Sepsis-induced apoptosis leads to active suppression of delayed-type hypersensitivity by CD8+ regulatory T cells through a TRAIL-dependent mechanism

Journal of Immunology

Volumn 184, Issue 12, 2010, Pages 6766-6772

  Unsinger, Jacqueline ^a   Kazama, Hirotaka ^a   McDonough, Jacqueline S ^a   Griffith, Thomas S ^b   Hotchkiss, Richard S ^a   Ferguson, Thomas A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PICRIC ACID; PROTEIN BCL 2; APOPTOSIS REGULATORY PROTEIN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; MEMBRANE PROTEIN; ONCOPROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CECUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; GENE OVEREXPRESSION; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SEPSIS; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; METABOLISM; NICK END LABELING; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; HYPERSENSITIVITY, DELAYED; IN SITU NICK-END LABELING; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS; SEPSIS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 77953635470     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0904054     Document Type: Article

References (51)

1. Angus, D. C., W. T. Linde-Zwirble, J. Lidicker, G. Clermont, J. Carcillo, and M. R. Pinsky. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29: 1303-1310.
2. Murphy, S. L. 2000. Deaths: final data for 1998. Natl. Vital Stat. Rep. 48: 1-105.
3. Munford, R. S., and J. Pugin. 2001. Normal responses to injury prevent systemic inflammation and can be immunosuppressive. Am. J. Respir. Crit. Care Med. 163: 316-321.
4. Monneret, G., F. Venet, A. Pachot, and A. Lepape. 2008. Monitoring immune dysfunctions in the septic patient: a new skin for the old ceremony. Mol. Med. 14: 64-78.
5. Oberholzer, A., C. Oberholzer, and L. L. Moldawer. 2001. Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 16: 83-96.
6. Hotchkiss, R. S., C. M. Coopersmith, J. E. McDunn, and T. A. Ferguson. 2009. The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15: 496-497.
7. Hotchkiss, R. S., P. E. Swanson, B. D. Freeman, K. W. Tinsley, J. P. Cobb, G. M. Matuschak, T. G. Buchman, and I. E. Karl. 1999. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27: 1230-1251.
8. Huber-Lang, M. S., E. M. Younkin, J. V. Sarma, S. R. McGuire, K. T. Lu, R. F. Guo, V. A. Padgaonkar, J. T. Curnutte, R. Erickson, and P. A. Ward. 2002. Complement-induced impairment of innate immunity during sepsis. J. Immunol. 169: 3223-3231.
9. Guisset, O., M. S. Dilhuydy, R. Thiébaut, J. Lefèvre, F. Camou, A. Sarrat, C. Gabinski, J. F. Moreau, and P. Blanco. 2007. Decrease in circulating dendritic cells predicts fatal outcome in septic shock. Intensive Care Med. 33: 148-152. (Pubitemid 46115483)
10. Wen, H., Y. Dou, C. M. Hogaboam, and S. L. Kunkel. 2008. Epigenetic regulation of dendritic cell-derived interleukin-12 facilitates immunosuppression after a severe innate immune response. Blood 111: 1797-1804.
11. Flohé, S. B., H. Agrawal, D. Schmitz, M. Gertz, S. Flohé, and F. U. Schade. 2006. Dendritic cells during polymicrobial sepsis rapidly mature but fail to initiate a protective Th1-type immune response. J. Leukoc. Biol. 79: 473-481.
12. Ayala, A., C. S. Chung, G. Y. Song, and I. H. Chaudry. 2001. IL-10 mediation of activation-induced TH1 cell apoptosis and lymphoid dysfunction in polymicrobial sepsis. Cytokine 14: 37-48.
13. Heuer, J. G., T. Zhang, J. Zhao, C. Ding, M. Cramer, K. L. Justen, S. L. Vonderfecht, and S. Na. 2005. Adoptive transfer of in vitro-stimulated CD4+ CD25+ regulatory T cells increases bacterial clearance and improves survival in polymicrobial sepsis. J. Immunol. 174: 7141-7146.
