TSCOT+ thymic epithelial cell-mediated sensitive CD4 tolerance by direct presentation

PLoS Biology

Volumn 6, Issue 8, 2008, Pages 1746-1757

  Ahn, Sejin ^a,e   Lee, Gwanghee ^a,f   Soo, Jung Yang ^a,g   Lee, Deokjae ^b   Lee, Seunghyuk ^b   Hyo, Sun Shin ^b   Min, Cheol Kim ^b   Kee, Nyung Lee ^a,h   Palmer, Douglas C ^c   Theoret, Marc R ^c   Jenkinson, Eric J ^d   Anderson, Graham ^d   Restifo, Nicholas P ^c   Moon, Gyo Kim ^b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b Inha University   (South Korea)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e HARVARD MEDICAL SCHOOL   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g Seoul National University   (South Korea)

^h Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BETA GALACTOSIDASE; CARRIER PROTEIN; CD4 ANTIGEN; CD45 ANTIGEN; CELL MARKER; INTERCELLULAR ADHESION MOLECULE 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; PROTEIN CDR1; PROTEIN S 100; PROTEIN TSCOT; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; COTRANSPORTER; TSCOT PROTEIN, MOUSE;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; BRAIN CORTEX; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL POPULATION; CONTROLLED STUDY; EPITHELIUM CELL; GENE DELETION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PROTEIN EXPRESSION; STROMA CELL; THYMOCYTE; ANIMAL; ANTIGEN PRESENTING CELL; CELL DIFFERENTIATION; CYTOLOGY; DENDRITIC CELL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LACTOSE OPERON; LYMPHOCYTE ACTIVATION; MOUSE; THYMUS; TRANSGENIC MOUSE;

MUS;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS; EPITHELIAL CELLS; IMMUNE TOLERANCE; LAC OPERON; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; STROMAL CELLS; SYMPORTERS; THYMUS GLAND;

EID: 50249171702     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060191     Document Type: Article

References (72)

