IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages

European Journal of Immunology

Volumn 28, Issue 1, 1998, Pages 359-369

  Allavena, Paola ^a   Piemonti, Lorenzo ^a   Longoni, Daniela ^a,d   Bernasconi, Sergio ^a   Stoppacciaro, Antonella ^b   Ruco, Luigi ^b   Mantovani, Alberto ^a,c  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF BRESCIA   (Italy)

^d SAN GERARDO HOSPITAL   (Italy)

Author keywords

Antigen presenting cell; Dendritic cell; IL 10

Indexed keywords

CD1 ANTIGEN; CD14 ANTIGEN; CD16 ANTIGEN; CD68 ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NONSPECIFIC ESTERASE; TETANUS TOXIN;

ANTIGEN PRESENTATION; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; DENDRITIC CELL; DOSE RESPONSE; ENDOCYTOSIS; HUMAN; HUMAN CELL; MACROPHAGE; MIXED LYMPHOCYTE REACTION; MONOCYTE; PRIORITY JOURNAL; T LYMPHOCYTE; UMBILICAL CORD BLOOD;

ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HLA-D ANTIGENS; HUMANS; INTERLEUKIN-10; INTERLEUKIN-13; LYMPHOCYTE CULTURE TEST, MIXED; MACROPHAGES; MONOCYTES; RECOMBINANT PROTEINS;

EID: 0031974687     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199801)28:01<359::AID-IMMU359>3.0.CO;2-4     Document Type: Article

References (44)

