Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 83-93 , 25 January 2010

Evaluation of capsular and acapsular strains of S. aureus in an experimental brain abscess model

  • Nilufer Esen

      Affiliations

    • Department of Neurology, Holtom-Garrett Program in Neuroimmunology, University of Michigan Medical School, Ann Arbor, MI 48109, United States
    • Corresponding Author InformationCorresponding author. University of Michigan Medical School, Department of Neurology, Holtom-Garrett Program in Neuroimmunology, BSRB Room 4218, 109 Zina Pitcher Place, Ann Arbor, MI 48109-2200, United States. Tel.: +1 734 615 6939; fax: +1 734 615 2866.
    • ,
  • Gail Wagoner

      Affiliations

    • Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, AR 72205, United States
    • ,
  • Napoleon Philips

      Affiliations

    • Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, AR 72205, United States

Received 15 June 2009 ,Revised 8 October 2009 ,Accepted 9 October 2009.

References 

  1. Abdelnour A, Arvidson S, Bremell T, Ryden C, Tarkowski A. The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect. Immun. 1993;61:3879–3885
  2. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol. Aging. 2000;21:383–421
  3. Archer GL. Staphylococcus aureus: a well-armed pathogen. Clin. Infect. Dis. 1998;26:1179–1181
  4. Asano-Kato N, Fukagawa K, Okada N, Dogru M, Tsubota K, Fujishima H. Tryptase increases proliferative activity of human conjunctival fibroblasts through protease-activated receptor-2. Invest. Ophthalmol. Vis. Sci. 2005;46:4622–4626
  5. Baldwin AC, Kielian T. Persistent immune activation associated with a mouse model of Staphylococcus aureus-induced experimental brain abscess. J. Neuroimmunol. 2004;151:24–32
  6. Barnum SR, Ames RS, Maycox PR, Hadingham SJ, Meakin J, Harrison D, et al. Expression of the complement C3a and C5a receptors after permanent focal ischemia: an alternative interpretation. Glia. 2002;38:169–173
  7. Beenken KE, Blevins JS, Smeltzer MS. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 2003;71:4206–4211
  8. Birmingham DJ. Erythrocyte complement receptors. Crit. Rev. Immunol. 1995;15:133–154
  9. Birmingham DJ, Hebert LA. CR1 and CR1-like: the primate immune adherence receptors. Immunol. Rev. 2001;180:100–111
  10. Blevins JS, Beenken KE, Elasri MO, Hurlburt BK, Smeltzer MS. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect. Immun. 2002;70:470–480
  11. Boos L, Campbell IL, Ames R, Wetsel RA, Barnum SR. Deletion of the complement anaphylatoxin C3a receptor attenuates, whereas ectopic expression of C3a in the brain exacerbates, experimental autoimmune encephalomyelitis. J. Immunol. 2004;173:4708–4714
  12. Booth MC, Cheung AL, Hatter KL, Jett BD, Callegan MC, Gilmore MS. Staphylococcal accessory regulator (sar) in conjunction with agr contributes to Staphylococcus aureus virulence in endophthalmitis. Infect. Immun. 1997;65:1550–1556
  13. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. Mature microglia resemble immature antigen-presenting cells. Glia. 1998;22:72–85
  14. Cassat J, Dunman PM, Murphy E, Projan SJ, Beenken KE, Palm KJ, et al. 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. 2006;152:3075–3090
  15. Chavakis T, Preissner KT, Herrmann M. The anti-inflammatory activities of Staphylococcus aureus. Trends Immunol. 2007;28:408–418
  16. Cheung AL, Yeaman MR, Sullam PM, Witt MD, Bayer AS. Role of the sar locus of Staphylococcus aureus in induction of endocarditis in rabbits. Infect. Immun. 1994;62:1719–1725
  17. Claman HN. On scleroderma. Mast cells, endothelial cells, and fibroblasts. Jama. 1989;262:1206–1209
