IL-10 deficiency blocks the ability of LPS to regulate expression of tolerance-related molecules on dendritic cells

European Journal of Immunology

Volumn 42, Issue 6, 2012, Pages 1449-1458

  Zhou, Fang ^a,b   Ciric, Bogoljub ^a   Li, Hongmei ^a   Yan, Yaping ^a   Li, Ke ^a,c   Cullimore, Melissa ^a   Lauretti, Elisabetta ^a   Gonnella, Patricia ^a   Zhang, Guang Xian ^a   Rostami, Abdolmohamad ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b SHENZHEN THIRD PEOPLE S HOSPITAL   (China)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Costimulatory molecule DCs IL 10 TLR4

Indexed keywords

B7 ANTIGEN; CD103 ANTIGEN; CD14 ANTIGEN; CD40 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; GALECTIN 1; GLYCOPROTEIN P 15095; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 10; INTERLEUKIN 27; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE SEVERITY; DOWN REGULATION; FEMALE; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84862116936     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141733     Document Type: Article

References (49)

1. Steinman, R. M. and Banchereau, J., Taking dendritic cells into medicine. Nature 2007. 449: 419-426.
2. Wu, L. and Liu, Y. J., Development of dendritic-cell lineages. Immunity 2007. 26: 741-750.
3. Sathe, P. and Wu, L., The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets. Protein Cell 2011. 2: 620-630.
4. Joffre, O., Nolte, M. A., Sporri, R. and Reis e Sousa, C., Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev. 2009. 227: 234-247.
5. Kehrl, J. H., Hwang, I. Y. and Park, C., Chemoattract receptor signaling and its role in lymphocyte motility and trafficking. Curr. Top. Microbiol. Immunol. 2009. 334: 107-127.
6. He, S., Cao, Q., Yoneyama, H., Ge, H., Zhang, Y. and Zhang, Y., MIP-3alpha and MIP-1alpha rapidly mobilize dendritic cell precursors into the peripheral blood. J Leukoc. Biol. 2008. 84: 1549-1556.
7. Dorfel, D., Appel, S., Grunebach, F., Weck, M. M., Muller, M. R., Heine, A. and Brossart, P., Processing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro-transcribed MUC1 RNA. Blood 2005. 105: 3199-3205.
8. Keir, M. E. and Sharpe, A. H., The B7/CD28 costimulatory family in autoimmunity. Immunol. Rev. 2005. 204: 128-143.
9. Gee, K., Guzzo, C., Che Mat, N. F., Ma, W. and Kumar, A., The IL-12 family of cytokines in infection, inflammation and autoimmune disorders. Inflamm. Allergy Drug Targets 2009. 8: 40-52.
10. Duraes, F. V., Carvalho, N. B., Melo, T. T., Oliveira, S. C. and Fonseca, C. T., IL-12 and TNF-alpha production by dendritic cells stimulated with Schistosoma mansoni schistosomula tegument is TLR4- and MyD88-dependent. Immunol. Lett. 2009. 125: 72-77.
11. Oz-Arslan, D., Ruscher, W., Myrtek, D., Ziemer, M., Jin, Y., Damaj, B. B., Sorichter, S. et al., IL-6 and IL-8 release is mediated via multiple signaling pathways after stimulating dendritic cells with lysophospholipids. J. Leukoc. Biol. 2006. 80: 287-297.
12. Mosser, D. M. and Zhang, X., Interleukin-10: new perspectives on an old cytokine. Immunol. Rev. 2008. 226: 205-218.
13. Tadokoro, C. E., Vallochi, A. L., Rios, L. S., Martins, G. A., Schlesinger, D., Mosca, T., Kuchroo, V. K. et al., Experimental autoimmune encephalomyelitis can be prevented and cured by infection with Trypanosoma cruzi. J. Autoimmun. 2004. 23: 103-115.
14. Massey, E. J., Sundstedt, A., Day, M. J., Corfield, G., Anderton, S. and Wraith, D. C., Intranasal peptide-induced peripheral tolerance: the role of IL-10 in regulatory T-cell function within the context of experimental autoimmune encephalomyelitis. Vet. Immunol. Immunopathol. 2002. 87: 357-372.
