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Differences in lipopolysaccharide- and lipoteichoic acid-induced cytokine/chemokine expressionOpen access

Simon J. Finney| Susannah K. Leaver| Timothy W. Evans| Anne Burke-Gaffney
Experimental
Volume 38, Issue 2 / February , 2012

Pages 324 - 332

Abstract

Purpose

To investigate differences in cytokine/chemokine release in response to lipoteichoic acid (LTA) or lipopolysaccharide (LPS) and contributing cellular mechanisms, in order to improve understanding of the pathogenesis of sepsis.

Methods

Levels of cytokines/chemokines were measured in plasma and peritoneal lavage fluid of 10-week-old male mice (C57/B16) following intraperitoneal injection of LTA or LPS (250 µg), and in supernatants of murine J774.2 cells, immortalised blood monocytes, or isolated human monocytes treated with LTA or LPS (0–10 µg/ml). The role of cytokine/chemokine messenger RNA (mRNA) stability versus nuclear factor-kappaB (NF-κB) and activator protein-1 (AP-1) in mediating cytokine/chemokine release in J774 cells was also assessed.

Results

In mice, plasma levels of keratinocyte-derived chemokine (KC), macrophage inflammatory protein (MIP)-2, interleukin (IL)-10, interferon (IFN)-γ and tumour necrosis factor-alpha (TNF-α) and peritoneal lavage fluid levels of KC, MIP-2 and TNF-α increased significantly 1 h after LPS. Only KC and MIP-2 levels increased 1 h after LTA. LPS-treated (10 μg/ml) J774 cells released MIP-2, IL-10, IFN-γ and TNF-α but not KC (24 h), whereas cells treated with 10 μg/ml LTA released only MIP-2. LPS-stimulated human monocytes released IL-10 and IL-8 (24 h); by contrast, LTA-treated cells released only IL-8. LPS and LTA activated NF-κB and AP-1 in J774 cells. The protein synthesis inhibitor cycloheximide abolished LPS-induced IL-10 mRNA expression and increased LTA- and LPS-induced mRNA for MIP-2 in J774 cells.

Conclusion

LTA and LPS, at clinically relevant concentrations, induced differential cytokine/chemokine release in vitro and in vivo, via effects distal to activation of NF-κB/AP-1 that might include chromatin remodelling or mRNA stability.

