Uptake of apoptotic DC converts immature DC into tolerogenic DC that induce differentiation of Foxp3+ Treg

European Journal of Immunology

Volumn 40, Issue 4, 2010, Pages 1022-1035

  Kushwah, Rahul ^a,b   Wu, Jing ^a   Oliver, Jordan R ^a,b   Jiang, George ^c   Zhang, Jinyi ^c,d   Siminovitch, Katherine A ^c,d   Hu, Jim ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Apoptosis; Autoimmunity; DC; Tolerance

Indexed keywords

TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; ULTRAVIOLET RADIATION;

ANIMALS; ANTIGENS, CD86; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE TOLERANCE; INTERLEUKIN-12; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; LYMPHOPOIESIS; MICE; MICE, INBRED C57BL; NECROSIS; PHAGOCYTOSIS; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; SPLEEN; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 77951033594     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939782     Document Type: Article

References (40)

1. Steinman, R. M., Hawiger, D. and Nussenzweig, M. C., Tolerogenic dendritic cells. Annu. Rev. Immunol. 2003. 21: 685-711.
2. Huang, F. P., Platt, N., Wykes, M., Major, J. R., Powell, T. J., Jenkins, C. D. and MacPherson, G. G., A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 2000. 191: 435-444.
3. Sauter, B., Albert, M. L., Francisco, L., Larsson, M., Somersan, S. and Bhardwaj, N., Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 2000. 191: 423-434.
4. Peng, Y., Martin, D. A., Kenkel, J., Zhang, K., Ogden, C. A. and Elkon, K. B., Innate and adaptive immune response to apoptotic cells. J. Autoimmun. 2007. 29: 303-309. (Pubitemid 47633145)
5. Winau, F., Weber, S., Sad, S., de Diego, J., Hoops, S. L., Breiden, B., Sandhoff, K. et al., Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 2006. 24: 105-117. (Pubitemid 43077204)
6. Feng, H., Zeng, Y., Graner, M. W. and Katsanis, E., Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 2002. 100: 4108-4115. (Pubitemid 35396879)
7. Johansson, U., Walther-Jallow, L., Smed-Sorensen, A. and Spetz, A. L., Triggering of dendritic cell responses after exposure to activated, but not resting, apoptotic PBMCs. J. Immunol. 2007. 179: 1711-1720.
8. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y. and Henson, P. M., Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 1998. 101: 890-898. (Pubitemid 28096086)
9. Chen, W., Frank, M. E., Jin, W. and Wahl, S. M., TGF-beta released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 2001. 14: 715-725. (Pubitemid 32592419)
10. Chen, M., Wang, Y. H., Wang, Y., Huang, L., Sandoval, H., Liu, Y. J. and Wang, J., Dendritic cell apoptosis in the maintenance of immune tolerance. Science 2006. 311: 1160-1164. (Pubitemid 43305956)
11. Doerfler, P., Forbush, K. A. and Perlmutter, R. M., Caspase enzyme activity is not essential for apoptosis during thymocyte development. J. Immunol. 2000. 164: 4071-4079. (Pubitemid 30215062)
12. Walsh, C. M., Wen, B. G., Chinnaiyan, A. M., O'Rourke, K., Dixit, V. M. and Hedrick, S. M., A role for FADD in T cell activation and development. Immunity 1998. 8: 439-449. (Pubitemid 28196798)
13. Newton, K., Harris, A. W., Bath, M. L., Smith, K. G. and Strasser, A., A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J. 1998. 17: 706-718. (Pubitemid 28062050)
14. Ito, M., Minamiya, Y., Kawai, H., Saito, S., Saito, H., Nakagawa, T., Imai, K. et al., Tumor-derived TGFbeta-1 induces dendritic cell apoptosis in the sentinel lymph node. J. Immunol. 2006. 176: 5637-5643.
15. Pinzon-Charry, A., Maxwell, T., McGuckin, M. A., Schmidt, C., Furnival, C. and Lopez, J. A., Spontaneous apoptosis of blood dendritic cells in patients with breast cancer. Breast Cancer Res. 2006. 8: R5. (Pubitemid 44644834)
16. Pinzon-Charry, A., Ho, C. S., Maxwell, T., McGuckin, M. A., Schmidt, C., Furnival, C., Pyke, C. M. and Lopez, J. A., Numerical and functional defects of blood dendritic cells in early- and late-stage breast cancer. Br. J. Cancer 2007. 97: 1251-1259. (Pubitemid 350035809)
17. Zeni, F., Freeman, B. and Natanson, C., Anti-inflammatory therapies to treat sepsis and septic shock: a reassessment. Crit. Care Med. 1997. 25: 1095-1100.
18. Park, Y., Lee, S. W. and Sung, Y. C., Cutting edge: CpG DNA inhibits dendritic cell apoptosis by up-regulating cellular inhibitor of apoptosis proteins through the phosphatidylinositide-3′-OH kinase pathway. J. Immunol. 2002. 168: 5-8. (Pubitemid 34014095)
19. Chen, M., Huang, L. and Wang, J., Deficiency of Bim in dendritic cells contributes to overactivation of lymphocytes and autoimmunity. Blood 2007. 109: 4360-4367. (Pubitemid 46743404)
