β-(I→3)-D-glucan modulates DNA binding of nuclear factors κB, AT and IL-6 leading to an anti-inflammatory shift of the IL-I β/IL-I receptor antagonist ratio

BMC Immunology

Volumn 7, Issue , 2006, Pages

  Luhm, Juergen ^a   Langenkamp, Ulrich ^a   Hensel, Jenny ^a   Frohn, Christoph ^a   Brand, Joerg M ^a   Hennig, Holger ^a   Rink, Lothar ^a   Koritke, Petra ^a   Wittkopf, Nadine ^a   Williams, David L ^b   Mueller, Antje ^c  

^a UNIVERSITY OF LÜBECK   (Germany)

^b East Tennessee State University   (United States)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,3 GLUCAN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; TOXIC SHOCK SYNDROME TOXIN 1; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR ALPHA; BACTERIAL TOXIN; BETA GLUCAN; BETA-1,3-D-GLUCAN; DNA; ENTEROTOXIN; ENTEROTOXIN F, STAPHYLOCOCCAL; IL1RN PROTEIN, HUMAN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN DERIVATIVE; NFATC2 PROTEIN, HUMAN; SIALOGLYCOPROTEIN; SUPERANTIGEN; TGFB1 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DNA BINDING; HUMAN; HUMAN CELL; IMMUNOMODULATION; LEUKOCYTE FUNCTION; MOLECULAR MECHANICS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROMOTER REGION; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; BINDING SITE; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; CONSENSUS SEQUENCE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; INFLAMMATION; METABOLISM; MONONUCLEAR CELL;

BACTERIAL TOXINS; BETA-GLUCANS; BINDING SITES; CELLS, CULTURED; CONSENSUS SEQUENCE; DNA; DRUG SYNERGISM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENTEROTOXINS; GENE EXPRESSION REGULATION; HUMANS; IMMUNOBLOTTING; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-6; INTERLEUKIN-8; INTERLEUKINS; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIALOGLYCOPROTEINS; SUPERANTIGENS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33744543916     PISSN: 14712172     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-7-5     Document Type: Article

References (57)

