Peripheral CD8 T-cell responses to apoptotic cell proteins and peptides

Critical Reviews in Immunology

Volumn 27, Issue 4, 2007, Pages 357-365

  Peng, Yu Feng ^a   Elkon, Keith B ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptotic cells; Costimulation; Dendritic cells; Tolerance

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

ANTIGEN PRESENTING CELL; APOPTOSIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE SUBPOPULATION;

EID: 38049017419     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v27.i4.50     Document Type: Review

References (72)

1. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature. 1991;351(6324):290-6.
2. Rocha B, Tanchot C, Von Boehmer H. Clonal anergy blocks in vivo growth of mature T cells and can be reversed in the absence of antigen. J Exp Med. 1993;177(5):1517-21.
3. Kurts C, Kosaka H, Carbone FR, Miller JF, Heath WR. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J Exp Med. 1997;186(2):239-45.
4. Hernandez J, Aung S, Redmond WL, Sherman LA. Phenotypic and functional analysis of CD8(+) T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J Exp Med. 2001;194(6):707-17.
5. Ohlen C, Kalos M, Cheng LE, Shur AC, Hong DJ, Carson BD, Kokot NC, Lerner CG, Sather BD, Huseby ES, Greenberg PD. CD8(+) T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J Exp Med. 2002;195(11):1407-18.
6. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol. 2002;2(12):965-75.
7. Wong FS, Karttunen J, Dumont C, Wen L, Visintin I, Pilip IM, Shastri N, Pamer EG, Janeway CA Jr. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat Med. 1999;5(9):1026-31.
8. Amrani A, Verdaguer J, Serra P, Tafuro S, Tan R, Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature. 2000;406(6797):739-42.
9. Probst HC, Lagnel J, Kollias G, van den Broek M. Inducible transgenic mice reveal resting dendritic cells as potent inducers of CD8+ T cell tolerance. Immunity. 2003;18(5):713-20.
10. Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M, Ravetch JV, Steinman RM, Nussenzweig MC. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med. 2001;194(6):769-79.
11. Norbury CC, Basta S, Donohue KB, Tscharke DC, Princiotta MF, Berglund P, Gibbs J, Bennink JR, Yewdell JW. CD8+ T cell cross-priming via transfer of proteasome substrates. Science. 2004;304(5675):1318-21.
12. Reis e Sousa C, Germain RN. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis. J Exp Med. 1995;182(3):841-51.
13. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, Lacy-Hulbert A. Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol. 2002;168(4):1627-35.
14. Kim S, Elkon KB, Ma X. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity. 2004;21(5):643-53.
15. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell. 2004;14(3):277-87.
16. Peng Y, Kowalewski R, Kim S, Elkon KB. The role of IgM antibodies in the recognition and clearance of apoptotic cells. Mol Immunol. 2005;42(7):781-7.
17. Botto M, Dell'Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet. 1998;19(1):56-9.
18. Hanayama R, Tanaka M, Miyasaka K, Aozasa K, Koike M, Uchiyama Y, Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 2004;304(5674):1147-50.
19. Bickerstaff MC, Botto M, Hutchinson WL, Herbert J, Tennent GA, Bybee A, Mitchell DA, Cook HT, Butler PJ, Walport MJ, Pepys MB. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat Med. 1999;5(6):694-7.
20. Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey RA, Earp HS, Matsushima G, Reap EA. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med. 2002;196(1):135-40.
21. Bygrave AE, Rose KL, Cortes-Hernandez J, Warren J, Rigby RJ, Cook HT, Walport MJ, Vyse TJ, Botto M. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in genetargeted mice. PLoS Biol. 2004;2(8):E243.
22. Carbone FR, Belz GT, Heath WR. Transfer of antigen between migrating and lymph node-resident DCs in peripheral T-cell tolerance and immunity. Trends Immunol. 2004;25(12):655-8.
23. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P, Santamaria P, Locksley RM, Krummel MF, Bluestone JA. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol. 2006;7(1):83-92.
24. Turley S, Poirot L, Hattori M, Benoist C, Mathis D. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J Exp Med. 2003;198(10):1527-37.
25. Scheinecker C, McHugh R, Shevach EM, Germain RN. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J Exp Med. 2002;196(8):1079-90.
26. Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y, Maeda Y, Takahara K, Steinman RM, Inaba K. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med. 2002;195(10):1289-302.
27. Inaba K, Turley S, Yamaide F, Iyoda T, Mahnke K, Inaba M, Pack M, Subklewe M, Sauter B, Sheff D, Albert M, Bhardwaj N, Mellman I, Steinman RM. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med. 1998;188(11):2163-73.
28. Ochando JC, Homma C, Yang Y, Hidalgo A, Garin A, Tacke F, Angeli V, Li Y, Boros P, Ding Y, Jessberger R, Trinchieri G, Lira SA, Randolph GJ, Bromberg JS. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat Immunol. 2006;7(6):652-62.
29. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I. Activation of lysosomal function during dendritic cell maturation. Science. 2003;299(5611):1400-3.
30. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell. 2002;111(7):927-30.
31. Kalinski P, Hilkens CM, Snijders A, Snijdewint FG, Kapsenberg ML. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J Immunol. 1997;159(1):28-35.
32. Randolph GJ, Sanchez-Schmitz G, Angeli V. Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin Immunopathol. 2005;26(3):273-87.
33. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, Wu S, Vuthoori S, Ko K, Zavala F, Pamer EG, Littman DR, Lang RA. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity. 2002;17(2):211-20.
34. Probst HC, Tschannen K, Odermatt B, Schwendener R, Zinkernagel RM, Van Den Broek M. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin Exp Immunol. 2005;141(3):398-404.
35. Ramirez MC, Sigal LJ. Macrophages and dendritic cells use the cytosolic pathway to rapidly cross-present antigen from live, vaccinia-infected cells. J Immunol. 2002;169(12):6733-42.
36. den Haan JM, Lehar SM, Bevan MJ. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med. 2000;192(12):1685-96.
37. Belz GT, Behrens GM, Smith CM, Miller JF, Jones C, Lejon K, Fathman CG, Mueller SN, Shortman K, Carbone FR, Heath WR. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med. 2002;196(8):1099-104.
38. Schnorrer P, Behrens GM, Wilson NS, Pooley JL, Smith CM, El-Sukkari D, Davey G, Kupresanin F, Li M, Maraskovsky E, Belz GT, Carbone FR, Shortman K, Heath WR, Villadangos JA. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U S A. 2006;103(28):10729-34.
39. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol. 2000;164(6):2978-86.
40. Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature. 1998;392(6671):86-9.
41. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature. 2006;440(7085):808-12.
42. Hoglund P, Mintern J, Waltzinger C, Heath W, Benoist C, Mathis D. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J Exp Med. 1999;189(2):331-9.
43. Kurts C, Carbone FR, Barnden M, Blanas E, Allison J, Heath WR, Miller JF. CD4+ T cell help impairs CD8+ T cell deletion induced by cross- presentation of self-antigens and favors autoimmunity. J Exp Med. 1997;186(12):2057-62.
44. Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, O'Keeffe M, Shortman K. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol. 2006;7(6):663-71.
45. Haring JS, Badovinac VP, Harty JT. Inflaming the CD8+ T cell response. Immunity. 2006;25(1):19-29.
46. Sporri R, Reis e Sousa C. Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nat Immunol. 2005;6(2):163-70.
47. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature. 2003;425(6957):516-21.