20. Inaba, K., Turley, S., Yamaide, F., Iyoda, T., Mahnke, K., Inaba, M., Pack, M. et al., Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J. Exp. Med. 1998. 188: 2163-2173.
21. Albert, M. L., Sauter, B. and Bhardwaj, N., Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998. 392: 86-89. (Pubitemid 28150594)
22. De, S. R., Ajmone-Cat, M. A., Nicolini, A. and Minghetti, L., Expression of phosphatidylserine receptor and down-regulation of pro-inflammatory molecule production by its natural ligand in rat microglial cultures. J. Neuropathol. Exp. Neurol. 2002. 61: 237-244.
23. Huynh, M. L., Fadok, V. A. and Henson, P. M., Phosphatidylserine- dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J. Clin. Invest. 2002. 109: 41-50.
24. Chen, X., Doffek, K., Sugg, S. L. and Shilyansky, J., Phosphatidylserine regulates the maturation of human dendritic cells. J. Immunol. 2004. 173: 2985-2994. (Pubitemid 39142003)
25. Takahashi, M. and Kobayashi, Y., Cytokine production in association with phagocytosis of apoptotic cells by immature dendritic cells. Cell. Immunol. 2003. 226: 105-115.
26. Morelli, A. E., Larregina, A. T., Shufesky,W. J., Zahorchak, A. F., Logar, A. J., Papworth, G. D.,Wang, Z. et al., Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 2003. 101: 611-620.
27. Reuveny, M., Heller, H. and Bengal, E., RhoA controls myoblast survival by inducing the phosphatidylinositol 3-kinase-Akt signaling pathway. FEBS Lett. 2004. 569: 129-134. (Pubitemid 38844605)
28. Williams, C. A., Harry, R. A. and McLeod, J. D., Apoptotic cells induce dendritic cell-mediated suppression via interferon-gamma-induced IDO. Immunology 2008. 124: 89-101.
29. Orabona, C., Pallotta, M. T., Volpi, C., Fallarino, F., Vacca, C., Bianchi, R., Belladonna, M. L. et al., SOCS3 drives proteasomal degradation of indoleamine 2,3-dioxygenase (IDO) and antagonizes IDO-dependent tolerogenesis. Proc. Natl. Acad. Sci. USA 2008. 105: 20828-20833.
30. Hotchkiss, R. S. and Karl, I. E., The pathophysiology and treatment of sepsis. N. Engl. J. Med. 2003. 348: 138-150.
31. Hotchkiss, R. S., Tinsley, K. W., Swanson, P. E., Grayson, M. H., Osborne, D. F., Wagner, T. H., Cobb, J. P. et al., Depletion of dendritic cells, but not macrophages, in patients with sepsis. J. Immunol. 2002. 168: 2493-2500.
32. Tinsley, K. W., Grayson, M. H., Swanson, P. E., Drewry, A. M., Chang, K. C., Karl, I. E. and Hotchkiss, R. S., Sepsis induces apoptosis and profound depletion of splenic interdigitating and follicular dendritic cells. J. Immunol. 2003. 171: 909-914.
33. Monneret, G., Debard, A. L., Venet, F., Bohe, J., Hequet, O., Bienvenu, J. and Lepape, A., Marked elevation of human circulating CD4+CD25+ regulatory T cells in sepsis-induced immunoparalysis. Crit. Care Med. 2003. 31: 2068-2071.
34. Kushwah, R., Cao, H. and Hu, J., Characterization of pulmonary T cell response to helper-dependent adenoviral vectors following intranasal delivery. J. Immunol. 2008. 180: 4098-4108.
35. Angelov, G. S., Tomkowiak, M., Marcais, A., Leverrier, Y. and Marvel, J., Flt3 ligand-generated murine plasmacytoid and conventional dendritic cells differ in their capacity to prime naïve CD8 T cells and to generate memory cells in vivo. J. Immunol. 2005. 175: 189-195. (Pubitemid 40884317)
36. Wu, J., Duan, R., Cao, H., Field, D., Newnham, C. M., Koehler, D. R., Zamel, N. et al., Regulation of epithelium-specific Ets-like factors ESE-1 and ESE-3 in airway epithelial cells: potential roles in airway inflammation. Cell. Res. 2008. 18: 649-663.
37. Huang, X. R., Chung, A. C., Wang, X. J., Lai, K. N. and Lan, H. Y., Mice overexpressing latent TGF-betal are protected against renal fibrosis in obstructive kidney disease. Am. J. physiol. Renal. Physiol. 2008. 295: F118-127.
38. Zhang, T. Y. and Daynes, R. A., Marophages from 11beta-hydroxysteroid dehydrogenase type 1-deficient mice exhibit an increased sensitiity to lipopolysaccharide stimulation due to TGF-beta-mediated up-regulation of SHIP1 expression. J. Immunol. 2007. 179: 6325-6335.
39. Gautier, G., Humbert, M., Deauvieau, F., Scuiller, M., Hiscott, J., Bates, E. E., Trinchieri, G. et al., A type I interferon autocrine-paracrine loop is involved in toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J. Exp. Med. 2005. 201: 1435-1446.
40. Nolte, M. A., Leibundgut-Landmann, S., Joffre, O. and Reis e Sousa, C., Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J. Exp. Med. 2007. 204: 1487-1501.