14. Venet, F., A. Pachot, A. L. Debard, J. Bohé, J. Bienvenu, A. Lepape, and G. Monneret. 2004. Increased percentage of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25- lymphocytes. Crit. Care Med. 32: 2329-2331.
15. Lukaszewicz, A. C., M. Grienay, M. Resche-Rigon, R. Pirracchio, V. Faivre, B. Boval, and D. Payen. 2009. Monocytic HLA-DR expression in intensive care patients: interest for prognosis and secondary infection prediction. Crit. Care Med. 37: 2746-2752.
16. Hotchkiss, R. S., and D. W. Nicholson. 2006. Apoptosis and caspases regulate death and inflammation in sepsis. Nat. Rev. Immunol. 6: 813-822.
17. Christou, N. V., J. L. Meakins, J. Gordon, J. Yee, M. Hassan-Zahraee, C. W. Nohr, H. M. Shizgal, and L. D. MacLean. 1995. The delayed hypersensitivity response and host resistance in surgical patients. 20 years later. Ann. Surg. 222: 534-546; discussion 546-538.
18. Meakins, J. L., N. V. Christou, J. Bohnen, and L. D. MacLean. 1982. Failure of delayed hypersensitivity skin testing to predict postoperative sepsis and mortality. Br. Med. J. (Clin. Res. Ed.) 285: 1207-1208.
19. Griffith, T. S., H. Kazama, R. L. VanOosten, J. K. Earle, Jr., J. M. Herndon, D. R. Green, and T. A. Ferguson. 2007. Apoptotic cells induce tolerance by generating helpless CD8+ T cells that produce TRAIL. J. Immunol. 178: 2679-2687.
20. Griffith, T. S., X. Yu, J. M. Herndon, D. R. Green, and T. A. Ferguson. 1996. CD95-induced apoptosis of lymphocytes in an immune privileged site induces immunological tolerance. Immunity 5: 7-16.
21. Ferguson, T. A., J. Herndon, B. Elzey, T. S. Griffith, S. Schoenberger, and D. R. Green. 2002. Uptake of apoptotic antigen-coupled cells by lymphoid dendritic cells and cross-priming of CD8(+) T cells produce active immune unresponsiveness. J. Immunol. 168: 5589-5595.
22. Gao, Y., J. M. Herndon, H. Zhang, T. S. Griffith, and T. A. Ferguson. 1998. Antiinflammatory effects of CD95 ligand (FasL)-induced apoptosis. J. Exp. Med. 188: 887-896.
23. 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.
24. Kazama, H., J. E. Ricci, J. M. Herndon, G. Hoppe, D. R. Green, and T. A. Ferguson. 2008. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 29: 21-32.
25. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, K. C. Chang, J. P. Cobb, T. G. Buchman, S. J. Korsmeyer, and I. E. Karl. 1999. Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. USA 96: 14541-14546.
26. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, M. H. Grayson, D. F. Osborne, T. H. Wagner, J. P. Cobb, C. Coopersmith, and I. E. Karl. 2002. Depletion of dendritic cells, but not macrophages, in patients with sepsis. J. Immunol. 168: 2493-2500.
27. Green, D. R., T. Ferguson, L. Zitvogel, and G. Kroemer. 2009. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9: 353-363.
28. 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.
29. 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-beta, PGE2, and PAF. J. Clin. Invest. 101: 890-898.
30. 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.
31. Janssen, E. M., N. M. Droin, E. E. Lemmens, M. J. Pinkoski, S. J. Bensinger, B. D. Ehst, T. S. Griffith, D. R. Green, and S. P. Schoenberger. 2005. CD4+ Tcell help controls CD8+ T-cell memory via TRAIL-mediated activation-induced cell death. Nature 434: 88-93.
32. Sedger, L. M., M. B. Glaccum, J. C. Schuh, S. T. Kanaly, E. Williamson, N. Kayagaki, T. Yun, P. Smolak, T. Le, R. Goodwin, and B. Gliniak. 2002. Characterization of the in vivo function of TNF-alpha-related apoptosis-inducing ligand, TRAIL/Apo2L, using TRAIL/Apo2L gene-deficient mice. Eur. J. Immunol. 32: 2246-2254.
33. Domen, J., K. L. Gandy, and I. L. Weissman. 1998. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 91: 2272-2282.
