Maturation and emigration of single-positive thymocytes

Clinical and Developmental Immunology

Volumn 2013, Issue , 2013, Pages

  Xu, Xi ^a   Zhang, Shusong ^a   Li, Pingping ^a   Lu, Jin ^b   Xuan, Qun ^c   Ge, Qing ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

^c KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; AUTOIMMUNE REGULATOR PROTEIN; CD24 ANTIGEN; CD40 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; CONCANAVALIN A; EARLY GROWTH RESPONSE FACTOR 1; INTERLEUKIN 2; KALININ; KRUPPEL LIKE FACTOR 2; L SELECTIN; LYMPHOTOXIN BETA RECEPTOR; MESSENGER RNA; MICRORNA; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN KINASE LCK; REACTIVE OXYGEN METABOLITE; RNA POLYMERASE II; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP2; TRANSCRIPTION FACTOR SP3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; VERY LATE ACTIVATION ANTIGEN 5; LEUKOCYTE ANTIGEN;

ADOPTIVE TRANSFER; APOPTOSIS; AUTOIMMUNITY; AUTOPHAGY; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CELL SURVIVAL; CELLULAR DISTRIBUTION; COMPLEMENTARITY DETERMINING REGION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DOWN REGULATION; EPITHELIUM CELL; GLYCOSYLATION; IMMUNOLOGICAL TOLERANCE; MACROAUTOPHAGY; MITOCHONDRION; NONHUMAN; ONTOGENY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; THYMOCYTE; UPREGULATION; ANIMAL; ANTIGEN MEDIATED CLONAL SELECTION; CELL MOTION; CYTOLOGY; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD; CELL DIFFERENTIATION; CELL MOVEMENT; CLONAL SELECTION, ANTIGEN-MEDIATED; HUMANS; OXIDATION-REDUCTION; PHENOTYPE; T-LYMPHOCYTE SUBSETS; THYMOCYTES;

EID: 84886450185     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2013/282870     Document Type: Review

References (148)

1. Nitta T., Murata S., Ueno T., Tanaka K., Takahama Y., Thymic microenvironments for T-cell repertoire formation. Advances in Immunology 2008 99 59 94 2-s2.0-57949090638 10.1016/S0065-2776(08)00603-2
2. Rothenberg E. V., Taghon T., Molecular genetics of T cell development. Annual Review of Immunology 2005 23 601 649 2-s2.0-17444396980 10.1146/annurev.immunol.23.021704.115737 (Pubitemid 40563181)
3. Takahama Y., Journey through the thymus: stromal guides for T-cell development and selection. Nature Reviews Immunology 2006 6 2 127 135 2-s2.0-33644845679 10.1038/nri1781 (Pubitemid 43361588)
4. de Pooter R., Zúñiga-Pflücker J. C., T-cell potential and development in vitro: the OP9-DL1 approach. Current Opinion in Immunology 2007 19 2 163 168 2-s2.0-33847656103 10.1016/j.coi.2007.02.011 (Pubitemid 46356972)
5. Berzins S. P., Godfrey D. I., Miller J. F. A. P., Boyd R. L., A central role for thymic emigrants in peripheral T cell homeostasis. Proceedings of the National Academy of Sciences of the United States of America 1999 96 17 9787 9791 2-s2.0-0033578325 10.1073/pnas.96.17.9787 (Pubitemid 29398810)
6. Zachariah M. A., Cyster J. G., Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 2010 328 5982 1129 1135 2-s2.0-77952961847 10.1126/science.1188222
7. Kurobe H., Liu C., Ueno T., Saito F., Ohigashi I., Seach N., Arakaki R., Hayashi Y., Kitagawa T., Lipp M., Boyd R. L., Takahama Y., CCR7-dependent cortex-to-medulla migration of positively selected thymocytes is essential for establishing central tolerance. Immunity 2006 24 2 165 177 2-s2.0-32244432265 10.1016/j.immuni.2005.12.011 (Pubitemid 43214586)
