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Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55

H Tilg, E Trehu, MB Atkins, CA Dinarello and JW Mier

Department of Medicine, New England Medical Center, Boston, MA 02111.

The aim of this study was to investigate whether interleukin (IL)-6 induces the production of IL-1 and tumor necrosis factor (TNF) antagonists. Serial plasma samples were obtained from cancer patients participating in phase I and II trials of recombinant IL-6 administered as a 120-hour continuous intravenous (IV) infusion. Plasma IL-1 receptor antagonist (IL-1Ra) and soluble TNF receptor p55 (TNFsRp55) levels were measured by specific radioimmunoassays (RIAs). IL-1Ra levels increased rapidly, reaching peak values (9.6 +/- 1.7 ng/mL) within 2 to 4 hours of beginning treatment. Thereafter, levels promptly declined, reaching near baseline within 24 hours despite continuation of IL-6. TNFsRp55 plasma levels increased within 4 to 8 hours after initiating treatment and increased progressively throughout the duration of therapy. IL-1 beta and TNF-alpha plasma levels were below the detection limit in all samples tested. Peripheral blood mononuclear cells (PBMC) exposed to IL-6 produced only small amounts (1.56 +/- 0.3 ng/mL) of IL-1Ra, even in the presence of exogenous soluble IL-6 receptor (gp80). TNFsRp55 levels measured in the supernatants of IL-6- stimulated PBMC were below the detection limit of the assay. Macrophages generated by culturing monocytes in granulocyte-macrophage colony-stimulating factor (GM-CSF) were much more responsive to IL-6 than freshly isolated unfractionated or adherent PBMC and synthesized almost as much IL-1Ra when stimulated with IL-6 as with endotoxin. These results suggest that the antinflammatory properties of IL-6 may be due; in part, to the induction of IL-1Ra synthesis and the release of soluble TNF receptors. Our findings also suggest that tissue macrophages may be an important source of IL-6-induced IL-1Ra.

Volume 83, Issue 1, pp. 113-118, 01/01/1994
Copyright © 1994 by The American Society of Hematology