34. Bouillet, P., D. Metcalf, D. C. Huang, D. M. Tarlinton, T. W. Kay, F. Köntgen, J. M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286: 1735-1738. (Pubitemid 129515880)
35. Hotchkiss, R. S., P. E. Swanson, C. M. Knudson, K. C. Chang, J. P. Cobb, D. F. Osborne, K. M. Zollner, T. G. Buchman, S. J. Korsmeyer, and I. E. Karl. 1999. Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J. Immunol. 162: 4148-4156.
36. Unsinger, J., J. M. Herndon, C. G. Davis, J. T. Muenzer, R. S. Hotchkiss, and T. A. Ferguson. 2006. The role of TCR engagement and activation-induced cell death in sepsis-induced T cell apoptosis. J. Immunol. 177: 7968-7973.
37. Hotchkiss, R. S., S. B. Osmon, K. C. Chang, T. H. Wagner, C. M. Coopersmith, and I. E. Karl. 2005. Accelerated lymphocyte death in sepsis occurs by both the death receptor and mitochondrial pathways. J. Immunol. 174: 5110-5118.
38. Hotchkiss, R. S., and I. E. Karl. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348: 138-150.
39. Chang, K. C., J. Unsinger, C. G. Davis, S. J. Schwulst, J. T. Muenzer, A. Strasser, and R. S. Hotchkiss. 2007. Multiple triggers of cell death in sepsis: death receptor and mitochondrial-mediated apoptosis. FASEB J. 21: 708-719.
40. Hotchkiss, R. S., K. C. Chang, M. H. Grayson, K. W. Tinsley, B. S. Dunne, C. G. Davis, D. F. Osborne, and I. E. Karl. 2003. Adoptive transfer of apoptotic splenocytes worsens survival, whereas adoptive transfer of necrotic splenocytes improves survival in sepsis. Proc. Natl. Acad. Sci. USA 100: 6724-6729.
41. Wesche, D. E., J.L. Lomas-Neira, M. Perl, C.S. Chung, and A. Ayala. 2005. Leukocyte apoptosis and its significance in sepsis and shock. J. Leukoc. Biol. 78: 325-337.
42. Ayala, A., J. L. Lomas, P. S. Grutkoski, and S. Chung. 2003. Fas-ligand mediated apoptosis in severe sepsis and shock. Scand. J. Infect. Dis. 35: 593-600.
43. Chung, C. S., G.Y. Song, J. Lomas, H.H. Simms, I. H. Chaudry, and A. Ayala. 2003. Inhibition of Fas/Fas ligand signaling improves septic survival: differential effects on macrophage apoptotic and functional capacity. J. Leukoc. Biol. 74: 344-351.
44. Wiley, S. R., K. Schooley, P. J. Smolak, W. S. Din, C. P. Huang, J. K. Nicholl, G. R. Sutherland, T. D. Smith, C. Rauch, C. A. Smith, et al. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682.
45. Renshaw, S. A., J. S. Parmar, V. Singleton, S. J. Rowe, D. H. Dockrell, S. K. Dower, C. D. Bingle, E. R. Chilvers, and M. K. Whyte. 2003. Acceleration of human neutrophil apoptosis by TRAIL. J. Immunol. 170: 1027-1033.
46. Griffith, T. S., and D. H. Lynch. 1998. TRAIL: a molecule with multiple receptors and control mechanisms. Curr. Opin. Immunol. 10: 559-563.
47. Lee, H. O., J. M. Herndon, R. Barreiro, T. S. Griffith, and T. A. Ferguson. 2002. TRAIL: a mechanism of tumor surveillance in an immune privileged site. J. Immunol. 169: 4739-4744.
48. Zheng, S. J., J. Jiang, H. Shen, and Y. H. Chen. 2004. Reduced apoptosis and ameliorated listeriosis in TRAIL-null mice. J. Immunol. 173: 5652-5658.
49. Zheng, S. J., P. Wang, G. Tsabary, and Y. H. Chen. 2004. Critical roles of TRAIL in hepatic cell death and hepatic inflammation. J. Clin. Invest. 113: 58-64.
50. Diehl, G. E., H. H. Yue, K. Hsieh, A. A. Kuang, M. Ho, L. A. Morici, L. L. Lenz, D. Cado, L. W. Riley, and A. Winoto. 2004. TRAIL-R as a negative regulator of innate immune cell responses. Immunity 21: 877-889.
51. Brincks, E. L., T. A. Kucaba, K. L. Legge, and T. S. Griffith. 2008. Influenza-induced expression of functional tumor necrosis factor-related apoptosis-inducing ligand on human peripheral bloodmononuclear cells. Hum. Immunol. 69: 634-646.