  18. Davoust N, Jones J, Stahel PF, Ames RS, Barnum SR. Receptor for the C3a anaphylatoxin is expressed by neurons and glial cells. Glia. 1999;26:201–211
  19. Engelhardt B. Immune cell entry into the central nervous system: involvement of adhesion molecules and chemokines. J. Neurol. Sci. 2008;274:23–26
  20. Esen N, Tanga FY, DeLeo JA, Kielian T. Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus. J. Neurochem. 2004;88:746–758
  21. Flaris NA, Hickey WF. Development and characterization of an experimental model of brain abscess in the rat. Am. J. Pathol. 1992;141:1299–1307
  22. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol. 1995;154:4309–4321
  23. Frungieri MB, Weidinger S, Meineke V, Kohn FM, Mayerhofer A. Proliferative action of mast-cell tryptase is mediated by PAR2, COX2, prostaglandins, and PPARgamma: possible relevance to human fibrotic disorders. Proc. Natl. Acad. Sci. U. S. A. 2002;99:15072–15077
  24. Galimberti R, Pietropaolo N, Galimberti G, Kowalczuk A. Adult purpura fulminans associated with staphylococcal infection and administration of colony-stimulating factors. Eur. J. Dermatol. 2003;13:95–97
  25. Gasque P, Singhrao SK, Neal JW, Wang P, Sayah S, Fontaine M, et al. The receptor for complement anaphylatoxin C3a is expressed by myeloid cells and nonmyeloid cells in inflamed human central nervous system: analysis in multiple sclerosis and bacterial meningitis. J. Immunol. 1998;160:3543–3554
  26. Gruber BL, Kew RR, Jelaska A, Marchese MJ, Garlick J, Ren S, et al. Human mast cells activate fibroblasts: tryptase is a fibrogenic factor stimulating collagen messenger ribonucleic acid synthesis and fibroblast chemotaxis. J. Immunol. 1997;158:2310–2317
  27. Guo RF, Ward PA. Role of C5a in inflammatory responses. Annu. Rev. Immunol. 2005;23:821–852
  28. Hochkeppel HK, Braun DG, Vischer W, Imm A, Sutter S, Staeubli U, et al. Serotyping and electron microscopy studies of Staphylococcus aureus clinical isolates with monoclonal antibodies to capsular polysaccharide types 5 and 8. J. Clin. Microbiol. 1987;25:526–530
  29. Hoffman WH, Stamatovic SM, Andjelkovic AV. Inflammatory mediators and blood brain barrier disruption in fatal brain edema of diabetic ketoacidosis. Brain Res. 2009;1254:138–148
  30. Karakawa WW, Sutton A, Schneerson R, Karpas A, Vann WF. Capsular antibodies induce type-specific phagocytosis of capsulated Staphylococcus aureus by human polymorphonuclear leukocytes. Infect. Immun. 1988;56:1090–1095
  31. Kawanami O, Ferrans VJ, Fulmer JD, Crystal RG. Ultrastructure of pulmonary mast cells in patients with fibrotic lung disorders. Lab. Invest. 1979;40:717–734
  32. Kielian T. Immunopathogenesis of brain abscess. J. Neuroinflammation. 2004;1:16
  33. Kielian T, Hickey WF. Proinflammatory cytokine, chemokine, and cellular adhesion molecule expression during the acute phase of experimental brain abscess development. Am. J. Pathol. 2000;157:647–658
  34. Kielian T, Cheung A, Hickey WF. Diminished virulence of an alpha-toxin mutant of Staphylococcus aureus in experimental brain abscesses. Infect. Immun. 2001;69:6902–6911
  35. Kielian T, Barry B, Hickey WF. CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J. Immunol. 2001;166:4634–4643
  36. Kielian T, Bearden ED, Baldwin AC, Esen N. IL-1 and TNF-alpha play a pivotal role in the host immune response in a mouse model of Staphylococcus aureus-induced experimental brain abscess. J. Neuropathol. Exp. Neurol. 2004;63:381–396
  37. Kielian T, McMahon M, Bearden ED, Baldwin AC, Drew PD, Esen N. S. aureus-dependent microglial activation is selectively attenuated by the cyclopentenone prostaglandin 15-deoxy-Delta12, 14- prostaglandin J2 (15d-PGJ2). J. Neurochem. 2004;90:1163–1172