48. Janssen E, Tabeta K, Barnes MJ, Rutschmann S, McBride S, Bahjat KS, Schoenberger SP, Theofilopoulos AN, Beutler B, Hoebe K. Efficient T cell activation via a Toll-interleukin 1 receptor-independent pathway. Immunity. 2006;24(6):787-99.
49. Millar DG, Garza KM, Odermatt B, Elford AR, Ono N, Li Z, Ohashi PS. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat Med. 2003;9(12):1469-76.
50. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191-5.
51. Schwartz RH. T cell anergy. Annu Rev Immunol. 2003;21:305-34.
52. Otten GR, Germain RN. Split anergy in a CD8+ T cell: receptor-dependent cytolysis in the absence of interleukin-2 production. Science. 1991;251(4998):1228-31.
53. Perez VL, Van Parijs L, Biuckians A, Zheng XX, Strom TB, Abbas AK. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity. 1997;6(4):411-7.
54. Greenwald RJ, Boussiotis VA, Lorsbach RB, Abbas AK, Sharpe AH. CTLA-4 regulates induction of anergy in vivo. Immunity. 2001;14(2):145-55.
55. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A, Bluestone JA. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000;12(4):431-40.
56. Kurts C, Heath WR, Kosaka H, Miller JF, Carbone FR. The peripheral deletion of autoreactive CD8+ T cells induced by cross-presentation of self-antigens involves signaling through CD95 (Fas, Apo-1). J Exp Med. 1998;188(2):415-20.
57. Kurts C, Miller JF, Subramaniam RM, Carbone FR, Heath WR. Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J Exp Med. 1998;188(2):409-14.
58. Hernandez J, Aung S, Marquardt K, Sherman LA. Uncoupling of proliferative potential and gain of effector function by CD8(+) T cells responding to self-antigens. J Exp Med. 2002;196(3):323-33.
59. Adler AJ, Marsh DW, Yochum GS, Guzzo JL, Nigam A, Nelson WG, Pardoll DM. CD4+ T cell tolerance to parenchymal self-antigens requires presentation by bone marrow-derived antigen-presenting cells. J Exp Med. 1998;187(10):1555-64.
60. Frauwirth KA, Alegre ML, Thompson CB. CTLA-4 is not required for induction of CD8(+) T cell anergy in vivo. J Immunol. 2001;167(9):4936-41.
61. Redmond WL, Marincek BC, Sherman LA. Distinct requirements for deletion versus anergy during CD8 T cell peripheral tolerance in vivo. J Immunol. 2005;174(4):2046-53.
62. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol. 2003;4(12):1191-8.
63. Davey GM, Kurts C, Miller JF, Bouillet P, Strasser A, Brooks AG, Carbone FR, Heath WR. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J Exp Med. 2002;196(7):947-55.
64. Hoffmann P, Eder R, Kunz-Schughart LA, Andreesen R, Edinger M. Large-scale in vitro expansion of polyclonal human CD4(+)CD25high regulatory T cells. Blood. 2004;104(3):895-903.
65. Apostolou I, von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med. 2004;199(10):1401-8.
66. Kretschmer K, Apostolou I, Jaeckel E, Khazaie K, von Boehmer H. Making regulatory T cells with defined antigen specificity: role in autoimmunity and cancer. Immunol Rev. 2006;212:163-9.
67. Chen W, Frank ME, Jin W, Wahl SM. TGF-beta released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity. 2001;14(6):715-25.
68. Kleinclauss F, Perruche S, Masson E, de Carvalho Bittencourt M, Biichle S, Remy-Martin JP, Ferrand C, Martin M, Bittard H, Chalopin JM, Seilles E, Tiberghien P, Saas P. Intravenous apoptotic spleen cell infusion induces a TGF-beta-dependent regulatory T-cell expansion. Cell Death Differ. 2006;13(1):41-52.
69. Zehn D, Bevan MJ. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity. 2006;25(2):261-70.
70. Kawane K, Ohtani M, Miwa K, Kizawa T, Kanbara Y, Yoshioka Y, Yoshikawa H, Nagata S. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature. 2006;443(7114):998-1002.
71. -/- mice. J Cell Biol. 2004;167(6):1161-70.
72. Stuart LM, Takahashi K, Shi L, Savill J, Ezekowitz RA. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol. 2005;174(6):3220-6.