8. McCaughtry T. M., Wilken M. S., Hogquist K. A., Thymic emigration revisited. Journal of Experimental Medicine 2007 204 11 2513 2520 2-s2.0-35748979722 10.1084/jem.20070601 (Pubitemid 350044776)
9. - medullary thymocytes during mouse ontogeny and its defect in Aire-/- mice. Proceedings of the National Academy of Sciences of the United States of America 2007 104 46 18175 18180 2-s2.0-36749066715 10.1073/pnas.0708884104 (Pubitemid 350210840)
10. - thymocyte development. Journal of Immunology 2008 180 4 2256 2263 2-s2.0-42149090516
11. + regulatory T cells induced by an agonist self-peptide. Nature Immunology 2001 2 4 301 306 2-s2.0-0035320679 10.1038/86302 (Pubitemid 33706340)
12. Marks B. R., Nowyhed H. N., Choi J.-Y., Poholek A. C., Odegard J. M., Flavell R. A., Craft J., Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nature Immunology 2010 10 1125 1132
13. Zuniga L. A., Jain R., Haines C., Cua D.J., Th17 cell development: from the cradle to the grave. Immunological Reviews 2013 252 78 88
14. Yuan X., Malek T. R., Cellular and molecular determinants for the development of natural and induced regulatory T cells. Human Immunology 2012 73 773 782
15. Lucas B., Vasseur F., Penit C., Production, selection, and maturation of thymocytes with high surface density of TCR. Journal of Immunology 1994 153 1 53 62 2-s2.0-0028229558 (Pubitemid 24186518)
16. - thymocytes are functionally immature. Journal of Immunology 1991 147 6 1779 1785 2-s2.0-0026044445
17. Kirberg J., Brocker T., CD45 up-regulation during lymphocyte maturation. International Immunology 1996 8 11 1743 1749 2-s2.0-0029801586 10.1093/intimm/8.11.1743 (Pubitemid 26382145)
18. - thymocytes lacking the heat-stable antigen. Cellular Immunology 1988 117 2 312 326 2-s2.0-0024211845 (Pubitemid 19017874)
19. + T cell subsets: a subset (Thy0) that secretes diverse cytokines and overexpresses the V β 8 T cell receptor gene family. Journal of Experimental Medicine 1992 176 1 269 274 2-s2.0-0026642684 10.1084/jem.176.1.269
20. Yamashita I., Nagata T., Tada T., Nakayama T., CD69 cell surface expression identifies developing thymocytes which audition for T cell antigen receptor-mediated positive selection. International Immunology 1993 5 9 1139 1150 2-s2.0-0027427713 (Pubitemid 23291163)
21. Vernachio J., Li M., Donnenberg A. D., Soloski M. J., Qa-2 expression in the adult murine thymus. A unique marker for a mature thymic subset. Journal of Immunology 1989 142 1 48 56 2-s2.0-0024528059 (Pubitemid 19034721)
22. Gabor M. J., Godfrey D. I., Scollay R., Recent thymic emigrants are distinct from most medullary thymocytes. European Journal of Immunology 1997 27 8 2010 2015 2-s2.0-0030844377 10.1002/eji.1830270827 (Pubitemid 27346018)
23. - thymocytes and its implication in the late stage of thymocyte development. Immunology 1999 97 4 665 671 2-s2.0-0032790221 10.1046/j.1365-2567.1999.00816.x (Pubitemid 29356417)
24. + thymocytes in normal mouse thymus. International Immunology 2001 13 3 313 320 2-s2.0-0035114467 (Pubitemid 32179079)
25. + thymocyte development. Journal of Experimental Medicine 2013
26. + T cells in two major waves of thymic deletion distinguished by induction of PD-1 or NF-kappaB. Journal of Experimental Medicine 2013 210 269 285
27. - thymocytes. PLoS ONE 2011 6 10 2-s2.0-80054081610 10.1371/journal.pone.0025567 e25567