  38. Kielian T, Haney A, Mayes PM, Garg S, Esen N. Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect. Immun. 2005;73:7428–7435
  39. Kielian T, Phulwani NK, Esen N, Syed MM, Haney AC, McCastlain K, et al. MyD88-dependent signals are essential for the host immune response in experimental brain abscess. J. Immunol. 2007;178:4528–4537
  40. Kielian T, Syed MM, Liu S, Phulwani NK, Phillips N, Wagoner G, et al. The synthetic peroxisome proliferator-activated receptor-gamma agonist ciglitazone attenuates neuroinflammation and accelerates encapsulation in bacterial brain abscesses. J. Immunol. 2008;180:5004–5016
  41. Kildsgaard J, Hollmann TJ, Matthews KW, Bian K, Murad F, Wetsel RA. Cutting edge: targeted disruption of the C3a receptor gene demonstrates a novel protective anti-inflammatory role for C3a in endotoxin-shock. J. Immunol. 2000;165:5406–5409
  42. Kondo S, Kagami S, Kido H, Strutz F, Muller GA, Kuroda Y. Role of mast cell tryptase in renal interstitial fibrosis. J. Am. Soc. Nephrol. 2001;12:1668–1676
  43. Krych-Goldberg M, Barlow Paul N, Mallin Rosie L, Atkinson JP. C3b/C4b binding site of complement receptor type 1 (CR1, CD35). In:  Lambris JD,  Morikis D editor. Structural Biology of Complement System. Boca Raton, Florida, USA: CRC Press; 2005;p. 179–232
  44. Leroy EC, Smith EA, Kahaleh MB, Trojanowska M, Silver RM. A strategy for determining the pathogenesis of systemic sclerosis. Is transforming growth factor beta the answer?. Arthritis Rheum. 1989;32:817–825
  45. Levi-Schaffer F, Piliponsky AM. Tryptase, a novel link between allergic inflammation and fibrosis. Trends Immunol. 2003;24:158–161
  46. Lindorfer MA, Hahn CS, Foley PL, Taylor RP. Heteropolymer-mediated clearance of immune complexes via erythrocyte CR1: mechanisms and applications. Immunol. Rev. 2001;183:10–24
  47. Lowy FD. Staphylococcus aureus infections. N. Engl. J. Med. 1998;339:520–532
  48. Mathisen GE, Johnson JP. Brain abscess. Clin Infect Dis. 1997;25:763–779quiz 780–761
  49. Matsushima R, Takahashi A, Nakaya Y, Maezawa H, Miki M, Nakamura Y, et al. Human airway trypsin-like protease stimulates human bronchial fibroblast proliferation in a protease-activated receptor-2-dependent pathway. Am. J. Physiol. Lung Cell Mol. Physiol. 2006;290:L385–395
  50. Montano RF, Morrison SL. A colorimetric-enzymatic microassay for the quantitation of antibody-dependent complement activation. J. Immunol. Methods. 1999;222:73–82
  51. Moser M, Murphy KM. Dendritic cell regulation of TH1–TH2 development. Nat. Immunol. 2000;1:199–205
  52. Mukherjee P, Pasinetti GM. Complement anaphylatoxin C5a neuroprotects through mitogen-activated protein kinase-dependent inhibition of caspase 3. J. Neurochem. 2001;77:43–49
  53. Murray PJ. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 2006;6:379–386
  54. Nilsson IM, Bremell T, Ryden C, Cheung AL, Tarkowski A. Role of the staphylococcal accessory gene regulator (sar) in septic arthritis. Infect. Immun. 1996;64:4438–4443
  55. Nilsson IM, Lee JC, Bremell T, Ryden C, Tarkowski A. The role of staphylococcal polysaccharide microcapsule expression in septicemia and septic arthritis. Infect. Immun. 1997;65:4216–4221
  56. O'Riordan K, Lee JC. Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev. 2004;17:218–234
  57. Projan SJ, Novick RP. The molecular basis of pathogenicity. In:  Crossley GL,  Archer KB editor. The Staphyloccci in Human Disease. New York, NY: Churchill Livingstone; 1997;p. 55–81
  58. Renno T, Krakowski M, Piccirillo C, Lin JY, Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J. Immunol. 1995;154:944–953