1. Sprent J, Lo D, Gao EK, Ron Y (1988) T cell selection in the thymus. Immunol Rev 101: 173-190.
2. Ohashi PS (2003) Negative selection and autoimmunity. Curr Opin Immunol 15: 668-676.
3. Schwartz RH (2003) T cell anergy. Annu Rev Immunol 21: 305-334.
4. Arnold B, Schonrich G, Hammerling GJ (1993) Multiple levels of peripheral tolerance. Immunol Today 14: 12-14.
5. Coutinho A (2000) Germ-line selection ensures embryonic autoreactivity and a positive discrimination of self mediated by supraclonal mechanisms. Semin Immunol 12: 205-213.
6. Matzinger P (2002) The danger model: a renewed sense of self. Science 296: 301-305.
7. Anderson G, Lane PJ, Jenkinson EJ (2007) Generating intrathymic microenvironments to establish T-cell tolerance. Nat Rev Immunol 7: 954-963.
8. Kyewski B, Rottinger B, Klein L (2000) Making central T-cell tolerance efficient: thymic stromal cells sample distinct self-antigen pools. Curr Top Microbiol Immunol 251: 139-145.
9. Kyewski B, Derbinski J (2004) Self-representation in the thymus: an extended view. Nat Rev Immunol 4: 688-698.
10. Kyewski B, Klein L (2006) A central role for central tolerance. Annu Rev Immunol 24: 571-606.
11. Pitkanen J, Peterson P (2003) Autoimmune regulator: from loss of function to autoimmunity. Genes Immun 4: 12-21.
12. Villasenor J, Benoist C, Mathis D (2005) AIRE and APECED: molecular insights into an autoimmune disease. Immunol Rev 204: 156-164.
13. Heino M, Peterson P, Kudoh J, Nagamine K, Lagerstedt A, et al. (1999) Autoimmune regulator is expressed in the cells regulating immune tolerance in thymus medulla. Biochem Biophys Res Commun 257: 821-825.
14. Kogawa K, Nagafuchi S, Katsuta H, Kudoh J, Tamiya S, et al. (2002) Expression of AIRE gene in peripheral monocyte/dendritic cell lineage. Immunol Lett 80: 195-198.
15. Derbinski J, Gabler J, Brors B, Tierling S, Jonnakuty S, et al. (2005) Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels. J Exp Med 202: 33-45.
16. Gallegos AM, Bevan MJ (2004) Central tolerance to tissue-specific antigens mediated by direct and indirect antigen presentation. J Exp Med 200: 1039-1049.
17. Houssaint E, Flajnik M (1990) The role of thymic epithelium in the acquisition of tolerance. Immunol Today 11: 357-360.
18. Klein L, Kyewski B (2000) Self-antigen presentation by thymic stromal cells: a subtle division of labor. Curr Opin Immunol 12: 179-186.
19. Laufer TM, Glimcher LH, Lo D (1999) Using thymus anatomy to dissect T cell repertoire selection. Semin Immunol 11: 65-70.
20. Starr TK, Jameson SC, Hogquist KA (2003) Positive and negative selection of T cells. Annu Rev Immunol 21: 139-176.
21. Bonomo A, Matzinger P (1993) Thymus epithelium induces tissue-specific tolerance. J Exp Med 177: 1153-1164.
22. Goldman KP, Park CS, Kim M, Matzinger P, Anderson CC (2005) Thymic cortical epithelium induces self tolerance. Eur J Immunol 35: 709-717.
23. Pimenta-Araujo R, Mascarell L, Huesca M, Cumano A, Bandeira A (2001) Embryonic thymic epithelium naturally devoid of APCs is acutely rejected in the absence of indirect recognition. J Immunol 167: 5034-5041.
24. Ready AR, Jenkinson EJ, Kingston R, Owen JJ (1984) Successful transplantation across major histocompatibility barrier of deoxyguanosine- treated embryonic thymus expressing class II antigens. Nature 310: 231-233.
25. Laufer TM, DeKoning J, Markowitz JS, Lo D, Glimcher LH (1996) Unopposed positive selection and autoreactivity in mice expressing class II MHC only on thymic cortex. Nature 383: 81-85.
26. Capone M, Romagnoli P, Beermann F, MacDonald HR, van Meerwijk JP (2001) Dissociation of thymic positive and negative selection in transgenic mice expressing major histocompatibility complex class I molecules exclusively on thymic cortical epithelial cells. Blood 97: 1336-1342.
27. Frazer IH, Fernando GJ, Fowler N, Leggatt GR, Lambert PF, et al. (1998) Split tolerance to a viral antigen expressed in thymic epithelium and keratinocytes. Eur J Immunol 28: 2791-2800.
28. Mayerova D, Hogquist KA (2004) Central tolerance to self-antigen expressed by cortical epithelial cells. J Immunol 172: 851-856.
29. Volkmann A, Zal T, Stockinger B (1997) Antigen-presenting cells in the thymus that can negatively select MHC class II-restricted T cells recognizing a circulating self antigen. J Immunol 158: 693-706.
30. Goldschneider I, Cone RE (2003) A central role for peripheral dendritic cells in the induction of acquired thymic tolerance. Trends Immunol 24: 77-81.
31. Bonasio R, Scimone ML, Schaerli P, Grabie N, Lichtman AH, et al. (2006) Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat Immunol 7: 1092-1100.
32. Hengartner H, Odermatt B, Schneider R, Schreyer M, Walle G, et al. (1988) Deletion of self-reactive T cells before entry into the thymus medulla. Nature 336: 388-390.
33. Murphy KM, Heimberger AB, Loh DY (1990) Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250: 1720-1723.
34. Lorenz RG, Allen PM (1989) Thymic cortical epithelial cells can present self-antigens in vivo. Nature 337: 560-562.
35. Kasai M, Hirokawa K, Kajino K, Ogasawara K, Tatsumi M, et al. (1996) Difference in antigen presentation pathways between cortical and medullary thymic epithelial cells. Eur J Immunol 26: 2101-2107.
36. Mizuochi T, Kasai M, Kokuho T, Kakiuchi T, Hirokawa K (1992) Medullary but not cortical thymic epithelial cells present soluble antigens to helper T cells. J Exp Med 175: 1601-1605.