Keywords

References

  1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303–1310
    • View reference on PubMed
    • View reference on publisher's website
  2. Zanotti S, Kumar A (2002) Cytokine modulation in sepsis and septic shock. Expert Opin Investig Drugs 11:1061–1075
    • View reference on PubMed
    • View reference on publisher's website
  3. Fisher CJ Jr, Agosti JM, Opal SM, Lowry SF, Balk RA, Sadoff JC, Abraham E, Schein RM, Benjamin E (1996) Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The soluble TNF receptor sepsis study group. N Engl J Med 334:1697–1702
    • View reference on PubMed
    • View reference on publisher's website
  4. Moreno RP, Metnitz B, Adler L, Hoechtl A, Bauer P, Metnitz PG (2008) Sepsis mortality prediction based on predisposition, infection and response. Intensive Care Med 34:496–504
  5. Feezor RJ, Oberholzer C, Baker HV, Novick D, Rubinstein M, Moldawer LL, Pribble J, Souza S, Dinarello CA, Ertel W, Oberholzer A (2003) Molecular characterization of the acute inflammatory response to infections with gram-negative versus gram-positive bacteria. Infect Immun 71:5803–5813
    • View reference on PubMed
    • View reference on publisher's website
  6. Lorne E, Dupont H, Abraham E (2010) Toll-like receptors 2 and 4: initiators of non-septic inflammation in critical care medicine? Intensive Care Med 36:1826–1835
  7. Markham JL, Knox KW, Wicken AJ, Hewett MJ (1975) Formation of extracellular lipoteichoic acid by oral streptococci and lactobacilli. Infect Immun 12:378–386
    • View reference on PubMed
  8. van Langevelde P, van Dissel JT, Ravensbergen E, Appelmelk BJ, Schrijver IA, Groeneveld PH (1998) Antibiotic-induced release of lipoteichoic acid and peptidoglycan from Staphylococcus aureus: quantitative measurements and biological reactivities. Antimicrob Agents Chemother 42:3073–3078
    • View reference on PubMed
  9. Leemans JC, Vervoordeldonk MJ, Florquin S, van Kessel KP, van der Poll T (2002) Differential role of interleukin-6 in lung inflammation induced by lipoteichoic acid and peptidoglycan from Staphylococcus aureus. Am J Respir Crit Care Med 165:1445–1450
    • View reference on PubMed
    • View reference on publisher's website
  10. van Zoelen MA, de Vos AF, Larosa GJ, Draing C, von Aulock S, van der Poll T (2007) Intrapulmonary delivery of ethyl pyruvate attenuates lipopolysaccharide- and lipoteichoic acid-induced lung inflammation in vivo. Shock 28:570–575
    • View reference on PubMed
  11. Draing C, Sigel S, Deininger S, Traub S, Munke R, Mayer C, Hareng L, Hartung T, von Aulock S, Hermann C (2008) Cytokine induction by gram-positive bacteria. Immunobiology 213:285–296
    • View reference on PubMed
    • View reference on publisher's website
  12. Manthey CL, Perera PY, Henricson BE, Hamilton TA, Qureshi N, Vogel SN (1994) Endotoxin-induced early gene expression in C3H/HeJ (Lpsd) macrophages. J Immunol 153:2653–2663
    • View reference on PubMed
  13. Finney SJ, Anning PB, Cao TV, Perretti M, Evans TW, Burke-Gaffney A (2007) Butanol-extracted lipoteichoic acid induces in vivo leukocyte adhesion. Biochem Biophys Res Commun 364:831–837
    • View reference on PubMed
    • View reference on publisher's website
  14. Morath S, Stadelmaier A, Geyer A, Schmidt RR, Hartung T (2002) Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 195:1635–1640
    • View reference on PubMed
    • View reference on publisher's website
  15. Baydoun AR, Bogle RG, Pearson JD, Mann GE (1993) Selective inhibition by dexamethasone of induction of NO synthase, but not of induction of l-arginine transport, in activated murine macrophage J774 cells. Br J Pharmacol 110:1401–1406
    • View reference on PubMed
  16. Delgado M, Ganea D (2001) Inhibition of endotoxin-induced macrophage chemokine production by VIP and PACAP in vitro and in vivo. Arch Physiol Biochem 109:377–382
    • View reference on PubMed
  17. Koay MA, Christman JW, Segal BH, Venkatakrishnan A, Blackwell TR, Holland SM, Blackwell TS (2001) Impaired pulmonary NF-kappaB activation in response to lipopolysaccharide in NADPH oxidase-deficient mice. Infect Immun 69:5991–5996
    • View reference on PubMed
    • View reference on publisher's website
  18. Cheng SS, Lukacs NW, Kunkel SL (2002) Eotaxin/CCL11 is a negative regulator of neutrophil recruitment in a murine model of endotoxemia. Exp Mol Pathol 73:1–8
    • View reference on PubMed
    • View reference on publisher's website
  19. Hoogerwerf JJ, de Vos AF, Bresser P, van der Zee JS, Pater JM, de Boer A, Tanck M, Lundell DL, Her-Jenh C, Draing C, von Aulock S, van der Poll T (2008) Lung inflammation induced by lipoteichoic acid or lipopolysaccharide in humans. Am J Respir Crit Care Med 178:34–41
    • View reference on PubMed
    • View reference on publisher's website
  20. Hermann C, Spreitzer I, Schroder NW, Morath S, Lehner MD, Fischer W, Schutt C, Schumann RR, Hartung T (2002) Cytokine induction by purified lipoteichoic acids from various bacterial species–role of LBP, sCD14, CD14 and failure to induce IL-12 and subsequent IFN-gamma release. Eur J Immunol 32:541–551
    • View reference on PubMed
    • View reference on publisher's website