1. Steinman, R. M., The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 1991. 9: 271-296.
2. Caux, C., Liu, Y. J. and Banchereau, J., Recent advances in the study of dendritic cells and follicular dendritic cells. Immunol. Today 1995. 16: 2-4.
3. Girolomoni, G. and Ricciardi-Castagnoli, P., Dendritic cells hold promise for immunotherapy. Immunol. Today 1997. 18: 102-104.
4. Cella, M., Sallusto, F. and Lanzavecchia, A., Origin, maturation and antigen presenting function of dendritic cells. Curr. Opin. Immunol. 1997. 9: 10-16.
5. McWilliam, A. S., Nelson, D., Thomas, J. A. and Holt, P. G., Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J. Exp. Med. 1994. 179: 1331-1336.
6. Macpherson, G. G., Jenkins, C. D., Stein, M. J. and Edwards, C., Endotoxin-mediated dendritic cell release from the intestine - Characterization of released dendritic cells and TNF dependence. J. Immunol. 1995. 154: 1317-1322.
7. Caux, C., Massacrier, C., Vanbervliet, B., Dubois, B., Vankooten, C., Durand, I. and Banchereau, J., Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 1994. 180: 1263-1272.
8. Sallusto, F. and Lanzavecchia, A., Efficient Presentation of Soluble Antigen by Cultured Human Dendritic Cells Is Maintained by Granulocyte/Macrophage Colony-Stimulating Factor Plus Interleukin-4 and Downregulated by Tumor Necrosis Factor-alpha. J. Exp. Med. 1994. 179: 1109-1118.
9. Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A., Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: Downregulation by cytokines and bacterial products. J. Exp. Med. 1995. 182: 389-400.
10. Caux, C., Dezutter-Dambuyant, C., Schmitt, D. and Banchereau, J., GM-CSF and TNF-α cooperate in the generation of dendritic Langerhans cells. Nature 1992. 360: 258-261.
11. Rosenzwajg, M., Canque, B. and Gluckman, J. C., Human dendritic cell differentiation pathway from CD34(+) hematopoietic precursor cells. Blood 1996. 87: 535-544.
12. Mackensen, A., Herbst, B., Kohler, G., Wolffvorbeck, G., Rosenthal, F. M., Veelken, H., Kulmburg, P., Schaefer, H. E., Mertelsmann, R. and Lindemann, A., Delineation of the dendritic cell lineage by generating large numbers of Birbeck granule-positive Langerhans cells from human peripheral blood progenitor cells in vitro. Blood 1995. 86: 2699-2707.
13. Peters, J. H., Gieseler, R., Thiele, B. and Steinbach, F., Dendritic cells: from ontogenetic orphans to myelomonocyteic descendants, Immunol. Today 1996. 17: 273-278.
14. Romani, N., Gruner, S., Brang, D., Kampgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M. and Schuler, G., Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 1994. 180: 83-93.
15. Caux, C., Vanberliet, B., Massacrier, C., Dezutter-Dambuyant, C., de Saint-Vis, B., Jacquet, C., Yoneda, K., Imamura, S., Schmitt, D. and Banchereau, J., CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF-α. J. Exp. Med. 1996. 184: 695-706.
16. + dendritic cells. Proc. Natl. Acad. Sci. USA 1996. 93: 2588-2592.
17. Kiertscher, S. M. and Roth, M. D., Human CD14+ leukocytes acquire the phenotype and function of antigen-presenting dendritic cells when cultured in GM-CSF and IL-4. J. Leukocyte Biol. 1996. 59: 208-218.
18. Piemonti, L., Bernasconi, S., Luini, W., Trobonjaca, Z., Minty, A., Allavena, P. and Mantovani, A., IL-13 supports differentiation of dendritic cells from circulating precursors in concert with GM-CSF. Eur. Cytokine Network 1995. 6: 245-252.
19. Mosmann, T. R., Properties and functions of interleukin-10. Adv. Immunol. 1994. 56: 1-26.
20. de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G. and de Vries, J. E., Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 1991. 174: 1209-1220.
21. Ding, L., Linsley, P. S., Huang, L. Y., Germain, R. N. and Shevach, E. M., IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 1993. 151: 1224-1234.
22. de Waal Malefyt, R., Haanen, J., Spits, H., Roncarolo, M. G., te Velde, A., Figdor, C., Johnson, K., Kastelein, R., Yssel, H. and de Vries, J. E., Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 1991. 174: 915-924.
23. Fiorentino, D. F., Zlotnik, A., Mosmann, T. R., Howard, M. and O'Garra, A., IL-10 inbitis cytokine production by activated macrophages. J. Immunol. 1991. 147: 3815-3822.
24. Chang, C. H., Furue, M. and Tamaki, K., B7-1 expression of Langerhans cells is up-regulated by proinflammatory cytokines, and is down-regulated by interferon-gamma or by interleukin-10. Eur. J. Immunol. 1995. 25: 394-398.
25. Buelens, C., Willems, F., Delvaux, A., Pierard, G., Delville, J. P., Velu, T. and Goldman, M., Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur J. Immunol. 1995. 25: 2668-2672.