28. McNeill L., Salmond R. J., Cooper J. C., Carret C. K., Cassady-Cain R. L., Roche-Molina M., Tandon P., Holmes N., Alexander D. R., The differential regulation of Lck kinase phosphorylation sites by CD45 is critical for T cell receptor signaling responses. Immunity 2007 27 3 425 437 2-s2.0-34548679868 10.1016/j.immuni.2007.07.015 (Pubitemid 47418669)
29. Stephen T. L., Wilson B. S., Laufer T. M., Subcellular distribution of Lck during CD4 T-cell maturation in the thymic medulla regulates the T-cell activation threshold. Proceedings of the National Academy of Sciences of the United States of America 2012 109 7415 7420
30. Azzam H. S., Grinberg A., Lui K., Shen H., Shores E. W., Love P. E., CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. Journal of Experimental Medicine 1998 188 12 2301 2311 2-s2.0-0032445491 10.1084/jem.188.12.2301 (Pubitemid 29028502)
31. Starr T. K., Daniels M. A., Lucido M. M., Jameson S. C., Hogquist K. A., Thymocyte sensitivity and supramolecular activation cluster formation are developmentally regulated: a partial role for sialylation. Journal of Immunology 2003 171 9 4512 4520 2-s2.0-0142149044 (Pubitemid 37310566)
32. Li Q.-J., Chau J., Ebert P. J. R., Sylvester G., Min H., Liu G., Braich R., Manoharan M., Soutschek J., Skare P., Klein L. O., Davis M. M., Chen C.-Z., miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 2007 129 1 147 161 2-s2.0-33947721625 10.1016/j.cell.2007.03.008 (Pubitemid 46507589)
33. Wurbel M. A., Philippe J. M., Nguyen C., The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. European Journal of Immunology 2000 30 262 271 (Pubitemid 30011788)
34. Choi Y. I., Duke-Cohan J. S., Ahmed W. B., Handley M. A., Mann F., Epstein J. A., Clayton L. K., Reinherz E. L., PlexinD1 glycoprotein controls migration of positively selected thymocytes into the medulla. Immunity 2008 29 6 888 898 2-s2.0-57449117667 10.1016/j.immuni.2008.10.008
35. Ueno T., Saito F., Gray D. H. D., Kuse S., Hieshima K., Nakano H., Kakiuchi T., Lipp M., Boyd R. L., Takahama Y., CCR7 signals are essential for cortex-medulla migration of developing thymocytes. Journal of Experimental Medicine 2004 200 4 493 505 2-s2.0-4344668118 10.1084/jem.20040643 (Pubitemid 39121906)
36. Mick V. E., Starr T. K., McCaughtry T. M., McNeil L. K., Hogquist K. A., The regulated expression of a diverse set of genes during thymocyte positive selection in vivo. Journal of Immunology 2004 173 9 5434 5444 2-s2.0-6344274985 (Pubitemid 39392127)
37. Nitta T., Nitta S., Yu L., Lipp M., Takahama Y., CCR7-mediated migration of developing thymocytes to the medulla is essential for negative selection to tissue-restricted antigens. Proceedings of the National Academy of Sciences of the United States of America 2009 106 40 17129 17133 2-s2.0-70350131707 10.1073/pnas.0906956106
38. Weinreich M. A., Hogquist K. A., Thymic emigration: when and how T cells leave home. Journal of Immunology 2008 181 4 2265 2270 2-s2.0-53149130236
39. Bai A., Hu H., Yeung M., Chen J., Krüppel-like factor 2 controls T cell trafficking by activating L-selectin (CD62L) and sphingosine-1-phosphate receptor 1 transcription. Journal of Immunology 2007 178 12 7632 7639 2-s2.0-34250189127 (Pubitemid 46898033)
40. Carlson C. M., Endrizzi B. T., Wu J., Ding X., Weinreich M. A., Walsh E. R., Wani M. A., Lingrel J. B., Hogquist K. A., Jameson S. C., Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 2006 442 7100 299 302 2-s2.0-33746334804 10.1038/nature04882 (Pubitemid 44114904)