1. Bartnicki-Garcia S: Cell wall chemistry, morphogenesis and taxonomy of fungi. Ann Rev Microbial 1968, 22:87-108.
2. Gordon S: Pattern recognition receptors: doubling up for the innate immune response. Cell 2002, 111:927-930.
3. Müller A, Rice PJ, Ensley HE, Coogan PS, Kalbfleisch JH, Kelley JL, Love EJ, Portera CA, Ha T, Browder IW, Williams DL: Receptor binding and internalization of a water-solubie (1→3)-β-D-Glucan biologic response modifier in two monocyte/macrophage cell lines. J Immunol 1996, 156:3418-3425.
4. Rice PJ, Kelley JL, Kogan G, Ensley HE, Kalbfleisch JH, Browder IW, Williams DL: Human monocyte scavenger receptors are pattern recognition receptors for (1→3)-beta-d-glucans. J Leukoc Biol 2002, 72:140-146.
5. Kougias P, Wei D, Rice PJ, Ensley HE, Kalbfleisch J, Williams DL, Browder IW. Normal human fibroblasts express pattern recognition receptors for fungal (1→3)-beta-d-glucans. Infect Immun 2001, 69:3933-3938.
6. Lowe EP, Wei D, Rice PJ, Li C, Kalbfleisch J, Browder IW, Williams DL: Human vascular enclothelial cells express pattern recognition receptors for fungal glucans which stimulates nuclear factor kappaB activation and interleukin 8 production. Am Surg 2002, 68:508-517.
7. Willment JA, Gordon S, Brown GD: Characterisation of the human {beta}-glucan receptor and its alternatively spliced isoforms. J Biol Chem 2001, 276:43818-43823.
8. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SYC, Gordon S: Dectin-I is a major beta-glucan receptor on macrophages. J Exp Med 2002, 196:407-412.
9. Herre J, Gordon S, Brown GD: Dectin-1 and its role in the recognition of β-glucans by macrophages. Mol Immunol 2004, 40:869-876.
10. Herre J, Willment A, Gordon S, Brown GD: The role of Dectin-1 in antifungal immunity. Crit Rev Immunol 2004, 24:193-203.
11. Willment JA, Marshall AS, Reid DM, Williams DL, Wong SY, Gordon S, Brown GD: The human beta-glucan receptor is widely expressed and functionally equivalent to murine dectin-1 on primary cells. Eur J Immunol 2005, 35:1539-1547.
12. Brown GD, Herre J, Williams DL, Willment JA, Marshall ASJ, Gordon S: Dectin-1 mediates the biological effects of β-glucans. J Exp Med 2003, 197:1119-1124.
13. Adams DS, Pero SC, Petro JB, Nathans R, Mackin WM, Wakshull E: PGG-glucan activates NF-κB-like and NF-IL-6-like transcription factor complexes in a murine monocytic cell line. J Leukoc Biol 1997, 62:865-873.
14. Adams DS, Nathans R, Pero SC, Sen A, Wakshull E: Activation of a rel-A/ CEBP-beta-related transcription factor heteromer by PGG-glucan in a murine monocytic cell fine. J Cell Biochem 2000, 77:221-233.
15. Battle J, Ha T, Li C, Della Beffa V, Rice P, Kalbfleisch J, Browder W, Williams D: Ligand binding to the (1→3)-β-D-glucan receptor stimulates NFκB activation but not apoptosis in U937 cells. Biochem Biophys Res Comm 1998, 249:499-504.
16. Wakshull E, Brunke-Reese D, Lindermuth J, Fisette L, Nathans RS, Crowley JJ, Tufts JC, Zimmerman J, Mackin W, Adams DS. PGG-glucan, a soluble beta(1,3)-glucan enhances the oxidative burst response, microbicidal activity, and activates an NF-κB-like factor in human PMN: evidence for a glycosphingolipid β-(1,3)-receptor. Imunophormocal 1999, 41:89-107.
17. Poutsiaka DD, Mengozzi M, Vannier E, Sinha B, Dinarello CA: Cross-linking of the β-glucan receptor on human monocytes results in interleukin-1 receptor antagonist but not interleukin-1 production. Blood 1993, 82:3695-3700.
18. Altstaedt J, Kirchner H, Rink L: Cytokine production of neutrophils is limited to interleukin-8. Immunology 1996, 89:563-568.
19. Engstad CS, Engstad RE, Olsen JO, Osterud B: The effect of soluble beta-1,3-glucan and lipopolysaccharide on cytokine production and coagulation activation in whole blood. Int Immunpharmacol 2002, 2:1585-1897.
