Antigen Recognition By Autoreactive Cd4+ Thymocytes Drives Homeostasis Of The Thymic Medulla

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Irla, Magali ^a,e   Guerri, Lucia ^b   Guenot, Jeanne ^a   Sergé, Arnauld ^a,f   Lantz, Olivier ^b   Liston, Adrian ^c   Imhof, Beat A ^a   Palmer, Ed ^d   Reith, Walter ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b PSL RESEARCH UNIVERSITY   (France)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^f AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; LYMPHOTOXIN; OSTEOCLAST DIFFERENTIATION FACTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; T LYMPHOCYTE RECEPTOR;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ THYMOCYTE; CELL COUNT; CELL EXPANSION; CONTROLLED STUDY; CROSS REACTION; EMBRYO; FLOW CYTOMETRY; IMMUNOREACTIVITY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYMOCYTE; WILD TYPE;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD40; AUTOANTIGENS; BODY PATTERNING; CD40 LIGAND; CELL PROLIFERATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HOMEOSTASIS; LYMPHOTOXIN BETA RECEPTOR; LYMPHOTOXIN-ALPHA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; SIGNAL TRANSDUCTION; THYMOCYTES; THYMUS GLAND; TISSUE CULTURE TECHNIQUES;

MUS;

EID: 84871661087     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052591     Document Type: Article

References (47)

