Elimination of Self-Reactive T Cells in the Thymus: A Timeline for Negative Selection

PLoS Biology

Volumn 11, Issue 5, 2013, Pages

  Dzhagalov, Ivan Lilyanov ^a   Chen, Katherine Grace ^a   Herzmark, Paul ^a   Robey, Ellen A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CASPASE 3; PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL SELECTION; CELL SYNCHRONIZATION; CHROMATIN; CLEARANCE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PHAGOCYTOSIS; T LYMPHOCYTE; T LYMPHOCYTE ELIMINATION; THYMOCYTE; THYMUS;

ANIMALS; APOPTOSIS; CASPASE 3; CELL DEATH; MICE; MICE, INBRED STRAINS; PHAGOCYTOSIS; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84878289907     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001566     Document Type: Article

References (49)

1. Starr T, Jameson S, Hogquist K, (2003) Positive and negative selection of T cells. Annu Rev Immunol 21: 139-176 doi:10.1146/annurev.immunol.21.120601.141107.
2. Kappler JW, Roehm N, Marrack P, (1987) T cell tolerance by clonal elimination in the thymus. Cell 49: 273-280.
3. Kisielow P, Blüthmann H, Staerz UD, Steinmetz M, Boehmer von H, (1988) Tolerance in T-cell-receptor transgenic mice involves deletion of nonmature CD 4+ 8+ thymocytes. Nature 333: 742-746.
4. Pircher H, Bürki K, Lang R, Hengartner H, Zinkernagel RM, (1989) Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342: 559-561 doi:10.1038/342559a0.
5. Murphy KM, Heimberger AB, Loh DY, (1990) Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250: 1720-1723.
6. Wack A, Ladyman HM, Williams O, Roderick K, Ritter MA, et al. (1996) Direct visualization of thymocyte apoptosis in neglect, acute and steady-state negative selection. Int Immunol 8: 1537-1548.
7. Tarazona R, Williams O, Moskophidis D, Smyth LA, Tanaka Y, et al. (1998) Susceptibility and resistance to antigen-induced apoptosis in the thymus of transgenic mice. J Immunol 160: 5397-5403.
8. Zhan Y, Purton JF, Godfrey DI, Cole TJ, Heath WR, et al. (2003) Without peripheral interference, thymic deletion is mediated in a cohort of double-positive cells without classical activation. Proc Natl Acad Sci U S A 100: 1197-1202 doi:10.1073/pnas.0237316100.
9. Vasquez NJ, Kaye J, Hedrick SM, (1992) In vivo and in vitro clonal deletion of double-positive thymocytes. J Exp Med 175: 1307-1316.
10. Swat W, Ignatowicz L, Boehmer von H, Kisielow P, (1991) Clonal deletion of immature CD4+8+ thymocytes in suspension culture by extrathymic antigen-presenting cells. Nature 351: 150-153 doi:10.1038/351150a0.
11. Mcgargill MA, Hogquist KA, (1999) Antigen-induced coreceptor down-regulation on thymocytes is not a result of apoptosis. J Immunol 162: 1237-1245.
12. Martin S, Bevan MJ, (1997) Antigen-specific and nonspecific deletion of immature cortical thymocytes caused by antigen injection. Eur J Immunol 27: 2726-2736 doi:10.1002/eji.1830271037.
13. Brewer JA, Kanagawa O, Sleckman BP, Muglia LJ, (2002) Thymocyte apoptosis induced by T cell activation is mediated by glucocorticoids in vivo. J Immunol 169: 1837-1843.
14. McCaughtry TM, Baldwin TA, Wilken MS, Hogquist KA, (2008) Clonal deletion of thymocytes can occur in the cortex with no involvement of the medulla. J Exp Med 205: 2575-2584 doi:10.1084/jem.20080866.
15. Green DR, (2011) The End and After: How Dying Cells Impact the Living Organism. Immunity 35: 441-444 doi:10.1016/j.immuni.2011.10.003.
16. Ravichandran KS, (2010) Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J Exp Med 207: 1807-1817 doi:10.1084/jem.20101157.
17. Surh CD, Sprent J, (1994) T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372: 100-103 doi:10.1038/372100a0.
18. Bousso P, (2008) T-cell activation by dendritic cells in the lymph node: lessons from the movies. Nat Rev Immunol 8: 675-684 doi:10.1038/nri2379.
19. Henrickson SE, Mempel TR, Mazo IB, Liu B, Artyomov MN, et al. (2008) T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol 9: 282-291 doi:10.1038/ni1559.
20. Mempel TR, Henrickson SE, Von Andrian UH, (2004) T-cell priming by dendriticcells in lymph nodes occurs in three distinct phases. Nature 427: 154-159 doi:10.1038/nature02238.
21. Le Borgne M, Ladi E, Dzhagalov IL, Herzmark P, Liao YF, et al. (2009) The impact of negative selection on thymocyte migration in the medulla. Nat Immunol 10: 823-830 doi:10.1038/ni.1761.
22. Klein L, Hinterberger M, Wirnsberger G, Kyewski B, (2009) Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 9: 833-844 doi:10.1038/nri2669.
23. Mathis D, Benoist C, (2009) Aire. Annu Rev Immunol 27: 287-312 doi:10.1146/annurev.immunol.25.022106.141532.