  21. Yamamoto S, Tin Tin Win S, Ahmed S, Kobayashi T, Fujimaki H (2006) Effect of ultrafine carbon black particles on lipoteichoic acid-induced early pulmonary inflammation in BALB/c mice. Toxicol Appl Pharmacol 213:256–266
    • View reference on PubMed
    • View reference on publisher's website
  22. Knapp S, von Aulock S, Leendertse M, Haslinger I, Draing C, Golenbock DT, van der Poll T (2008) Lipoteichoic acid-induced lung inflammation depends on TLR2 and the concerted action of TLR4 and the platelet-activating factor receptor. J Immunol 180:3478–3484
    • View reference on PubMed
  23. Jiao YL, Wu MP (2008) Apolipoprotein A-I diminishes acute lung injury and sepsis in mice induced by lipoteichoic acid. Cytokine 43:83–87
    • View reference on PubMed
    • View reference on publisher's website
  24. McDonald PP, Fadok VA, Bratton D, Henson PM (1999) Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J Immunol 163:6164–6172
    • View reference on PubMed
  25. Bozic CR, Kolakowski LF Jr, Gerard NP, Garcia-Rodriguez C, von Uexkull-Guldenband C, Conklyn MJ, Breslow R, Showell HJ, Gerard C (1995) Expression and biologic characterization of the murine chemokine KC. J Immunol 154:6048–6057
    • View reference on PubMed
  26. Daly KA, Mailer SL, Digby MR, Lefevre C, Thomson P, Deane E, Nicholas KR, Williamson P (2009) Molecular analysis of tammar (Macropus eugenii) mammary epithelial cells stimulated with lipopolysaccharide and lipoteichoic acid. Vet Immunol Immunopathol 129:36–48
    • View reference on PubMed
    • View reference on publisher's website
  27. Kimbrell MR, Warshakoon H, Cromer JR, Malladi S, Hood JD, Balakrishna R, Scholdberg TA, David SA (2008) Comparison of the immunostimulatory and proinflammatory activities of candidate gram-positive endotoxins, lipoteichoic acid, peptidoglycan, and lipopeptides, in murine and human cells. Immunol Lett 118:132–141
    • View reference on PubMed
    • View reference on publisher's website
  28. Jones KJ, Perris AD, Vernallis AB, Worthington T, Lambert PA, Elliott TS (2005) Induction of inflammatory cytokines and nitric oxide in J774.2 cells and murine macrophages by lipoteichoic acid and related cell wall antigens from Staphylococcus epidermidis. J Med Microbiol 54:315–321
    • View reference on PubMed
    • View reference on publisher's website
  29. Stich AN, DeClue AE (2011) Pathogen associated molecular pattern-induced TNF, IL-1beta, IL-6 and CXCL-8 production from feline whole blood culture. Res Vet Sci 90:59–63
    • View reference on PubMed
    • View reference on publisher's website
  30. Hessle C, Andersson B, Wold AE (2000) Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL-12) while gram-negative bacteria preferentially stimulate IL-10 production. Infect Immun 68:3581–3586
    • View reference on PubMed
    • View reference on publisher's website
  31. Wang JE, Jorgensen PF, Almlof M, Thiemermann C, Foster SJ, Aasen AO, Solberg R (2000) Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor alpha, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect Immun 68:3965–3970
    • View reference on PubMed
    • View reference on publisher's website
  32. Bjerre A, Brusletto B, Hoiby EA, Kierulf P, Brandtzaeg P (2004) Plasma interferon-gamma and interleukin-10 concentrations in systemic meningococcal disease compared with severe systemic gram-positive septic shock. Crit Care Med 32:433–438
    • View reference on PubMed
    • View reference on publisher's website
  33. Mandrekar P, Bala S, Catalano D, Kodys K, Szabo G (2009) The opposite effects of acute and chronic alcohol on lipopolysaccharide-induced inflammation are linked to IRAK-M in human monocytes. J Immunol 183:1320–1327
    • View reference on PubMed
    • View reference on publisher's website
  34. Zhao Y, Chen LH (2005) Eicosapentaenoic acid prevents lipopolysaccharide-stimulated DNA binding of activator protein-1 and c-Jun N-terminal kinase activity. J Nutr Biochem 16:78–84
    • View reference on PubMed
    • View reference on publisher's website
  35. Tang CH, Hsu CJ, Yang WH, Fong YC (2010) Lipoteichoic acid enhances IL-6 production in human synovial fibroblasts via TLR2 receptor, PKCdelta and c-Src dependent pathways. Biochem Pharmacol 79:1648–1657
    • View reference on PubMed
    • View reference on publisher's website
  36. Kim DS, Han JH, Kwon HJ (2003) NF-kappaB and c-Jun-dependent regulation of macrophage inflammatory protein-2 gene expression in response to lipopolysaccharide in RAW 264.7 cells. Mol Immunol 40:633–643
    • View reference on PubMed
    • View reference on publisher's website
  37. Albrecht I, Tapmeier T, Zimmermann S, Frey M, Heeg K, Dalpke A (2004) Toll-like receptors differentially induce nucleosome remodelling at the IL-12p40 promoter. EMBO Rep 5:172–177
    • View reference on PubMed
    • View reference on publisher's website
  38. Blease K, Chen Y, Hellewell PG, Burke-Gaffney A (1999) Lipoteichoic acid inhibits lipopolysaccharide-induced adhesion molecule expression and IL-8 release in human lung microvascular endothelial cells. J Immunol 163:6139–6147
    • View reference on PubMed

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