Fas-mediated apoptosis regulates the composition of peripheral αβ T cell repertoire by constitutively purging out double negative T cells

PLoS ONE

Volumn 3, Issue 10, 2008, Pages

  Mohamood, Abdiaziz S ^a   Bargatze, Dylan ^a   Xiao, Zuoxiang ^a   Jie, Chunfa ^a   Yagita, Hideo ^b   Ruben, Dawn ^a   Watson, Julie ^a   Chakravarti, Shukti ^a   Schneck, Jonathan P ^a   Hamad, Abdel Rahim A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; FAS ANTIGEN; FAS LIGAND; CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL LABELING; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE MUTATION; HOMEOSTASIS; INTESTINE EPITHELIUM; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEADY STATE; T LYMPHOCYTE; TISSUE DISTRIBUTION; ANIMAL; CELL PROLIFERATION; CYTOLOGY; LYMPHOCYTE COUNT; LYMPHOPROLIFERATIVE DISEASE; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

MUS;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD45; ANTIGENS, CD8; ANTIGENS, CD95; APOPTOSIS; CELL PROLIFERATION; FAS LIGAND PROTEIN; GENE EXPRESSION PROFILING; LYMPHOCYTE COUNT; LYMPHOPROLIFERATIVE DISORDERS; MICE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 54949112078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003465     Document Type: Article

References (58)