24. Suen AYW, Baldwin TA, (2012) Proapoptotic protein Bim is differentially required during thymic clonal deletion to ubiquitous versus tissue-restricted antigens. Proc Natl Acad Sci U S A 109: 893-898 doi:10.1073/pnas.1114834109.
25. Kersh GJ, Hedrick SM, (1995) Role of TCR specificity in CD4 versus CD8 lineage commitment. J Immunol 154: 1057-1068.
26. Bhakta NR, Oh DY, Lewis RS, (2005) Calcium oscillations regulate thymocyte motility during positive selection in the three-dimensional thymic environment. Nat Immunol 6: 143-151 doi:10.1038/ni1161.
27. Campbell JJ, Pan J, Butcher EC, (1999) Cutting edge: developmental switches in chemokine responses during T cell maturation. J Immunol 163: 2353-2357.
28. Yin X, Ladi E, Chan SW, Li O, Killeen N, et al. (2007) CCR7 expression in developing thymocytes is linked to the CD4 versus CD8 lineage decision. J Immunol 179: 7358-7364.
29. Ehrlich LIR, Oh DY, Weissman IL, Lewis RS, (2009) Differential contribution of chemotaxis and substrate restriction to segregation of immature and mature thymocytes. Immunity 31: 986-998 doi:10.1016/j.immuni.2009.09.020.
30. Mempel TR, Pittet MJ, Khazaie K, Weninger W, Weissleder R, et al. (2006) Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 25: 129-141 doi:10.1016/j.immuni.2006.04.015.
31. Faust N, Varas F, Kelly LM, Heck S, Graf T, (2000) Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96: 719-726.
32. Derbinski J, Pinto S, Roesch S, Hexel K, Kyewski B, (2008) Promiscuous gene expression patterns in single medullary thymic epithelial cells argue for a stochastic mechanism. Proc Natl Acad Sci USA 105: 657-662 doi:10.1073/pnas.0707486105.
33. Ueda Y, Katagiri K, Tomiyama T, Yasuda K, Habiro K, et al. (2012) Mst1 regulates integrin-dependent thymocyte trafficking and antigen recognition in the thymus. Nat Comm 3: 1098-13 doi:10.1038/ncomms2105.
34. Stritesky GL, Jameson SC, Hogquist KA, (2012) Selection of Self-Reactive T Cells in the Thymus. Annu Rev Immunol 30: 95-114 doi:10.1146/annurev-immunol-020711-075035.
35. McCaughtry TM, Wilken MS, Hogquist KA, (2007) Thymic emigration revisited. J Exp Med 204: 2513-2520 doi:10.1084/jem.20070601.
36. Enouz S, Carrié L, Merkler D, Bevan MJ, Zehn D, (2012) Autoreactive T cells bypass negative selection and respond to self-antigen stimulation during infection. J Exp Med 209: 1769-1779 doi:10.1084/jem.20120905.
37. Ravichandran KS, (2011) Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35: 445-455 doi:10.1016/j.immuni.2011.09.004.
38. van Ham TJ, Kokel D, Peterson RT, (2012) Apoptotic Cells Are Cleared by Directional Migration and elmo1- Dependent Macrophage Engulfment. Curr Biol 22: 830-836 doi:10.1016/j.cub.2012.03.027.
39. Taatjes DJ, Sobel BE, Budd RC, (2007) Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 129: 33-43 doi:10.1007/s00418-007-0356-9.
40. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, et al. (2007) Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14: 1237-1243 doi:10.1038/sj.cdd.4402148.
41. 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.
42. Guerri L, Peguillet I, Geraldo Y, Nabti S, Premel V, et al. (2013) Analysis of APC Types Involved in CD4 Tolerance and Regulatory T Cell Generation Using Reaggregated Thymic Organ Cultures. J Immunol doi:10.4049/jimmunol.1202883.
43. MacDonald HR, Lees RK, (1990) Programmed death of autoreactive thymocytes. Nature 343: 642-644 doi:10.1038/343642a0.
44. Canté-Barrett K, Gallo EM, Winslow MM, Crabtree GR, (2006) Thymocyte negative selection is mediated by protein kinase C- and Ca2+-dependent transcriptional induction of bim [corrected]. J Immunol 176: 2299-2306.
45. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR, (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2: 156-162 doi:10.1038/35004029.
46. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK, (2009) Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459: 428-432 doi:10.1038/nature08012.
47. Staton TL, Lazarevic V, Jones DC, Lanser AJ, Takagi T, et al. (2012) Dampening of death pathways by schnurri-2 is essential for T-cell development. Nature 472: 105-109 doi:10.1038/nature09848.
48. Mamalaki C, Norton T, Tanaka Y, Townsend AR, Chandler P, et al. (1992) Thymic depletion and peripheral activation of class I major histocompatibility complex-restricted T cells by soluble peptide in T-cell receptor transgenic mice. Proc Natl Acad Sci U S A 89: 11342-11346.
49. Dzhagalov IL, Melichar HJ, Ross JO, Herzmark P, Robey EA, (2012) Two-photon imaging of the immune system. Curr Protoc Cytom Chapter 12: Unit12.26 doi:10.1002/0471142956.cy1226s60.