41. Gubbels Bupp M. R., Edwards B., Guo C., Wei D., Chen G., Wong B., Masteller E., Peng S. L., T cells require Foxo1 to populate the peripheral lymphoid organs. European Journal of Immunology 2009 39 11 2991 2999 2-s2.0-70449353483 10.1002/eji.200939427
42. Ehrlich L. I. R., Oh D. Y., Weissman I. L., Lewis R. S., Differential contribution of chemotaxis and substrate restriction to segregation of immature and mature thymocytes. Immunity 2009 31 6 986 998 2-s2.0-71749104649 10.1016/j.immuni.2009.09.020
43. Le Borgne M., Ladi E., Dzhagalov I., Herzmark P., Liao Y. F., Chakraborty A. K., Robey E. A., The impact of negative selection on thymocyte migration in the medulla. Nature Immunology 2009 10 8 823 830 2-s2.0-67651158788 10.1038/ni.1761
44. Rooke R., Waltzinger C., Benoist C., Mathis D., Targeted complementation of MHC class II deficiency by intrathymic delivery of recombinant adenoviruses. Immunity 1997 7 1 123 134 2-s2.0-0030849637 10.1016/S1074-7613(00)80515-4 (Pubitemid 27357270)
45. Laufer T. M., DeKoning J., Markowitz J. S., Lo D., Glimcher L. H., Unopposed positive selection and autoreactivity in mice expressing class II MHC only on thymic cortex. Nature 1996 383 6595 81 85 2-s2.0-0029835390 10.1038/383081a0 (Pubitemid 26296465)
46. Laufer T. M., Fan L., Glimcher L. H., Self-reactive T cells selected on thymic cortical epithelium are polyclonal and are pathogenic in vivo. Journal of Immunology 1999 162 9 5078 5084 2-s2.0-0033136289 (Pubitemid 29307107)
47. Weih F., Carrasco D., Durham S. K., Barton D. S., Rizzo C. A., Ryseck R.-P., Lira S. A., Bravo R., Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF- B/Rel family. Cell 1995 80 2 331 340 2-s2.0-0028817585
48. Burkly L., Hession C., Ogata L., Reilly C., Marconi L. A., Olson D., Tizard R., Cate R., Lo D., Expression of relB is required for the development of thymic medulla and dendritic cells. Nature 1995 373 6514 531 536 2-s2.0-0028952482
49. Heino M., Peterson P., Sillanpaa N., RNA and protein expression of the murine autoimmune regulator gene (Aire) in normal, RelB-deficient and in NOD mouse. European Journal of Immunology 2000 30 1884 1893 (Pubitemid 30456184)
50. Zhu M., Chin R. K., Christiansen P. A., Lo J. C., Liu X., Ware C., Siebenlist U., Fu Y.-X., NF- B2 is required for the establishment of central tolerance through an Aire-dependent pathway. Journal of Clinical Investigation 2006 116 11 2964 2971 2-s2.0-33750585066 10.1172/JCI28326 (Pubitemid 44684481)
51. Kajiura F., Sun S., Nomura T., Izumi K., Ueno T., Bando Y., Kuroda N., Han H., Li Y., Matsushima A., Takahama Y., Sakaguchi S., Mitani T., Matsumoto M., NF-kappaB2 is required for the establishment of central tolerance through an Aire-dependent pathway. Journal of Immunology 2004 172 4 2067 2075 2-s2.0-10744226628
52. Boehm T., Scheu S., Pfeffer K., Bleul C. C., Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LT β R. Journal of Experimental Medicine 2003 198 5 757 769 2-s2.0-0041884736 10.1084/jem.20030794 (Pubitemid 37087775)
53. Akiyama T., Maeda S., Yamane S., Ogino K., Kasai M., Kajiura F., Matsumoto M., Inoue J.-I., Dependence of self-tolerance on TRAF6-directed development of thymic stroma. Science 2005 308 5719 248 251 2-s2.0-16444377660 10.1126/science.1105677 (Pubitemid 40558859)