1. Worth A, Thrasher AJ, Gaspar HB (2006) Autoimmune lymphoproliferative syndrome: molecular basis of disease and clinical phenotype. Br J Haematol 133: 124-140.
2. Green DR, Droin N, Pinkoski M (2003) Activation-induced cell death in T cells. Immunol Rev 193: 70-81.
3. Krueger A, Fas SC, Baumann S, Krammer PH (2003) The role of CD95 in the regulation of peripheral T-cell apoptosis. Immunol Rev 193: 58-69.
4. Brunner T, Mog R, LaFace D, Yoo N, Mahboubl A, et al. (1995) Cell autonomous Fas (CD95)/Fas ligand interaction mediates activation induced apoptosis in T cell hybridomas. Nature 373: 441-444.
5. Dhein J, Walczack H, Baumler C, Debatin K-M, Krammer P (1995) Autocrine T cell suicide mediated by APO-1 (Fas/CD95). Nature 373: 438-441.
6. Ju S, Panks D, Cul H, Ettingor R, Elkhatib M, et al. (1995) Fas (CD95)/ FasL interactions required for prgrammed cell death after T cell activation. Nature 373: 444-448.
7. Gillette-Ferguson I, Sidman CL (1994) A specific intercellular pathway of apoptotic cell death is defective in the mature peripheral T cells of autoimmune lpr and gld mice. Eur J Immunol 24: 1181-1185.
8. Mogil RJ, Radvanyi L, Gonzalez-Quintial R, Miller R, Mills G, et al. (1995) Fas (CD95) participates in peripheral T cell deletion and associated apoptosis in vivo. Int Immunol 7: 1451-1458.
9. Hildeman DA, Zhu Y, Mitchell TC, Bouillet P, Strasser A, et al. (2002) Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16: 759-767.
10. Gonzalo JA, Tarazona R, Schuurman HJ, Uytdehaag F, Wick G, C, et al. (1994) A single injection of Staphylococcus aureus enterotoxin B reduces autoimmunity in MRL/lpr mice. Clin Immunol Immunopathol 71: 176-182.
11. Lohman BL, Razvi ES, Welsh RM (1996) T-lymphocyte downregulation after acute viral infection is not dependent on CD95 (Fas) receptor-ligand interactions. J Virol 70: 8199-8203.
12. Miethke T, Vabulas R, Bittlingmaier R, Heeg K, Wagner H (1996) Mechanisms of peripheral T cell deletion: anergized T cells are Fas resistant but undergo proliferation-associated apoptosis. Eur J Immunol 26: 1459-1467.
13. Kotzin BL, Babcock SK, Herron LR (1988) Deletion of potentially self-reactive T cell receptor specificities in L3T4-, Lyt-2- T cells of lpr mice. J Exp Med 168: 2221-2229.
14. Singer PA, Balderas RS, McEvilly RJ, Bobardt M, Theofilopoulos AN (1989) Tolerance-related V beta clonal deletions in normal CD4-8-, TCR-alpha/ beta+and abnormal lpr and gld cell populations. J Exp Med 170: 1869-1877.
15. Mountz JD, Smith TM, Toth KS (1990) Altered expression of self-reactive T cell receptor V beta regions in autoimmune mice. J Immunol 144: 2159-2166.
16. Zhou T, Bluethmann H, Zhang J, Edwards CK 3rd, Mountz JD (1992) Defective maintenance of T cell tolerance to a superantigen in MRL-lpr/ lpr mice. J Exp Med 176: 1063-1072.
17. Cohen P, Eisenberg R (1991) Lpr and gld: Single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 9: 243-269.
18. Andrews BS, Eisenberg RA, Theofilopoulos AN, Izui S, Wilson CB, et al. (1978) Spontaneous murine lupus-like syndromes: Clinical and immunopathological manifestations in several strains. J Exp Med 148: 1198-1215.
19. Roths JB, Murphy ED, Eicher EM (1984) A new mutation, gld, that produces lymphoproliferation and autoimmunity in C3H/HeJ mice. J Exp Med 159: 1-20.
20. Watanabe Y, Akaike T (1994) Activation signal induces the expression of B cell-specific CD45R epitope (6B2) on murine T cells. Scand J Immunol 39: 419-425.
21. Renno T, Hahne M, Tschopp J, MacDonald HR (1996) Peripheral T cells undergoing superantigen-induced apoptosis in vivo express B220 and upregulate Fas and Fas ligand. J Exp Med 183: 431-437.
22. Renno T, Attinger A, Rimoldi D, Hahne M, Tschopp J, et al. (1998) Expression of B220 on activated T cell blasts precedes apoptosis. Eur J Immunol 28: 540-547.
23. Sneller M, Wang J, Dale J, Strober W, Middelton L, et al. (1997) Clinical, immunological and genetic features of an autoimmune lymphoproliferative syndrome associated with abnormal lymphocytes apoptosis. Blood 89: 1341-1348.
24. Wang J, Zheng L, Lobito A, Chan F, Dale J, M, et al. (1998) Inherited human Caspase 10 mutations underlie defective lymphocyte and dendritic cell apoptosis in autoimmune lymphoporliferative syndrome type II. Cell 98: 47-58.
25. Clark LB, Appleby MW, Brunkow ME, Wilkinson JE, Ziegler SF, et al. (1999) Cellular and molecular characterization of the scurfy mouse mutant. J Immunol 162: 2546-2554.
26. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061.
27. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, et al. (1995) Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3: 541-547.
28. Giese T, Allison J, Davidson W (1993) Functionally anergic lpr and gld B220+ T cell receptor (TCR)-ab double negative T cells express CD28 and respond to costimulation with phorbol myristate acetate and antibodies to CD28 and the TCR. J immunol 151: 597-609.
29. Ohteki T, Seki S, Abo T, Kumagai K (1990) Liver is a possible site for the proliferation of abnormal CD3+4-8- double-negative lymphocytes in autoimmune MRL-lpr/lpr mice. J Exp Med 172: 7-12.
30. Maldonado MA, Eisenberg RA, Roper E, Cohen PL, Kotzin BL (1995) Greatly reduced lymphoproliferation in lpr mice lacking major histocompatibility complex class I. J Exp Med 181: 641-648.