26. Beissert, S., Hosoi, J., Grabbe, S., Asahina, A. and Granstein, R. D., IL-10 inhibits tumor antigen presentation by epidermal antigen-presenting cells. J. Immunol. 1995. 154: 1280-1286.
27. Koch, F., Stanzl, U., Jennewein, P., Janke, K., Heufler, C., Kampgen, E., Romani, N. and Schuler, G., High levels IL-12 production by murine dendritic cells: up-regulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 1996. 184: 747-752.
28. Thomssen, H., Kahan, M. and Londei, M., Differential effects of interleukin-10 on the expression of HLA class II and CD1 molecules induced by granulocyte/macrophage colony-stimulating factor/interleukin-4. Eur. J. Immunol. 1995. 25: 2465-2470.
29. De Smedt, T., Van Mchelen, M.E., De Becker, G., Urbain, J., Leo, O. and Moser, M., Effect of interleukin-10 on dendritic cell maturation and function. Eur. J. Immunol. 1997. 27: 1229-1235.
30. Buelens, C., Verhasselt, V., De Groote, D., Thielemans, K., Goldman, M. and Willems, F., Interleukin-10 prevents the generation of dendritic cells from human peripheral blood mononuclear cells cultured with Interleukin-4 and granulocyte/macrophage-colony-stimulating factor. Eur. J. Immunol. 1997. 27: 756-762.
31. Morel, A-S., Quarantino, S., Douek, D. C. and Londei, M., Split activity of interleukin-10 on antigen capture and antigen presentation by human dendritic cells: definition of a maturative step. Eur. J. Immunol. 1997. 27: 26-34.
32. de Waal Malefyt, R., Figdor, C. G., Huijbens, R., Mohan Peterson, S., Bennett, B., Culpepper, J., Dang, W., Zurawski, G. and de Vries, J. E., Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J. Immunol. 1993. 151: 6370-6381.
33. te Velde, A. A., de Waal Malefyt, R., Huijbens, R. J., de Vries, J. E. and Figdor, C. G., IL-10 stimulates monocyte Fc gamma R surface expression and cytotoxic activity. Distinct regulation of antibody-dependent cellular cytotoxicity by IFN-gamma, IL-4, and IL-10. J. Immunol. 1992. 149: 4048-4052.
34. Gastl, G. A., Abrams, J. S., Nanus, D. M., Oosterkamp, R., Silver, J., Liu, F., Chen, M., Albino, A. P. and Bander, N. H., Interleukin-10 production by human carcinoma cell lines and its relationship to interleukin-6 expression. Int. J. Cancer 1993. 55: 96-101.
35. Alleva, D. G., Burger, C. J. and Elgert, K. D., Tumor-induced regulation of suppressor macrophage nitric oxide and TNF-Alpha production. Role of tumor-derived IL-10, TGF-beta, and protaglandin E2. J. Immunol. 1994. 153: 1674-1686.
36. Yamamura, M., Modlin, R. L., Ohmen, J. D. and Moy, R. L., Local expression of antiinflammatory cytokines in cancer. J. Clin. Invest. 1993. 91: 1005-1010.
37. Pisa, P., Halapi, E., Pisa, E. K., Gerdin, E., Hising, C., Bucht, A., Gerdin, B. and Kiessling, R., Selective expression of interleukin-10, interferon gamma, and granulocyte-macrophage colony-stimulating factor in ovarian cancer biopsies. Proc. Natl. Acad. Sci. USA 1992. 89: 7708-7712.
38. Benjamin, D., Knobloch, T. J. and Dayton, M. A., Human B-cell interleukin-10: B-cell lines derived from patients with acquired immunodeficiency syndrome and Burkitt's lymphoma constitutively secrete large quantities of interleukin-10. Blood 1992. 80: 1289-1298.
39. Graziosi, C., Pantaleo, G., Gantt, K. R. Fortin, J. P., Demarest, J. F., Cohen, O. J., Sekaly, R. P. and Fauci, A. S., Lack of evidence for the dichotomy of TH1 and TH2 predominance in HIV-infected individuals. Science 1994. 265: 248-252.
40. Clerici, M., Hakim, F. T., Venzon, D. J., Blatt, S., Hendrix, C. W., Wynn, T. A. and Shearer, G. M., Changes in interleukin-2 and interleukin-4 production in asymptomatic, human immunodeficiency virus-seropositive individuals. J. Clin. Invest. 1993. 91: 759-765.
41. Thieblemont, N., Weiss, L., Sadeghi, H. M., Estcourt, C. and Haeffner-Cavaillon, N., CD14 low CD16 high: a cytokine-producing monocyte subset which expands during human immunodeficieny virus infection. Eur. J. Immunol. 1995. 25: 3418-3424.
42. Ullrich, S. E., Mechanism involved in the systemic suppression of antigen-presenting cell function by UV irradiation. Keratinocyte-derived IL-10 modulates antigen-presenting cell function of splenic adherent cells. J. Immunol. 1994. 152: 3410-3416.
43. Meunier, L., Batacsorgo, Z. and Cooper, K. D., In human dermis, ultraviolet radiation induces expansion of a CD36(+) CD11b(+) CD1(-) macrophage subset by infiltration and proliferation; CD1 langerhans-like dendritic antigen-presenting cells are concomitantly depleted. J. Invest. Dermatol 1995. 105: 782-788.
44. Sozzani, S., Sallusto, F., Luini, W., Zhou, D., Piemonti, L., Allavena, P., Van Damme, J., Valitutti, S., Lanzavecchia, A. and Mantovani, A., Migration of dendritic cells in response to formyl peptides, C5a and a distinct set of chemokines. J. Immunol. 1995. 155: 3292-3295.