15. Zhang, X., Koldzic, D. N., Izikson, L., Reddy, J., Nazareno, R. F., Sakaguchi, S., Kuchroo, V. K. et al., IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+CD4+ regulatory T cells. Int. Immunol. 2004. 16: 249-256.
16. Murai, M., Turovskaya, O., Kim, G., Madan, R., Karp, C. L., Cheroutre, H. and Kronenberg, M., Interleukin 10 acts on Treg cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 2009. 10: 1178-1184.
17. Ilarregui, J. M., Croci, D. O., Bianco, G. A., Toscano, M. A., Salatino, M., Vermeulen, M. E., Geffner, J. R. et al., Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 2009. 10: 981-991.
18. Dhirapong, A., Lleo, A., Leung, P., Gershwin, M. E. and Liu, F. T., The immunological potential of galectin-1 and -3. Autoimmun. Rev. 2009. 8: 360-363.
19. Blois, S. M., Ilarregui, J. M., Tometten, M., Garcia, M., Orsal, A. S., Cordo-Russo, R., Toscano, M. A. et al., pivotal role for galectin-1 in fetomaternal tolerance. Nat. Med. 2007. 13: 1450-1457.
20. Shrimpton, R. E., Butler, M., Morel, A. S., Eren, E., Hue, S. S. and Ritter, M. A., CD205 (DEC-205): a recognition receptor for apoptotic and necrotic self. Mol. Immunol. 2009. 46: 1229-1239.
21. Yamazaki, S., Dudziak, D., Heidkamp, G. F., Fiorese, C., Bonito, A. J., Inaba, K., Nussenzweig, M. C. et al., CD8+ CD205+ splenic dendritic cells are specialized to induce Foxp3+ regulatory T cells. J. Immunol. 2008. 181: 6923-6933.
22. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J. L., Berg, P. L. et al., Small intestinal CD103 +dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008. 205: 2139-2149.
23. Strauch, U. G., Grunwald, N., Obermeier, F., Gurster, S. and Rath, H. C., Loss of CD103+ intestinal dendritic cells during colonic inflammation. World J. Gastroenterol. 2010. 16: 21-29.
24. Takeda, K., The lipid A receptor. Adv. Exp. Med. Biol. 2009. 667: 53-58.
25. Faria, A. M. and Weiner, H. L., Oral tolerance: therapeutic implications for autoimmune diseases. Clin. Dev. Immunol. 2006. 13: 143-157.
26. Prud'homme, G. J., Gene therapy of autoimmune diseases with vectors encoding regulatory cytokines or inflammatory cytokine inhibitors. J. Gene Med. 2000. 2: 222-232.
27. Taylor, A., Akdis, M., Joss, A., Akkoc, T., Wenig, R., Colonna, M., Daigle, I. et al., IL-10 inhibits CD28 and ICOS costimulations of T cells via src homology 2 domain-containing protein tyrosine phosphatase 1. J. Allergy Clin. Immunol. 2007. 120: 76-83.
28. Ozawa, H., Aiba, S., Nakagawa and Tagami, H., Interferon-gamma and interleukin-10 inhibit antigen presentation by Langerhans cells for T helper type 1 cells by suppressing their CD80 (B7-1) expression. Eur. J. Immunol. 1996. 26: 648-652.
29. 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.
30. Papenfuss, T. L., Kithcart, A. P., Powell, N. D., McClain, M. A., Gienapp, I. E., Shawler, T. M. and Whitacre, C. C., Disease-modifying capability of murine Flt3-ligand DCs in experimental autoimmune encephalomyelitis. J. Leukoc. Biol. 2007. 82: 1510-1518.
31. Ellestad, K. K., Tsutsui, S., Noorbakhsh, F., Warren, K. G., Yong, V. W., Pittman, Q. J. and Power, C., Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J. Immunol. 2009. 183: 298-309.
32. Albrecht, V., Hofer, T. P., Foxwell, B., Frankenberger, M. and Ziegler-Heitbrock, L., Tolerance induced via TLR2 and TLR4 in human dendritic cells: role of IRAK-1. BMC Immunol. 2008. 9: 69-82.