31. Giese T, Davidson WF (1995) The accumulation of B220+ CD4- CD8- (DN) T cells in C3H-lpr/lpr mice is not accelerated by the stimulation of CD8+ T cells or B220+ DN T cells with staphylococcal enterotoxin B and occurs independently of V beta 8+ T cells. Int Immunol 7: 1213-1223.
32. Giese T, Davidson WF (1994) Chronic treatment of C3H-lpr/lpr and C3H-gld/ gld mice with anti-CD8 monoclonal antibody prevents the accumulation of double negative T cells but not autoantibody production. J Immunol 152: 2000-2010.
33. + thymic precursor. J Immunol 151: 1086-1096.
34. Yamagiwa S, Sugahara S, Shimizu T, Iwanaga T, Yoshida Y, et al. (1998) The primary site of CD4- 8- B220+ alphabeta T cells in lpr mice: the appendix in normal mice. J Immunol 160: 2665-2674.
35. Scherer MT, Ignatowicz L, Winslow GM, Kappler JW, Marrack P (1993) Superantigens: bacterial and viral proteins that manipulate the immune system. Annu Rev Cell Biol 9: 101-128.
36. Inki P, Jalkanen M (1996) The role of syndecan-1 in malignancies. Ann Med 28: 63-67.
37. Nochi T, Yuki Y, Terahara K, Hino A, Kunisawa J, et al. (2004) Biological role of Ep-CAM in the physical interaction between epithelial cells and lymphocytes in intestinal epithelium. Clin Immunol 113: 326-339.
38. Schmidt A, Heid HW, Schafer S, Nuber UA, Zimbelmann R, et al. (1994) Desmosomes and cytoskeletal architecture in epithelial differentiation: cell type-specific plaque components and intermediate filament anchorage. Eur J Cell Biol 65: 229-245.
39. Borrmann CM, Mertens C, Schmidt A, Langbein L, Kuhn C, et al. (2000) Molecular diversity of plaques of epithelial-adhering junctions. Ann N Y Acad Sci 915: 144-150.
40. Inagaki-Ohara K, Sawaguchi A, Suganuma T, Matsuzaki G, Nawa Y (2005) Intraepithelial lymphocytes express junctional molecules in murine small intestine. Biochem Biophys Res Commun 331: 977-983.
41. Hughes RC (2001) Galectins as modulators of cell adhesion. Biochimie 83: 667-676.
42. Hamad AR, Mohamood AS, Trujillo CJ, Huang CT, Yuan E, et al. (2003) B220+ double-negative T cells suppress polyclonal T cell activation by a Fas-independent mechanism that involves inhibition of IL-2 production. J Immunol 171: 2421-2426.
43. Prasad VS, Sidman CL (1991) Cell cycle analysis and DNA aneuploidy in autoimmune mice homozygous for the lpr and gld mutations. J Immunol 147: 4200-4206.
44. Tan KH, Hunziker W (2003) Compartmentalization of Fas and Fas ligand may prevent auto- or paracrine apoptosis in epithelial cells. Exp Cell Res 284: 283-290.
45. Kayagaki N, Yamaguchi N, Nagao F, Matsuo S, Maeda H, et al. (1997) Polymorphism of murine Fas ligand that affects the biological activity. Proc Natl Acad Sci U S A 94: 3914-3919.
46. Mohamood AS, Guler ML, Xiao Z, Zheng D, Hess A, et al. (2007) Protection from autoimmune diabetes and T-cell lymphoproliferation induced by FasL mutation are differentially regulated and can be uncoupled pharmacologically. Am J Pathol 171: 97-106.
47. Hao Z, Hampel B, Yagita H, Rajewsky K (2004) T cell-specific ablation of Fas leads to Fas ligand-mediated lymphocyte depletion and inflammatory pulmonary fibrosis. J Exp Med 199: 1355-1365.
48. Xiao S, Zhang X, Mann KK, Jodo S, Li L, et al. (2004) Changes in sensitivity of peripheral lymphocytes of autoimmune gld mice to FasL-mediated apoptosis reveal a mechanism for the preferential deletion of CD4-CD8-B220+ T cells. Int Immunol 16: 759-766.
49. Mohamood AS, Trujillo CJ, Zheng D, Jie C, Martinez Murillo F, et al. (2006) Gld mutation of Fas ligand increases the frequency and up-regulates cell survival genes in CD25+CD4+ TR cells. Int Immunol 18: 1265-1277.
50. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, AR, et al. (2007) Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26: 629-641.
51. Van Parijs L, Peterson DA, Abbas AK (1998) The Fas/Fas ligand pathway and Bcl-2 regulate T cell responses to model self and foreign antigens. Immunity 8: 265-274.
52. van der Werff Ten Bosch J, Schotte P, Ferster A, Azzi N, Boehler T, Laurey G, et al. (2002) Reversion of autoimmune lymphoproliferative syndrome with an antimalarial drug: preliminary results of a clinical cohort study and molecular observations. Br J Haematol 117: 176-188.
53. Rao VK, Dugan F, Dale JK, Davis J, Tretler J, et al. (2005) Use of mycophenolate mofetil for chronic, refractory immune cytopenias in children with autoimmune lymphoproliferative syndrome. Br J Haematol 129: 534-538.
54. Teachey DT, Seif AE, Brown VI, Bruno M, Bunte RM, et al. (2008) Targeting Notch signaling in autoimmune and lymphoproliferative disease. Blood 111: 705-714.
55. Johansson M, Lycke N (2003) A unique population of extrathymically derived alpha beta TCR+CD4-CD8- T cells with regulatory functions dominates the mouse female genital tract. J Immunol 170: 1659-1666.
56. Davies MD, Parrott DM (1981) Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut 22: 481-488.
57. Tough DF, Sprent J (1994) Turnover of naive- and memory-phenotype T cells. J Exp Med 179: 1127-1135.
58. Kamath AT, Henri S, Battye F, Tough DF, Shortman K (2002) Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 100: 1734-1741.