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Prostaglandin E2 Selectively Enhances the IgE-Mediated Production of IL-6 and Granulocyte-Macrophage Colony-Stimulating Factor by Mast Cells Through an EP1/EP3-Dependent Mechanism
J. Immunol., December 1, 2000; 165(11): 6545 - 6552.
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J. Immunol.Home page
S. T. Ahmed and L. B. Ivashkiv
Inhibition of IL-6 and IL-10 Signaling and Stat Activation by Inflammatory and Stress Pathways
J. Immunol., November 1, 2000; 165(9): 5227 - 5237.
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J. Immunol.Home page
H. Sasaki, L. Hou, A. Belani, C.-Y. Wang, T. Uchiyama, R. Muller, and P. Stashenko
IL-10, But Not IL-4, Suppresses Infection-Stimulated Bone Resorption In Vivo
J. Immunol., October 1, 2000; 165(7): 3626 - 3630.
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J. Immunol.Home page
J. Wang, R. J. Homer, Q. Chen, and J. A. Elias
Endogenous and Exogenous IL-6 Inhibit Aeroallergen-Induced Th2 Inflammation
J. Immunol., October 1, 2000; 165(7): 4051 - 4061.
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J. Immunol.Home page
S. Hess, H. Smola, U. Sandaradura de Silva, D. Hadaschik, D. Kube, S. E. Baldus, U. Flucke, and H. Pfister
Loss of IL-6 Receptor Expression in Cervical Carcinoma Cells Inhibits Autocrine IL-6 Stimulation: Abrogation of Constitutive Monocyte Chemoattractant Protein-1 Production
J. Immunol., August 15, 2000; 165(4): 1939 - 1948.
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FASEB J.Home page
A. GORNIKIEWICZ, T. SAUTNER, C. BROSTJAN, B. SCHMIERER, R. FÜGGER, E. ROTH, F. MÜHLBACHER, and M. BERGMANN
Catecholamines up-regulate lipopolysaccharide-induced IL-6 production in human microvascular endothelial cells
FASEB J, June 1, 2000; 14(9): 1093 - 1100.
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Am. J. Respir. Cell Mol. Bio.Home page
N. S. Ward, A. B. Waxman, R. J. Homer, L. L. Mantell, O. Einarsson, Y. Du, and J. A. Elias
Interleukin-6-Induced Protection in Hyperoxic Acute Lung Injury
Am. J. Respir. Cell Mol. Biol., May 1, 2000; 22(5): 535 - 542.
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ChestHome page
S. M. Opal and V. A. DePalo
Anti-Inflammatory Cytokines
Chest, April 1, 2000; 117(4): 1162 - 1172.
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J. Immunol.Home page
K. Ohta, B. Wiggert, S. Yamagami, A. W. Taylor, and J. W. Streilein
Analysis of Immunomodulatory Activities of Aqueous Humor from Eyes of Mice with Experimental Autoimmune Uveitis
J. Immunol., February 1, 2000; 164(3): 1185 - 1192.
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Innate ImmunityHome page
L. L. Reznikov, A. J. Puren, G. Fantuzzi, G. R. Hamner, U. S. Schwertschlag, J. L. Ryan, and C. A. Dinarello
Suppression of endotoxin-inducible cytokines in whole blood from human subjects following single dose of recombinant human interleukin-11
Innate Immunity, August 1, 1999; 5(4): 197 - 204.
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Ann Rheum DisHome page
H. Schädlich, J. Ermann, M. Biskop, W. Falk, F. Sperling, A. Jüngel, J. Lehmann, F. Emmrich, and U. Sack
Anti-inflammatory effects of systemic anti-tumour necrosis factor alpha  treatment in human/murine SCID arthritis
Ann Rheum Dis, July 1, 1999; 58(7): 428 - 434.
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EndocrinologyHome page
A. Maret, S. Clamens, I. Delrieu, R. Elhage, J.-F. Arnal, and F. Bayard
Expression of the Interleukin-6 Gene Is Constitutive and Not Regulated by Estrogen in Rat Vascular Smooth Muscle Cells in Culture
Endocrinology, June 1, 1999; 140(6): 2876 - 2882.
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J. Physiol.Home page
K. Ostrowski, T. Rohde, S. Asp, P. Schjerling, and B. K. Pedersen
Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans
J. Physiol., February 15, 1999; 515(1): 287 - 291.
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Am. J. Respir. Crit. Care Med.Home page
I. TILLIE-LEBLOND, J. PUGIN, C.-H. MARQUETTE, C. LAMBLIN, F. SAULNIER, A. BRICHET, B. WALLAERT, A.-B. TONNEL, and P. GOSSET
Balance between Proinflammatory Cytokines and Their Inhibitors in Bronchial Lavage from Patients with Status Asthmaticus
Am. J. Respir. Crit. Care Med., February 1, 1999; 159(2): 487 - 494.
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JEMHome page
S. A. Jones, D. Novick, S. Horiuchi, N. Yamamoto, A. J. Szalai, and G. M. Fuller
C-reactive Protein: A Physiological Activator of Interleukin 6 Receptor Shedding
J. Exp. Med., February 1, 1999; 189(3): 599 - 604.
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Am. J. Respir. Cell Mol. Bio.Home page
