader. 2002. Gatifloxacin efficacy in treatment of experimental methicillin-sensitive Staphylococcus aureusinduced osteomyelitis in rabbits. Antimicrob. Agents Chemother. 46:231-233.
40. Shirtliff, M. E., and J. T. Mader. 2000. Osteomyelitis: clinical features and molecular aspects of persistence, p. 375-395. In J. P. Nataro, M. J. Blaser, and S. Cunningham-Rundles (ed.), Persistent bacterial infections. ASM Press, Washington, DC.
41. Shkreta, L., B. G. Talbot, M. S. Diarra, and P. Lacasse. 2004. Immune responses to a DNA/protein vaccination strategy against Staphylococcus aureus induced mastitis in dairy cows. Vaccine 23:114-126.
42. Sinha, P., A. K. Ghosh, T. Das, G. Sa, and P. K. Ray. 1999. Protein A of Staphylococcus aureus evokes Th1 type response in mice. Immunol. Lett. 67:157-165.
43. Smeltzer, M. S., F. L. Pratt, A. F. Gillaspy, and L. A. Young. 1996. Genomic fingerprinting for epidemiological differentiation of Staphylococcus aureus clinical isolates. J. Clin. Microbiol. 34:1364-1372.
44. Sun, D., M. A. Accavitti, and J. D. Bryers. 2005. Inhibition of biofilm formation by monoclonal antibodies against Staphylococcus epidermidis RP62A accumulation-associated protein. Clin. Diagn. Lab. Immunol. 12:93-100.
45. Tsuji, M., M. Takema, H. Miwa, J. Shimada, and S. Kuwahara. 2003. In vivo antibacterial activity of S-3578, a new broad-spectrum cephalosporin: methicillin-resistant Staphylococcus aureus and Pseudomonas aeruginosa experimental infection models. Antimicrob. Agents Chemother. 47:2507-2512.
46. Wagner, C., G. M. Hansch, A. Wentzensen, and V. Heppert. 2006. Implantassociated post-traumatic osteomyelitis. Bacterial biofilms and the immune defence as protagonists of the local inflammatory process. Unfallchirurg 109:761-769. (In German.)
47. Wang, R., et al. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 13:1510-1514.
48. Xu, G., et al. 2009. Interleukin-6 is essential for staphylococcal exotoxin B-induced T regulatory cell insufficiency in nasal polyps. Clin. Exp. Allergy 39(6):829-837.