20. Williams DL, McNamee RB, Jones EL, Pretus HA, Ensley HE, Browder IW, Di Luzio NR: A method for the solubilization of a (1-3)-β-D-glucan isolated from Saccharomyces cerevisiae. Carbohydr Res 1991, 219:203-213.
21. Williams DL, Ha T, Li C, Kalbfleisch JH, Laffan JJ, Ferguson DA: Inhibiting early activation of tissue nuclear factor-kappa B and nuclear factor interleukin 6 with (1→3)-beta-D-glucan increases long-term survival in polymicrobial sepsis. Surgery 1999, 126:54-65.
22. Williams DL, Li C, Ha T, Ozment-Skelton T, Kalbfleisch JH, Preiszner J, Brooks L, Breuel K, Schweitzer JB: Modulation of the phosphoinositide 3-kinase pathway alters innate resistance to polymicrobial sepsis. J Immunol 2004, 172:449-456.
23. Soltys J, Quinn MT: Modulation of endotoxin- and enterotoxin-induced cytokine release by in vivo treatment with β-(1,6)-branched β-(1,3)-glucan. Infect Immun 1999, 67:244-252.
24. Masihi KN, Madaj K, Hintelman H, Gast G, Kaneko Y: Down-regulation of tumor necrosis factor-α, moderate reduction of interleukin-1β, but not interleukin-6 or interleukin-10, by glucan immunomodulators curdlan sulfate and lentinan. Int J Immunopharmac 1997, 19:463-468.
25. Browder W, Williams D, Pretus H, Olivero G, Enrichens F, Mao P, Franchello A: Beneficial effect of enhanced macrophage function in the trauma patient. Ann Surg 1990, 211:605-613.
26. Lowman D, Ensley H, Williams D: Identification of phosphate substitution sites by NMR spectroscopy in a water-soluble phosphorylated (1→3)-β-D-glucan. Carbohydr Res 1998, 306:559-562.
27. Trede NS, Tsytsykova AV, Chatila T, Goldfeld AE, Geha RS: Transcriptional activation of the human TNF-α promoter by superantigen in human monocytic cells. J Immunol 1995, 155:902-908.
28. Schulte R, Grassl GA, Preger S, Fessele S, Jacobi CA, Schaller M, Nelson PJ, Autenrieth IB: Yersinia enterocolitica Invasin protein triggers IL-8 production in epithelial cells via activation of Rel p65-p65 homodimers. FASEB J 2000, 14:1471-1484.
29. Campbell PM, Pimm J, Ramassar V, Halloran PF: Identification of a calcium-inducible cyclosporine-sensitive element in the IFNγ promoter that is a potential NFAT binding site. Transplantation 1996, 61:933-939.
30. Smith Jr MF, Eidlen D, Arend WP, Gutierrez-Hartmann A: LPS-induced expression of the human IL-1 receptor antagonist gene is controlled by multiple interacting promoter elements. J Immunol 1994, 153:3584-3593.
31. Godambe SA, Chaplin DD, Takova T, Bellone CJ: Upstream NFIL-6-like site located within a DNase I hypersensitivity region mediates LPS-induced transcription of the murine interleukin-1β gene. J Immunol 1994, 153:143-152.
32. Lennard AC: Interleukin-1 receptor antagonist. Crit Rev Immunol 1995, 15:77-105.
33. Smith Jr MF, Carl VS, Lodie T, Fenton MJ: Secretory interleukin-I receptor antagonist gene expression requires both a PU. 1 and a novel composite NF-κB/PU. 1/GA-binding protein binding site. J Biol Chem 1998, 273:24272-24279.
34. Hennig H, Luhm J, Hartwig D, Klüter H, Kirchner H: A novel RT-PCR for reliable and rapid HCV RNA screening of blood donations. Transfusion 2001, 41:1100-1106.
35. Natarajan K, Singh S, Burke Jr TR, Grunberger D, Aggarwal BB: Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κB. Proc Natl Acad Sci 1996, 93:9090-9095.
36. Schwaninger M, Petersen N, Prinz S, Sallmann S, Neher M, Spranger M: Adenosine-induced expression of interleukin-6 in astrocytes through protein kinase A and NF-IL-6. Glia 2000, 31:51-58.
37. Li C, Ha T, Kelley J, Gao X, Qiu Y, Kao RL, Browder IW, Williams DL: Modulating Toll-like receptor mediated signaling by (1→3)-β-D-glucan rapidly induces cardioprotection. Cardiovascular Res 2004, 61:538-547.