54. Derbinski J., Kyewski B., Linking signalling pathways, thymic stroma integrity and autoimmunity. Trends in Immunology 2005 26 10 503 506 2-s2.0-24744448656 10.1016/j.it.2005.07.006 (Pubitemid 41297677)
55. Tykocinski L.-O., Sinemus A., Kyewski B., The thymus medulla slowly yields its secrets. Annals of the New York Academy of Sciences 2008 1143 105 122 2-s2.0-56549085984 10.1196/annals.1443.018
56. Chin R. K., Lo J. C., Kim O., Blink S. E., Christiansen P. A., Peterson P., Wang Y., Ware C., Fu Y.-X., Lymphotoxin pathway directs thymic Aire expression. Nature Immunology 2003 4 11 1121 1127 2-s2.0-0242624626 10.1038/ni982 (Pubitemid 37428040)
57. Anderson M. S., Venanzi E. S., Klein L., Chen Z., Berzins S. P., Turley S. J., Von Boehmer H., Bronson R., Dierich A., Benoist C., Mathis D., Projection of an immunological self shadow within the thymus by the aire protein. Science 2002 298 5597 1395 1401 2-s2.0-0037112047 10.1126/science.1075958 (Pubitemid 35346134)
58. Liston A., Lesage S., Wilson J., Peltonen L., Goodnow C. C., Aire regulates negative selection of organ-specific T cells. Nature Immunology 2003 4 4 350 354 2-s2.0-0037383758 10.1038/ni906 (Pubitemid 36432317)
59. Derbinski J., Schulte A., Kyewski B., Klein L., Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nature Immunology 2001 2 11 1032 1039 2-s2.0-0035171545 10.1038/ni723 (Pubitemid 33069498)
60. Aaltonen J., Björses P., Perheentupa J., Horelli-Kuitunen N., Palotie A., Peltonen L., Lee Su Y., Francis F., Hennig S., Thiel C., Lehrach H., Yaspo M.-L., An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nature Genetics 1997 17 4 399 403 2-s2.0-0346599403 (Pubitemid 27518387)
61. Nagamine K., Peterson P., Scott H. S., Kudoh J., Minoshima S., Heino M., Krohn K. J. E., Lalioti M. D., Mullis P. E., Antonarakis S. E., Kawasaki K., Asakawa S., Ito F., Shimizu N., Positional cloning of the APECED gene. Nature Genetics 1997 17 4 393 398 2-s2.0-16944367194 (Pubitemid 27518386)
62. Peterson P., Peltonen L., Autoimmune polyendocrinopathy syndrome type 1 (APS1) and AIRE gene: new views on molecular basis of autoimmunity. Journal of Autoimmunity 2005 25 49 55 2-s2.0-28444438159 10.1016/j.jaut.2005.09.022 (Pubitemid 41728045)
63. Waterfield M., Anderson M. S., Clues to immune tolerance: the monogenic autoimmune syndromes. Annals of the New York Academy of Sciences 2010 1214 1 138 155 2-s2.0-78650357758 10.1111/j.1749-6632.2010.05818.x
64. Ramsey C., Winqvist O., Puhakka L., Halonen M., Moro A., Kämpe O., Eskelin P., Pelto-Huikko M., Peltonen L., Aire deficient mice develop multiple features of APECED phenotype and show altered immune response. Human Molecular Genetics 2002 11 4 397 409 2-s2.0-0037084784 (Pubitemid 34213613)
65. Zumer K., Saksela K., Peterlin BM The mechanism of tissue-restricted antigen gene expression by AIRE. Journal of Immunology 2013 190 2479 2482
66. Metzger T. C., Anderson M. S., Control of central and peripheral tolerance by Aire. Immunological Reviews 2011 241 1 89 103 2-s2.0-79954463242 10.1111/j.1600-065X.2011.01008.x
67. Kroger C. J., Flores R. R., Morillon M., Wang B., Tisch R., Dysregulation of thymic clonal deletion and the escape of autoreactive T cells. Archivum Immunologiae et Therapiae Experimentalis 2010 58 6 449 457 2-s2.0-78649331463 10.1007/s00005-010-0100-3