37. Gray DH, Seach N, Ueno T, Milton MK, Liston A, et al. (2006) Developmental kinetics, turnover, and stimulatory capacity of thymic epithelial cells. Blood 108: 3777-3785.
38. Kim MG, Flomerfelt FA, Lee KN, Chen C, Schwartz RH (2000) A putative 12 transmembrane domain cotransporter expressed in thymic cortical epithelial cells. J Immunol 164: 3185-3192.
39. Chen C, Kim MG, Soo Lyu M, Kozak CA, Schwartz RH, et al. (2000) Characterization of the mouse gene, human promoter and human cDNA of TSCOT reveals strong interspecies homology. Biochim Biophys Acta 1493: 159-169.
40. Rouse RV, Bolin LM, Bender JR, Kyewski BA (1988) Monoclonal antibodies reactive with subsets of mouse and human thymic epithelial cells. J Histochem Cytochem 36: 1511-1517.
41. Yang SJ, Ahn S, Park CS, Choi S, Kim MG (2005) Identifying subpopulations of thymic epithelial cells by flow cytometry using a new specific thymic epithelial marker, Ly110. J Immunol Methods 297: 265-270.
42. Nehls M, Kyewski B, Messerle M, Waldschutz R, Schuddekopf K, et al. (1996) Two genetically separable steps in the differentiation of thymic epithelium. Science 272: 886-889.
43. Yang SJ (2006) The quantitative assessment of MHC II on thymic epithelium: implications in cortical thymocyte development. Int Immunol 18: 729-739.
44. 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.
45. Liston A, Lesage S, Wilson J, Peltonen L, Goodnow CC (2003) Aire regulates negative selection of organ-specific T cells. Nat Immunol 4: 350-354.
46. Uchida D, Hatakeyama S, Matsushima A, Han H, Ishido S, et al. (2004) AIRE functions as an E3 ubiquitin ligase. J Exp Med 199: 167-172.
47. Yang SJ, Ahn S, Park CS, Holmes KL, Westrup J, et al. (2006) The quantitative assessment of MHC II on thymic epithelium: implications in cortical thymocyte development. Int Immunol 18: 729-739.
48. Surman DR, Dudley ME, Overwijk WW, Restifo NP (2000) Cutting edge: CD4+ T cell control of CD8+ T cell reactivity to a model tumor antigen. J Immunol 164: 562-565.
49. 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.
50. Jenkinson EJ, Anderson G (1994) Fetal thymic organ cultures. Curr Opin Immunol 6: 293-297.
51. Gray DH, Chidgey AP, Boyd RL (2002) Analysis of thymic stromal cell populations using flow cytometry. J Immunol Methods 260: 15-28.
52. Klug DB, Carter C, Crouch E, Roop D, Conti CJ, et al. (1998) Interdependence of cortical thymic epithelial cell differentiation and T-lineage commitment. Proc Natl Acad Sci U S A 95: 11822-11827.
53. Klug DB, Carter C, Gimenez-Conti IB, Richie ER (2002) Cutting edge: thymocyte-independent and thymocyte-dependent phases of epithelial patterning in the fetal thymus. J Immunol 169: 2842-2845.
54. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, et al. (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
55. 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.
56. Peterson DA, DiPaolo RJ, Kanagawa O, Unanue ER (1999) Cutting edge: negative selection of immature thymocytes by a few peptide-MHC complexes: differential sensitivity of immature and mature T cells. J Immunol 162: 3117-3120.
57. Scollay R, Godfrey DI (1995) Thymic emigration: conveyor belts or lucky dips? Immunol Today 16: 268-273.
58. Shortman K, Egerton M, Spangrude GJ, Scollay R (1990) The generation and fate of thymocytes. Semin Immunol 2: 3-12.
59. Ramsdell F, Fowlkes BJ (1990) Clonal deletion versus clonal anergy: the role of the thymus in inducing self tolerance. Science 248: 1342-1348.
60. Schonrich G, Momburg F, Hammerling GJ, Arnold B (1992) Anergy induced by thymic medullary epithelium. Eur J Immunol 22: 1687-1691.
61. von Boehmer H, Kisielow P (2006) Negative selection of the T-cell repertoire: where and when does it occur? Immunol Rev 209: 284-289.
62. Takahama Y, Shores EW, Singer A (1992) Negative selection of precursor thymocytes before their differentiation into CD4+CD8+ cells. Science 258: 653-656.
63. Kishimoto H, Cai Z, Brunmark A, Jackson MR, Peterson PA, et al. (1996) Differing roles for B7 and intercellular adhesion molecule-1 in negative selection of thymocytes. J Exp Med 184: 531-537.
64. Gotter J, Kyewski B (2004) Regulating self-tolerance by deregulating gene expression. Curr Opin Immunol 16: 741-745.
65. Su MA, Anderson MS (2004) Aire: an update. Curr Opin Immunol 16: 746-752.
66. Robey E, Fowlkes BJ (1994) Selective events in T cell development. Annu Rev Immunol 12: 675-705.
67. Singer A (2002) New perspectives on a developmental dilemma: the kinetic signaling model and the importance of signal duration for the CD4/CD8 lineage decision. Curr Opin Immunol 14: 207-215.
68. Vukmanovic S, Jameson SC, Bevan MJ (1994) A thymic epithelial cell line induces both positive and negative selection in the thymus. Int Immunol 6: 239-246.
69. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, et al. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354.
70. Viret C, Barlow AK, Janeway CA Jr (1999) On the intrathymic intercellular transfer of self-determinants. Immunol Today 20: 8-10.
71. Klein L, Roettinger B, Kyewski B (2001) Sampling of complementing self-antigen pools by thymic stromal cells maximizes the scope of central T cell tolerance. Eur J Immunol 31: 2476-2486.
72. Kouskoff V, Vonesch JL, Benoist C, Mathis D (1995) The influence of positive selection on RAG expression in thymocytes. Eur J Immunol 25: 54-58.