33. Allam, J. P., Peng, W. M., Appel, T., Wenghoefer, M., Niederhagen, B., Bieber, T., Berge, S. et al., Toll-like receptor 4 ligation enforces tolerogenic properties of oral mucosal Langerhans cells. J. Allergy Clin. Immunol. 2008. 121: 368-374, e361.
34. Geisel, J., Kahl, F., Muller, M., Wagner, H., Kirschning, C. J., Autenrieth, I. B. and Frick, J. S., IL-6 and maturation govern TLR2 and TLR4 induced TLR agonist tolerance and cross-tolerance in dendritic cells. J. Immunol. 2007. 179: 5811-5818.
35. Hollingsworth, J. W., Whitehead, G. S., Lin, K. L., Nakano, H., Gunn, M. D., Schwartz, D. A. and Cook, D. N., TLR4 signaling attenuates ongoing allergic inflammation. J. Immunol. 2006. 176: 5856-5862.
36. Mahnke, K. and Enk, A. H., Dendritic cells: key cells for the induction of regulatory T cells? Curr. Top. Microbiol. Immunol. 2005. 293: 133-150.
37. Li, H., Zhang, G. X., Chen, Y., Xu, H., Fitzgerald, D. C., Zhao, Z. and Rostami, A., CD11c+CD11b +dendritic cells play an important role in intravenous tolerance and the suppression of experimental autoimmune encephalomyelitis. J. Immunol. 2008. 181: 2483-2493.
38. Moreau, A., Chiffoleau, E., Beriou, G., Deschamps, J. Y., Heslan, M., Ashton-Chess, J., Rolling, F. et al., Superiority of bone marrow-derived dendritic cells over monocyte-derived ones for the expansion of Treg cells in the macaque. Transplantation 2008. 85: 1351-1356.
39. Fehr, T., Wang, S., Haspot, F., Kurtz, J., Blaha, P., Hogan, T., Chittenden, M. et al., deletional peripheral CD8 T-cell tolerance induced by allogeneic bone marrow: role of donor class II MHC and B cells. J. Immunol. 2008. 181: 4371-4380.
40. Oriss, T. B., Ostroukhova, M., Seguin-Devaux, C., Dixon-McCarthy, B., Stolz, D. B., Watkins, S. C., Pillemer, B. et al., Dynamics of dendritic cell phenotype and interactions with CD4+ T cells in airway inflammation and tolerance. J. Immunol. 2005. 174: 854-863.
41. Kimura, A., Naka, T. and Kishimoto, T., IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA 2007. 104: 12099-12104.
42. Goodman, W. A., Levine, A. D., Massari, J. V., Sugiyama, H., McCormick, T. S. and Cooper, K. D., IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J. Immunol. 2009. 183: 3170-3176.
43. Tournadre, A. and Miossec, P., Chemokines and dendritic cells in inflammatory myopathies. Ann. Rheum. Dis. 2009. 68: 300-304.
44. Perros, F., Hoogsteden, H. C., Coyle, A. J., Lambrecht, B. N. and Hammad, H., Blockade of CCR4 in a humanized model of asthma reveals a critical role for DC-derived CCL17 and CCL22 in attracting Th2 cells and inducing airway inflammation. Allergy 2009. 64: 995-1002.
45. Bozzacco, L., Trumpfheller, C., Siegal, F. P., Mehandru, S., Markowitz, M., Carrington, M., Nussenzweig, M. C. et al., DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. USA 2007. 104: 1289-1294.
46. Wang, B., Kuroiwa, J. M., He, L. Z., Charalambous, A., Keler, T. and Steinman, R. M., The human cancer antigen mesothelin is more efficiently presented to the mouse immune system when targeted to the DEC-205/CD205 receptor on dendritic cells. Ann. NY Acad. Sci. 2009. 1174: 6-17.
47. Leach, M. W., Davidson, N. J., Fort, M. M., Powrie, F. and Rennick, D. M., The role of IL-10 in inflammatory bowel disease: "of mice and men". Toxicol. Pathol. 1999. 27: 123-133.
48. Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N. and Schuler, G., An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Meth. 1999. 223: 77-92.
49. Zhang, G. X., Kishi, M., Xu, H. and Rostami, A., Mature bone marrow-derived dendritic cells polarize Th2 response and suppress experimental autoimmune encephalomyelitis. Mult. Scler. 2002. 8: 463-468.