68. Lei Y., Ripen A. M., Ishimaru N., Ohigashi I., Nagasawa T., Jeker L. T., Bösl M. R., Holländer G. A., Hayashi Y., De Waal Malefyt R., Nitta T., Takahama Y., Aire-dependent production of XCL1 mediates medullary accumulation of thymic dendritic cells and contributes to regulatory T cell development. Journal of Experimental Medicine 2011 208 2 383 394 2-s2.0-79951715831 10.1084/jem.20102327
69. + thymocytes. Journal of Immunology 2009 183 12 7682 7691 2-s2.0-76249101988 10.4049/jimmunol.0804133
70. Danzl N. M., Donlin L. T., Alexandropoulos K., Regulation of medullary thymic epithelial cell differentiation and function by the signaling protein Sin. Journal of Experimental Medicine 2010 207 5 999 1013 2-s2.0-77952296464 10.1084/jem.20092384
71. Brazil M. I., Weiß S., Stockinger B., Excessive degradation of intracellular protein in macrophages prevents presentation in the context of major histocompatibility complex class II molecules. European Journal of Immunology 1997 27 6 1506 1514 2-s2.0-1842407189 10.1002/eji.1830270629 (Pubitemid 27254844)
72. Nimmerjahn F., Milosevic S., Behrends U., Jaffee E. M., Pardoll D. M., Bornkamm G. W., Mautner J., Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. European Journal of Immunology 2003 33 5 1250 1259 2-s2.0-0037960005 10.1002/eji.200323730 (Pubitemid 36609143)
73. Dörfel D., Appel S., Grünebach F., Weck M. M., Müller M. R., Heine A., Brossart P., Processing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro-transcribed MUC1 RNA. Blood 2005 105 8 3199 3205 2-s2.0-17044381835 10.1182/blood-2004-09-3556
74. Paludan C., Schmid D., Landthaler M., Vockerodt M., Kube D., Tuschl T., Münz C., Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005 307 5709 593 596 2-s2.0-12844275079 10.1126/science.1104904 (Pubitemid 40165684)
75. Riedel A., Nimmerjahn F., Burdach S., Behrends U., Bornkamm G. W., Mautner J., Endogenous presentation of a nuclear antigen on MHC class II by autophagy in the absence of CRM1-mediated nuclear export. European Journal of Immunology 2008 38 8 2090 2095 2-s2.0-51149098813 10.1002/eji.200737900
76. Nedjic J., Aichinger M., Emmerich J., Mizushima N., Klein L., Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 2008 455 7211 396 400 2-s2.0-52149099867 10.1038/nature07208
77. Aichinger M., Wu C., Nedjic J., Klein L., Macroautophagy substrates are loaded onto MHC class II of medullary thymic epithelial cells for central tolerance. Journal of Experimental Medicine 2013 210 287 300
78. Klein L., Hinterberger M., Wirnsberger G., Kyewski B., Antigen presentation in the thymus for positive selection and central tolerance induction. Nature Reviews Immunology 2009 9 12 833 844 2-s2.0-72949104779 10.1038/nri2669
79. Koble C., Kyewski B., The thymic medulla: a unique microenvironment for intercellular self-antigen transfer. Journal of Experimental Medicine 2009 206 7 1505 1513 2-s2.0-67650507153 10.1084/jem.20082449
80. Millet V., Naquet P., Guinamard R. R., Intercellular MHC transfer between thymic epithelial and dendritic cells. European Journal of Immunology 2008 38 5 1257 1263 2-s2.0-47049085776 10.1002/eji.200737982
81. Ohnmacht C., Pullner A., King S. B. S., Drexler I., Meier S., Brocker T., Voehringer D., Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. Journal of Experimental Medicine 2009 206 3 549 559 2-s2.0-63449108301 10.1084/jem.20082394
