Journal of Experimental Medicine, Vol 174, 1209-1220, Copyright © 1991 by Rockefeller University Press

ARTICLES

Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes

R de Waal Malefyt, J Abrams, B Bennett, CG Figdor and JE de Vries
Department of Human Immunology, DNAX Research Institute, Palo Alto, California 94304.

In the present study we demonstrate that human monocytes activated by lipopolysaccharides (LPS) were able to produce high levels of interleukin 10 (IL-10), previously designated cytokine synthesis inhibitory factor (CSIF), in a dose dependent fashion. IL-10 was detectable 7 h after activation of the monocytes and maximal levels of IL-10 production were observed after 24-48 h. These kinetics indicated that the production of IL-10 by human monocytes was relatively late as compared to the production of IL-1 alpha, IL-1 beta, IL-6, IL-8, tumor necrosis factor alpha (TNF alpha), and granulocyte colony-stimulating factor (G-CSF), which were all secreted at high levels 4-8 h after activation. The production of IL-10 by LPS activated monocytes was, similar to that of IL-1 alpha, IL-1 beta, IL-6, IL-8, TNF alpha, granulocyte-macrophage colony-stimulating factor (GM-CSF), and G-CSF, inhibited by IL-4. Furthermore we demonstrate here that IL-10, added to monocytes, activated by interferon gamma (IFN-gamma), LPS, or combinations of LPS and IFN-gamma at the onset of the cultures, strongly inhibited the production of IL-1 alpha, IL-1 beta, IL-6, IL-8, TNF alpha, GM-CSF, and G-CSF at the transcriptional level. Viral-IL-10, which has similar biological activities on human cells, also inhibited the production of TNF alpha and GM-CSF by monocytes following LPS activation. Activation of monocytes by LPS in the presence of neutralizing anti-IL-10 monoclonal antibodies resulted in the production of higher amounts of cytokines relative to LPS treatment alone, indicating that endogenously produced IL-10 inhibited the production of IL-1 alpha, IL-1 beta, IL-6, IL-8, TNF alpha, GM-CSF, and G-CSF. In addition, IL-10 had autoregulatory effects since it strongly inhibited IL-10 mRNA synthesis in LPS activated monocytes. Furthermore, endogenously produced IL-10 was found to be responsible for the reduction in class II major histocompatibility complex (MHC) expression following activation of monocytes with LPS. Taken together our results indicate that IL-10 has important regulatory effects on immunological and inflammatory responses because of its capacity to downregulate class II MHC expression and to inhibit the production of proinflammatory cytokines by monocytes.
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• Jeschke, M. G., Klein, D., Bolder, U., Einspanier, R. (2004). Insulin Attenuates the Systemic Inflammatory Response in Endotoxemic Rats. Endocrinology 145: 4084-4093 [Abstract] [Full Text]  
• Steinke, J. W., Barekzi, E., Hagman, J., Borish, L. (2004). Functional Analysis of -571 IL-10 Promoter Polymorphism Reveals a Repressor Element Controlled by Sp1. J. Immunol. 173: 3215-3222 [Abstract] [Full Text]  
• Deng, J., Muthu, K., Gamelli, R., Shankar, R., Jones, S. B. (2004). Adrenergic modulation of splenic macrophage cytokine release in polymicrobial sepsis. Am. J. Physiol. Cell Physiol. 287: C730-C736 [Abstract] [Full Text]  
• Kurreeman, F. A.S., Schonkeren, J. J.M., Heijmans, B. T., Toes, R. E.M., Huizinga, T. W.J. (2004). Transcription of the IL10 gene reveals allele-specific regulation at the mRNA level. Hum Mol Genet 13: 1755-1762 [Abstract] [Full Text]  
• Kurte, M., Lopez, M., Aguirre, A., Escobar, A., Aguillon, J. C., Charo, J., Larsen, C. G., Kiessling, R., Salazar-Onfray, F. (2004). A Synthetic Peptide Homologous to Functional Domain of Human IL-10 Down-Regulates Expression of MHC Class I and Transporter Associated with Antigen Processing 1/2 in Human Melanoma Cells. J. Immunol. 173: 1731-1737 [Abstract] [Full Text]  
• Beiting, D. P., Bliss, S. K., Schlafer, D. H., Roberts, V. L., Appleton, J. A. (2004). Interleukin-10 Limits Local and Body Cavity Inflammation during Infection with Muscle-Stage Trichinella spiralis. Infect. Immun. 72: 3129-3137 [Abstract] [Full Text]  
• Yokoyama, Y., Kitchens, W. C., Toth, B., Schwacha, M. G., Rue, L. W. III, Bland, K. I., Chaudry, I. H. (2004). Role of IL-10 in regulating proinflammatory cytokine release by Kupffer cells following trauma-hemorrhage. Am. J. Physiol. Gastrointest. Liver Physiol. 286: G942-G946 [Abstract] [Full Text]  
• Dalbeth, N, Yeoman, S, Dockerty, J L, Highton, J, Robinson, E, Tan, P L, Herman, D, McQueen, F M (2004). A randomised placebo controlled trial of delipidated, deglycolipidated Mycobacterium vaccae as immunotherapy for psoriatic arthritis. Ann Rheum Dis 63: 718-722 [Abstract] [Full Text]  
• Skapenko, A., Niedobitek, G. U., Kalden, J. R., Lipsky, P. E., Schulze-Koops, H. (2004). Generation and Regulation of Human Th1-Biased Immune Responses In Vivo: A Critical Role for IL-4 and IL-10. J. Immunol. 172: 6427-6434 [Abstract] [Full Text]  
• Tang, N., Liu, L., Kang, K., Mukherjee, P. K., Takahara, M., Chen, G., McCormick, T. S., Cooper, K. D., Ghannoum, M. (2004). Inhibition of Monocytic Interleukin-12 Production by Candida albicans via Selective Activation of ERK Mitogen-Activated Protein Kinase. Infect. Immun. 72: 2513-2520 [Abstract] [Full Text]  
• Kirkley, J. E., Robey, F. A. (2004). Inhibition of U937 Cytokine Secretion by HIV-1 gp120 C4-Derived Peptide Constructs. Journal of Bioactive and Compatible Polymers 19: 173-195 [Abstract]  
• Scumpia, P. O., Sarcia, P. J., Kelly, K. M., DeMarco, V. G., Skimming, J. W. (2004). Hypothermia Induces Anti-Inflammatory Cytokines and Inhibits Nitric Oxide and Myeloperoxidase-Mediated Damage in the Hearts of Endotoxemic Rats. Chest 125: 1483-1491 [Abstract] [Full Text]  

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