  59. Sandoval A, Ai R, Ostresh JM, Ogata RT. Distal recognition site for classical pathway convertase located in the C345C/netrin module of complement component C5. J. Immunol. 2000;165:1066–1073
  60. Sellebjerg F, Sorensen TL. Chemokines and matrix metalloproteinase-9 in leukocyte recruitment to the central nervous system. Brain Res. Bull. 2003;61:347–355
  61. Sompolinsky D, Samra Z, Karakawa WW, Vann WF, Schneerson R, Malik Z. Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. J. Clin. Microbiol. 1985;22:828–834
  62. Souza LF, Jardim FR, Sauter IP, Souza MM, Barreto F, Margis R, et al. Lipoteichoic acid from Staphylococcus aureus increases matrix metalloproteinase 9 expression in RAW 264.7 macrophages: modulation by A2A and A2B adenosine receptors. Mol Immunol. 2008;
  63. Stenzel W, Soltek S, Miletic H, Hermann MM, Korner H, Sedgwick JD, et al. An essential role for tumor necrosis factor in the formation of experimental murine Staphylococcus aureus-induced brain abscess and clearance. J. Neuropathol. Exp. Neurol. 2005;64:27–36
  64. Stenzel W, Soltek S, Sanchez-Ruiz M, Akira S, Miletic H, Schluter D, et al. Both TLR2 and TLR4 are required for the effective immune response in Staphylococcus aureus-induced experimental murine brain abscess. Am. J. Pathol. 2008;172:132–145
  65. Takemura S, Deguchi M, Ueda M, Yoshida N, Kato H, Yoshikawa T, et al. C3b receptor (CR1) on erythrocytes in various diseases. Immunol. Lett. 1984;7:325–328
  66. Tanga FY, Nutile-McMenemy N, DeLeo JA. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc. Natl. Acad. Sci. U. S. A. 2005;102:5856–5861
  67. Thornton P, Pinteaux E, Allan SM, Rothwell NJ. Matrix metalloproteinase-9 and urokinase plasminogen activator mediate interleukin-1-induced neurotoxicity. Mol. Cell Neurosci. 2008;37:135–142
  68. Townsend GC, Scheld WM. Infections of the central nervous system. Adv. Intern. Med. 1998;43:403–447
  69. Trabucchi E, Radaelli E, Marazzi M, Foschi D, Musazzi M, Veronesi AM, et al. The role of mast cells in wound healing. Int. J. Tissue React. 1988;10:367–372
  70. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003;3:133–146
  71. Tzianabos AO, Wang JY, Lee JC. Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. Proc. Natl. Acad. Sci. U. S. A. 2001;98:9365–9370
  72. Van Beek J, Bernaudin M, Petit E, Gasque P, Nouvelot A, MacKenzie ET, et al. Expression of receptors for complement anaphylatoxins C3a and C5a following permanent focal cerebral ischemia in the mouse. Exp. Neurol. 2000;161:373–382
  73. van Beek J, Elward K, Gasque P. Activation of complement in the central nervous system: roles in neurodegeneration and neuroprotection. Ann. N. Y. Acad Sci. 2003;992:56–71
  74. von Kockritz-Blickwede M, Rohde M, Oehmcke S, Miller LS, Cheung AL, Herwald H, et al. Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am. J. Pathol. 2008;173:1657–1668
  75. Wang YY, Myhre AE, Pettersen SJ, Dahle MK, Foster SJ, Thiemermann C, et al. Peptidoglycan of Staphylococcus aureus induces enhanced levels of matrix metalloproteinase-9 in human blood originating from neutrophils. Shock. 2005;24:214–218
  76. Wynn TA. Cellular and molecular mechanisms of fibrosis. J. Pathol. 2008;214:199–210
  77. Yamaguchi, M., Jadhav, V., Obenaus, A., Colohan, A., Zhang, J.H., 2007. Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery 61, 1067–1075; discussion 1075–1066.
  78. Yamaguchi M, Jadhav V, Obenaus A, Colohan A, Zhang JH. Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery. 2008;

PII: S0165-5728(09)00398-1

doi: 10.1016/j.jneuroim.2009.10.006

Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 83-93 , 25 January 2010

Article Tools

* Image Usage & Resolution