T. Hino, H. Nakamura, S. Abe, H. Saito, M. Inage, K. Terashita, S. Kato, and H. Tomoike
Hydrogen Peroxide Enhances Shedding of Type I Soluble Tumor Necrosis Factor Receptor from Pulmonary Epithelial Cells
Am. J. Respir. Cell Mol. Biol., January 1, 1999; 20(1): 122 - 128.
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J. Physiol.Home page
K. Ostrowski, C. Hermann, A. Bangash, P. Schjerling, J. N. Nielsen, and B. K. Pedersen
A trauma-like elevation of plasma cytokines in humans in response to treadmill running
J. Physiol., December 15, 1998; 513(3): 889 - 894.
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J. Immunol.Home page
R. H. van den Berg, M. C. Faber-Krol, R. B. Sim, and M. R. Daha
The First Subcomponent of Complement, C1q, Triggers the Production of IL-8, IL-6, and Monocyte Chemoattractant Peptide-1 by Human Umbilical Vein Endothelial Cells
J. Immunol., December 15, 1998; 161(12): 6924 - 6930.
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BloodHome page
E. Ayroldi, O. Zollo, L. Cannarile, F. D' Adamio, U. Grohmann, D. V. Delfino, and C. Riccardi
Interleukin-6 (IL-6) Prevents Activation-Induced Cell Death: IL-2-Independent Inhibition of Fas/fasL Expression and Cell Death
Blood, December 1, 1998; 92(11): 4212 - 4219.
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J. Immunol.Home page
J.-W. Oh, N. J. Van Wagoner, S. Rose-John, and E. N. Benveniste
Role of IL-6 and the Soluble IL-6 Receptor in Inhibition of VCAM-1 Gene Expression
J. Immunol., November 1, 1998; 161(9): 4992 - 4999.
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Arch. Dis. Child. Fetal Neonatal Ed.Home page
N. Oygür, O. Sönmez, O. Saka, and O. Yegin
Predictive value of plasma and cerebrospinal fluid tumour necrosis factor-alpha and interleukin-1beta concentrations on outcome of full term infants with hypoxic-ischaemic encephalopathy
Arch. Dis. Child. Fetal Neonatal Ed., November 1, 1998; 79(3): 190F - 193.
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Arterioscler. Thromb. Vasc. Bio.Home page
L. Pantoni, C. Sarti, and D. Inzitari
Cytokines and Cell Adhesion Molecules in Cerebral Ischemia : Experimental Bases and Therapeutic Perspectives
Arterioscler Thromb Vasc Biol, April 1, 1998; 18(4): 503 - 513.
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PediatricsHome page
A. Martin-Ancel, A. Garcia-Alix, D. Pascual-Salcedo, F. Cabanas, M. Valcarce, and J. Quero
Interleukin-6 in the Cerebrospinal Fluid After Perinatal Asphyxia Is Related to Early and Late Neurological Manifestations
Pediatrics, November 1, 1997; 100(5): 789 - 794.
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J. Clin. Endocrinol. Metab.Home page
R. DeRijk, D. Michelson, B. Karp, J. Petrides, E. Galliven, P. Deuster, G. Paciotti, P. W. Gold, and E. M. Sternberg
Exercise and Circadian Rhythm-Induced Variations in Plasma Cortisol Differentially Regulate Interleukin-1{beta} (IL-1{beta}), IL-6, and Tumor Necrosis Factor-{alpha} (TNF{alpha}) Production in Humans: High Sensitivity of TNF{alpha} and Resistance of IL-6
J. Clin. Endocrinol. Metab., July 1, 1997; 82(7): 2182 - 2191.
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Ann Rheum DisHome page
A. T MASI and G. P CHROUSOS
Dilemmas of low dosage glucocorticoid treatment in rheumatoid arthritis: considerations of timing
Ann Rheum Dis, January 1, 1997; 56(1): 1 - 4.
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Innate ImmunityHome page
T. van der Poll, C.V. Keogh, D. Helfgott, L. Berman, W.A. Buurman, and S.F. Lowry
Effects of anti-interleukin 6 on inflammatory responses during murine septic peritonitis
Innate Immunity, December 1, 1996; 3(6): 463 - 470.
[Abstract] [PDF]


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StrokeHome page
J. S. Kim, S. S. Yoon, Y. H. Kim, and J. S. Ryu
Serial Measurement of Interleukin-6, Transforming Growth Factor-ß, and S-100 Protein in Patients With Acute Stroke
Stroke, September 1, 1996; 27(9): 1553 - 1557.
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Circ. Res.Home page
T. Kanda, J. E. Wilson McManus, R. Nagai, S. Imai, T. Suzuki, D. Yang, B. M. McManus, and I. Kobayashi
Modification of Viral Myocarditis in Mice by Interleukin-6
Circ. Res., May 1, 1996; 78(5): 848 - 856.
[Abstract] [Full Text]


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Innate ImmunityHome page
P.J.G.M. Steverink, A. Sturk, V.P.M.G. Rutten, J.P.A. Wagenaar-Hilbers, W.R. Klein, M.A. van der Velden, and F. Nemeth
Endotoxin, interleukin-6 and tumor necrosis factor concentrations in equine acute abdominal disease: relation to clinical outcome
Innate Immunity, August 1, 1995; 2(4): 289 - 299.
[Abstract] [PDF]



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