Apoptotic cells induce immunosuppression through dendritic cells: Critical roles of IFN-γ and nitric oxide

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3277-3284

  Ren, Guangwen ^a   Su, Juanjuan ^b   Zhao, Xin ^a   Zhang, Liying ^a   Zhang, Jimin ^a   Roberts, Arthur I ^a   Zhang, Huatang ^b   Das, Gobardhan ^a,c   Shi, Yufang ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON ANTIBODY; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 2; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL CELL; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CELL EXPANSION; CELL PROLIFERATION; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EX VIVO STUDY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; COCULTURE TECHNIQUES; DENDRITIC CELLS; INTERFERON TYPE II; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; T-LYMPHOCYTES;

EID: 51549085896     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3277     Document Type: Article

References (45)

1. Michlewska, S., A. McColl, A. G. Rossi, I. L. Megson, and I. Dransfield. 2007. Clearance of dying cells and autoimmunity. Autoimmunity 40: 267-273.
2. Savill, J. S., A. H. Wyllie, J. E. Henson, M. J. Walport, P. M. Henson, and C. Haslett. 1989. Macrophage phagocytosis of aging neutrophils in inflammation: programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83: 865-875.
3. Sun, E. W., and Y. F. Shi. 2001. Apoptosis: the quiet death silences the immune system. Pharmacol. Ther. 92: 135-145.
4. Wyllie, A. H. 1987. Apoptosis: cell death in tissue regulation. J. Pathol. 153: 313-316. (Pubitemid 18008327)
5. Ferguson, T. A., P. M. Stuart, J. M. Herndon, and T. S. Griffith. 2003. Apoptosis, tolerance, and regulatory T cells: old wine, new wineskins. Immunol. Rev. 193: 111-123.
6. Sun, E., Y. Gao, J. Chen, A. I. Roberts, X. Wang, Z. Chen, and Y. Shi. 2004. Allograft tolerance induced by donor apoptotic lymphocytes requires phagocytosis in the recipient. Cell Death Differ. 11: 1258-1264. (Pubitemid 39591771)
7. May, R. C., and L. M. Machesky. 2001. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114: 1061-1077.
8. Zhou, Z., P. M. Mangahas, and X. Yu. 2004. The genetics of hiding the corpse: engulfment and degradation of apoptotic cells in C. elegans and D. melanogaster. Curr. Top. Dev. Biol. 63: 91-143.
9. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975. (Pubitemid 37323217)
10. Metchnikoff, E. 1905. Immunity in Infective Diseases. University Press, Cambridge.
11. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187. (Pubitemid 34506799)
12. Dini, L., F. Autuori, A. Lentini, S. Oliverio, and M. Piacentini. 1992. The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Lett. 296: 174-178.
13. Tarr, J., and P. Eggleton. 2005. Immune function of C1q and its modulators CD91 and CD93. Crit. Rev. Immunol. 25: 305-330. (Pubitemid 43075961)
14. Gregory, C. D. 2000. CD14-dependent clearance of apoptotic cells: relevance to the immune system. Curr. Opin. Immunol. 12: 27-34.
15. Ogden, C. A., and K. B. Elkon. 2006. Role of complement and other innate immune mechanisms in the removal of apoptotic cells. Curr. Dir. Autoimmun. 9: 120-142.
16. Gaipl, U. S., A. Kuhn, A. Sheriff, L. E. Munoz, S. Franz, R. E. Voll, J. R. Kalden, and M. Herrmann. 2006. Clearance of apoptotic cells in human SLE. Curr. Dir. Autoimmun. 9: 173-187.
17. Wu, Y., N. Tibrewal, and R. B. Birge. 2006. Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. 16: 189-197.
18. + T cells that produce TRAIL. J. Immunol. 178: 2679-2687.
19. Ferguson, T. A., and H. Kazama. 2005. Signals from dying cells: tolerance induction by the dendritic cell. Immunol. Res. 32: 99-108.
20. Savill, J. 1998. Apoptosis: phagocytic docking without shocking. Nature 392: 442-443. (Pubitemid 28168963)
21. Steinman, R. M., S. Turley, I. Mellman, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191: 411-416. (Pubitemid 30693565)
22. Sauter, B., M. L. Albert, L. Francisco, M. Larsson, S. Somersan, and N. Bhardwaj. 2000. 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. 191: 423-434. (Pubitemid 30693567)