1. Derbinski J, Schulte A, Kyewski B, Klein L, (2001) Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat Immunol 2: 1032-1039.
2. Anderson MS, Venanzi ES, Klein L, Chen Z, Berzins SP, et al. (2002) Projection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401.
3. Kyewski B, Klein L, (2006) A central role for central tolerance. Annu Rev Immunol 24: 571-606.
4. Gallegos AM, Bevan MJ, (2004) Central tolerance to tissue-specific antigens mediated by direct and indirect antigen presentation. J Exp Med 200: 1039-1049.
5. Hinterberger M, Aichinger M, da Costa OP, Voehringer D, Hoffmann R, et al. (2010) Autonomous role of medullary thymic epithelial cells in central CD4(+) T cell tolerance. Nat Immunol 11: 512-519.
6. Aschenbrenner K, D'Cruz LM, Vollmann EH, Hinterberger M, Emmerich J, et al. (2007) Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat Immunol 8: 351-358.
7. Proietto AI, van Dommelen S, Zhou P, Rizzitelli A, D'Amico A, et al. (2008) Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci U S A 105: 19869-19874.
8. Klein L, Hinterberger M, von Rohrscheidt J, Aichinger M, (2011) Autonomous versus dendritic cell-dependent contributions of medullary thymic epithelial cells to central tolerance. Trends in immunology 32: 188-193.
9. Philpott KL, Viney JL, Kay G, Rastan S, Gardiner EM, et al. (1992) Lymphoid development in mice congenitally lacking T cell receptor alpha beta-expressing cells. Science 256: 1448-1452.
10. Negishi I, Motoyama N, Nakayama K, Nakayama K, Senju S, et al. (1995) Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature 376: 435-438.
11. Palmer DB, Viney JL, Ritter MA, Hayday AC, Owen MJ, (1993) Expression of the alpha beta T-cell receptor is necessary for the generation of the thymic medulla. Dev Immunol 3: 175-179.
12. van Ewijk W, Shores EW, Singer A, (1994) Crosstalk in the mouse thymus. Immunol Today 15: 214-217.
13. Irla M, Hollander G, Reith W, (2010) Control of central self-tolerance induction by autoreactive CD4+ thymocytes. Trends Immunol 31: 71-79.
14. Irla M, Hugues S, Gill J, Nitta T, Hikosaka Y, et al. (2008) Autoantigen-specific interactions with CD4+ thymocytes control mature medullary thymic epithelial cell cellularity. Immunity 29: 451-463.
15. Rossi SW, Kim MY, Leibbrandt A, Parnell SM, Jenkinson WE, et al. (2007) RANK signals from CD4(+)3(-) inducer cells regulate development of Aire-expressing epithelial cells in the thymic medulla. J Exp Med 204: 1267-1272.
16. Akiyama T, Shimo Y, Yanai H, Qin J, Ohshima D, et al. (2008) The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-tolerance. Immunity 29: 423-437.
17. Hikosaka Y, Nitta T, Ohigashi I, Yano K, Ishimaru N, et al. (2008) The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 29: 438-450.
18. Zhu M, Fu YX, (2008) Coordinating development of medullary thymic epithelial cells. Immunity 29: 386-388.
19. Boehm T, Scheu S, Pfeffer K, Bleul CC, (2003) Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbetaR. J Exp Med 198: 757-769.
20. Venanzi ES, Gray DH, Benoist C, Mathis D, (2007) Lymphotoxin pathway and Aire influences on thymic medullary epithelial cells are unconnected. J Immunol 179: 5693-5700.
21. Mouri Y, Yano M, Shinzawa M, Shimo Y, Hirota F, et al. (2011) Lymphotoxin Signal Promotes Thymic Organogenesis by Eliciting RANK Expression in the Embryonic Thymic Stroma. J Immunol.
22. Zijlstra M, Bix M, Simister NE, Loring JM, Raulet DH, et al. (1990) Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature 344: 742-746.
23. Kontgen F, Suss G, Stewart C, Steinmetz M, Bluethmann H, (1993) Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int Immunol 5: 957-964.
24. Waldburger JM, Suter T, Fontana A, Acha-Orbea H, Reith W, (2001) Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J Exp Med 194: 393-406.
25. Mombaerts P, Clarke AR, Rudnicki MA, Iacomini J, Itohara S, et al. (1992) Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 360: 225-231.
26. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, et al. (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
27. Lantz O, Grandjean I, Matzinger P, Di Santo JP, (2000) Gamma chain required for naive CD4+ T cell survival but not for antigen proliferation. Nat Immunol 1: 54-58.
28. Backstrom BT, Muller U, Hausmann B, Palmer E, (1998) Positive selection through a motif in the alphabeta T cell receptor. Science 281: 835-838.
29. Huseby ES, White J, Crawford F, Vass T, Becker D, et al. (2005) How the T cell repertoire becomes peptide and MHC specific. Cell 122: 247-260.
30. De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, et al. (1994) Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703-707.
31. Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, et al. (1997) B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6: 303-313.
32. Shahinian A, Pfeffer K, Lee KP, Kundig TM, Kishihara K, et al. (1993) Differential T cell costimulatory requirements in CD28-deficient mice. Science 261: 609-612.
33. Kim JM, Rasmussen JP, Rudensky AY, (2007) Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nature immunology 8: 191-197.
34. Kurts C, Heath WR, Carbone FR, Allison J, Miller JF, et al. (1996) Constitutive class I-restricted exogenous presentation of self antigens in vivo. J Exp Med 184: 923-930.
35. Barnden MJ, Allison J, Heath WR, Carbone FR, (1998) Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol 76: 34-40.
36. Dejardin E, Droin NM, Delhase M, Haas E, Cao Y, et al. (2002) The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 17: 525-535.
37. Anderson G, Jenkinson EJ, Moore NC, Owen JJ, (1993) MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 362: 70-73.
38. van Ewijk W, Hollander G, Terhorst C, Wang B, (2000) Stepwise development of thymic microenvironments in vivo is regulated by thymocyte subsets. Development 127: 1583-1591.
39. Waldburger JM, Rossi S, Hollander GA, Rodewald HR, Reith W, et al. (2003) Promoter IV of the class II transactivator gene is essential for positive selection of CD4+ T cells. Blood 101: 3550-3559.
40. Anderson MS, Venanzi ES, Chen Z, Berzins SP, Benoist C, et al. (2005) The cellular mechanism of Aire control of T cell tolerance. Immunity 23: 227-239.
41. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, et al. (2000) B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
42. Tang Q, Henriksen KJ, Boden EK, Tooley AJ, Ye J, et al. (2003) Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. Journal of immunology 171: 3348-3352.
43. Shores EW, Van Ewijk W, Singer A, (1991) Disorganization and restoration of thymic medullary epithelial cells in T cell receptor-negative scid mice: evidence that receptor-bearing lymphocytes influence maturation of the thymic microenvironment. Eur J Immunol 21: 1657-1661.
44. Surh CD, Ernst B, Sprent J, (1992) Growth of epithelial cells in the thymic medulla is under the control of mature T cells. J Exp Med 176: 611-616.
45. McCaughtry TM, Wilken MS, Hogquist KA, (2007) Thymic emigration revisited. J Exp Med 204: 2513-2520.
46. Le Borgne M, Ladi E, Dzhagalov I, Herzmark P, Liao YF, et al. (2009) The impact of negative selection on thymocyte migration in the medulla. Nat Immunol 10: 823-830.
47. Heikenwalder M, Prinz M, Zeller N, Lang KS, Junt T, et al. (2008) Overexpression of lymphotoxin in T cells induces fulminant thymic involution. Am J Pathol 172: 1555-1570.