82. Wu L., Shortman K., Heterogeneity of thymic dendritic cells. Seminars in Immunology 2005 17 4 304 312 2-s2.0-22144444873 10.1016/j.smim.2005.05.001 (Pubitemid 40981935)
83. Proietto A. I., Van Dommelen S., Wu L., The impact of circulating dendritic cells on the development and differentiation of thymocytes. Immunology and Cell Biology 2009 87 1 39 45 2-s2.0-58149388025 10.1038/icb.2008.86
84. Donskoy E., Goldschneider I., Two developmentally distinct populations of dendritic cells inhabit the adult mouse thymus: demonstration by differential importation of hematogenous precursors under steady state conditions. Journal of Immunology 2003 170 7 3514 3521 2-s2.0-0037378671 (Pubitemid 36359217)
85. Li J., Park J., Foss D., Goldschneider I., Thymus-homing peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. Journal of Experimental Medicine 2009 206 3 607 622 2-s2.0-63449133991 10.1084/jem.20082232
86. Hadeiba H., Lahl K., Edalati A., Oderup C., Habtezion A., Pachynski R., Nguyen L., Ghodsi A., Adler S., Butcher E. C., Plasmacytoid dendritic cells transport peripheral antigens to the thymus to promote central tolerance. Immunity 2012 36 3 438 450 2-s2.0-84858786391 10.1016/j.immuni.2012.01.017
87. Baba T., Nakamoto Y., Mukaida N., Crucial contribution of thymic Sirp α + conventional dendritic cells to central tolerance against blood-borne antigens in a CCR2-dependent manner. Journal of Immunology 2009 183 5 3053 3063 2-s2.0-70349230989 10.4049/jimmunol.0900438
88. Sitkovsky M., Lukashev D., Regulation of immune cells by local-tissue oxygen tension: HIF1 α and adenosine receptors. Nature Reviews Immunology 2005 5 9 712 721 2-s2.0-25444454359 10.1038/nri1685 (Pubitemid 43086172)
89. Braun R. D., Lanzen J. L., Snyder S. A., Dewhirst M. W., Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. American Journal of Physiology: Heart and Circulatory Physiology 2001 280 6 H2533 H2544 2-s2.0-0034979156
90. Pua H. H., Guo J., Komatsu M., He Y.-W., Autophagy is essential for mitochondrial clearance in mature T lymphocytes. Journal of Immunology 2009 182 7 4046 4055 2-s2.0-64249123646 10.4049/jimmunol.0801143
91. Sandstrom P. A., Buttke T. M., Autocrine production of extracellular catalase prevents apoptosis of the human CEM T-cell line in serum-free medium. Proceedings of the National Academy of Sciences of the United States of America 1993 90 10 4708 4712 2-s2.0-0027155884 (Pubitemid 23148975)
92. Hildeman D. A., Mitchell T., Teague T. K., Henson P., Day B. J., Kappler J., Marrack P. C., Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 1999 10 6 735 744 2-s2.0-0033151622 10.1016/S1074-7613(00) 80072-2 (Pubitemid 29302926)
93. Rathmell J. C., Thompson C. B., The central effectors of cell death in the immune system. Annual Review of Immunology 1999 17 781 828 2-s2.0-0033009890 10.1146/annurev.immunol.17.1.781 (Pubitemid 29241140)
94. Hultqvist M., Bäcklund J., Bauer K., Gelderman K. A., Holmdahl R., Lack of reactive oxygen species breaks T cell tolerance to collagen type II and allows development of arthritis in mice. Journal of Immunology 2007 179 3 1431 1437 2-s2.0-34548657163
95. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z., Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO Journal 2007 26 7 1749 1760 2-s2.0-34247186472 10.1038/sj.emboj.7601623 (Pubitemid 46624042)