23. Li, A., O. Ojogho, and A. Escher. 2006. Saving death: apoptosis for intervention in transplantation and autoimmunity. Clin. Dev. Immunol. 13: 273-282. (Pubitemid 44963423)
24. Chung, E. Y., S. J. Kim, and X. J. Ma. 2006. Regulation of cytokine production during phagocytosis of apoptotic cells. Cell Res. 16: 154-161.
25. Chen, W., M. E. Frank, W. Jin, and S. M. Wahl. 2001. TGF-β released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 14: 715-725. (Pubitemid 32592419)
26. Freire-de-Lima, C. G., D. O. Nascimento, M. B. Soares, P. T. Bozza, H. C. Castro-Faria-Neto, F. G. de Mello, G. A. DosReis, and M. F. Lopes. 2000. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403: 199-203.
27. Wang, R., and Y. F. Shi. 2002. A simplified protocol for apoptosis assay by DNA content analysis. BioTechniques (Suppl.): 88-91. (Pubitemid 35168046)
28. Stoll, S., J. Delon, T. M. Brotz, and R. N. Germain. 2002. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296: 1873-1876. (Pubitemid 34596274)
29. Hussain, S., B. S. Zwilling, and W. P. Lafuse. 1999. Mycobacterium avium infection of mouse macrophages inhibits IFN-γ Janus kinase-STAT signaling and gene induction by down-regulation of the IFN-γ receptor. J. Immunol. 163: 2041-2048. (Pubitemid 29382208)
30. Chen, C. W., Y. H. Chang, C. J. Tsi, and W. W. Lin. 2003. Inhibition of IFN-γ-mediated inducible nitric oxide synthase induction by the peroxisome proliferator- activated receptor γ agonist, 15-deoxy-δ 12,14-prostaglandin J2, involves inhibition of the upstream Janus kinase/STAT1 signaling pathway. J. Immunol. 171: 979-988.
31. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350.
32. Meier, P., A. Finch, and G. Evan. 2000. Apoptosis in development. Nature 407: 796-801.
33. Ginaldi, L., M. De Martinis, A. D'Ostilio, L. Marini, M. F. Loreto, M. P. Corsi, and D. Quaglino. 2000. Cell proliferation and apoptosis in the immune system in the elderly. Immunol. Res. 21: 31-38. (Pubitemid 30224218)
34. Pittoni, V., and G. Valesini. 2002. The clearance of apoptotic cells: implications for autoimmunity. Autoimmun. Rev. 1: 154-161. (Pubitemid 38340266)
35. Ravichandran, K. S. 2003. "Recruitment signals" from apoptotic cells: invitation to a quiet meal. Cell 113: 817-820.
36. Xu, G., and Y. Shi. 2007. Apoptosis signaling pathways and lymphocyte homeostasis. Cell Res. 17: 759-771. (Pubitemid 47411431)
37. Cohen, P. L., R. Caricchio, V. Abraham, T. D. Camenisch, J. C. Jennette, R. A. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196: 135-140.
38. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59. (Pubitemid 28242023)
39. Bijl, M., E. Reefman, G. Horst, P. C. Limburg, and C. G. Kallenberg. 2006. Reduced uptake of apoptotic cells by macrophages in systemic lupus erythematosus: correlates with decreased serum levels of complement. Ann. Rheum. Dis. 65: 57-63. (Pubitemid 41815640)
40. Liu, K., T. Iyoda, M. Saternus, Y. Kimura, K. Inaba, and R. M. Steinman. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 196: 1091-1097. (Pubitemid 35231767)
41. Miyake, Y., K. Asano, H. Kaise, M. Uemura, M. Nakayama, and M. Tanaka. 2007. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J. Clin. Invest. 117: 2268-2278. (Pubitemid 47219572)
42. Fadok, V. A., D. L. Bratton, A. Konowal, P. W. Freed, J. Y. Westcott, and P. M. Henson. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101: 890-898.
43. Saas, P., F. Bonnefoy, S. Kury-Paulin, F. Kleinclauss, and S. Perruche. 2007. Mediators involved in the immunomodulatory effects of apoptotic cells. Transplantation 84: S31-34. (Pubitemid 47067539)
44. Xia, C. Q., R. Peng, Y. Qiu, M. Annamalai, D. Gordon, and M. J. Clare-Salzler. 2007. Transfusion of apoptotic β-cells induces immune tolerance to β-cell antigens and prevents type 1 diabetes in NOD mice. Diabetes 56: 2116-2123.
45. Bogdan, C. 1998. The multiplex function of nitric oxide in (auto)immunity. J. Exp. Med. 187: 1361-1365. (Pubitemid 28215395)