38. Hogan PG, Chen L, Nardone J, Rao A: Transcriptional regulation by calcium, calcineurin, and NFAT. Genes & Development 2003, 17:2205-2232.
39. Kunsch C, Lang RK, Rosen CA, Shannon MF: Synergistic transcriptional activation of the IL-8 gene by NF-κB p65 (ReIA) and NF-IL-6. J Immunol 1994, 153:153-164.
40. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, Ways JP, Gray JG: NF-κB regulates IL-1β transcription through a consensus NF-κB binding site and a nonconsensus CRE-like site. J Immunol 1994, 153:712-723.
41. Perkins ND, Schmid RM, Duckett CS, Leung K, Rice NR, Nabel GJ: Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc Natl Acad Sci 1992, 89:1529-1533.
42. Zabel U, Schreck R, Baeuerle PA. DNA binding of purified transcription factor NF-κB. J Biol Chem 1991, 266:252-260.
43. Guha M, Mackman N: The phosphatidylinositol 3-Kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 2002, 277:32124-32132.
44. Ramirez M, Fernandez-Troy N, Buxade M, Casaroli-Marano RP, Benitez D, Perez-Maldonado C, Espel E: Wortmannin inhibits translation of tumor necrosis factor-α in superantigen-activated T cells. Int Immunol 1999, 11:1479-1489.
45. Kum WWS, Cameron SB, Hung RWY, Kalyan S, Chow AW: Temporal sequence and kinetics of proinflammatory and anti-inflammatory cytokine secretion induced by toxic shock syndrome toxin 1 in human periperal blood mononuclear cells. Infect Immun 2001, 69:7544-7549.
46. Knop J, Martin MU: Effects of IL-1 receptor-associated kinase (IRAK) expression on IL-1 signaling are independent of its kinase activity. FEBS letters 1999, 448:81-85.
47. Yang Y, Bin W, Aksoy MC, Kelsen SG: Regulation of interleukin-1 beta and interleukin-1 beta inhibitor release by human airway epithelial cells. Eur Respir J 2004, 24:360-366.
48. Learn CA, Boger MS, Li L, McCall CE: The phosphatidylinositol 3-Kinase Pathway selectively controls sIL- 1RA not interleukin-1β production in the septic leukocyte. J Biol Chem 2001, 276:20234-20239.
49. Jascur T, Gilman J, Mustelin T: Involvement of phosphatidylinositol 3-kinase in NFAT activation in T cells. J Biol Chem 1997, 272:14483-14488.
50. Zhu Y, Culmsee C, Klumpp S, Krieglstein J: Neuroprotection by transforming growth factor-beta 1 involves activation of nuclear factor-kappaB through phosphatidylinositol-3-OH kinase/Akt and mitogen-activated protein kinase-extracellular-signal regulated kinase 1,2 signaling pathways. Neuroscience 2004, 123:897-906.
51. Carl VS, Brown-Steinke K, Nicklin MJH, Smith Jr MF: Toll-like receptor 2 and 4 (TLR2 and TLR4) agonists differentially regulate secretory Interleukin-1 receptor antagonist gene expression in macrophages. J Biol Chem 2002, 277:17448-17456.
52. Dinarello CA: The role of the interleukin-1-receptor antagonist in blocking inflammation mediated by interleukin 1. New Engl J Med 2000, 343:732-734.
53. Rupp J, Kothe H, Müller A, Maass M, Dahlhoff K: Imbalanced secretion of IL-1β and IL-1RA in C. pneumoniae -infected mononuclear cells from COPD patients. Eur Resp J 2003, 22:274-279.
54. Luhm J, Kirchner H, Rink L: One-way synergistic effect of low superantigen concentrations on lipopolysaccharide-induced cytokine production. J Interf Cytoki Res 1997, 17:229-238.
55. Luhm J, Schromm AB, Seydel U, Brandenburg K, Wellinghausen N, Riedel E, Schumann RR, Rink L: Hypothermia enhances the biological activity of lipopolysaccharide by altering its fluidity state. Eur J Biochem 1998, 256:325-333.
56. Brand JM, Frohn C, Cziupka K, Brockmann C, Kirchner H, Luhm J: Prolactin triggers pro-inflammatory immune responses in peripheral immune cells. Eur Cytokine Netw 2004, 15:99-104.
57. 2 in human blood samples by ELISA. J Immunol Methods 1995, 184:263-271.