96. Hale J. S., Boursalian T. E., Turk G. L., Fink P. J., Thymic output in aged mice. Proceedings of the National Academy of Sciences of the United States of America 2006 103 22 8447 8452 2-s2.0-33744826033 10.1073/pnas.0601040103 (Pubitemid 43838475)
97. Fink P. J., Hendricks D. W., Post-thymic maturation: young T cells assert their individuality. Nature Reviews Immunology 2011 11 8 544 549 2-s2.0-79960843999 10.1038/nri3028
98. Jin R., Zhang J., Chen W., Thymic output: influence factors and molecular mechanism. Cellular & Molecular Immunology 2006 3 5 341 350 2-s2.0-39049191367
99. Yager E. J., Ahmed M., Lanzer K., Randall T. D., Woodland D. L., Blackman M. A., Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. Journal of Experimental Medicine 2008 205 3 711 723 2-s2.0-41149170727 10.1084/jem.20071140 (Pubitemid 351439315)
100. Mackall C. L., Hakim F. T., Gress R. E., Restoration of T-cell homeostasis after T-cell depletion. Seminars in Immunology 1997 9 6 339 346 2-s2.0-18744435046 10.1006/smim.1997.0091 (Pubitemid 28021491)
101. Ge Q., Hu I., Eisen H. N., Chen J., Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proceedings of the National Academy of Sciences of the United States of America 2002 99 5 2989 2994 2-s2.0-0037022573 10.1073/pnas.052714099 (Pubitemid 34240573)
102. + pre-thymic emigrants in the thymus. PLoS ONE 2013 8 e56378
103. Venkataraman K., Lee Y.-M., Michaud J., Thangada S., Ai Y., Bonkovsky H. L., Parikh N. S., Habrukowich C., Hla T., Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circulation Research 2008 102 6 669 676 2-s2.0-41449112571 10.1161/CIRCRESAHA.107.165845 (Pubitemid 351457860)
104. Allende M. L., Dreier J. L., Mandala S., Proia R. L., Expression of the sphingosine 1-phosphate receptor, S1P1, on T-cells controls thymic emigration. Journal of Biological Chemistry 2004 279 15 15396 15401 2-s2.0-2442561611 10.1074/jbc.M314291200 (Pubitemid 38618938)
105. Matloubian M., Lo C. G., Cinamon G., Lesneski M. J., Xu Y., Brinkmann V., Allende M. L., Proia R. L., Cyster J. G., Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004 427 6972 355 360 2-s2.0-1642580757 10.1038/nature02284 (Pubitemid 38133663)
106. Schwab S. R., Pereira J. P., Matloubian M., Xu Y., Huang Y., Cyster J. G., Immunology: lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 2005 309 5741 1735 1739 2-s2.0-24644469502 10.1126/science.1113640 (Pubitemid 41285945)
107. Bréart B., Ramos-Perez W. D., Mendoza A., Salous A. K., Gobert M., Huang Y., Adams R. H., Lafaille J. J., Escalante-Alcalde D., Morris A. J., Schwab S. R., Lipid phosphate phosphatase 3 enables efficient thymic egress. Journal of Experimental Medicine 2011 208 6 1267 1278 2-s2.0-79958257954 10.1084/jem.20102551
108. Rosen H., Alfonso C., Surh C. D., McHeyzer-Williams M. G., Rapid induction of medullary thymocyte phenotypic maturation and egress inhibition by nanomolar sphingosine 1-phosphate receptor agonist. Proceedings of the National Academy of Sciences of the United States of America 2003 100 19 10907 10912 2-s2.0-0141814654 10.1073/pnas.1832725100 (Pubitemid 37140126)
109. Alfonso C., McHeyzer-Williams M. G., Rosen H., CD69 down-modulation and inhibition of thymic egress by short- and long-term selective chemical agonism of sphingosine 1-phosphate receptors. European Journal of Immunology 2006 36 1 149 159 2-s2.0-30944438292 10.1002/eji.200535127 (Pubitemid 43116401)
110. Yagi H., Kamba R., Chiba K., Soga H., Yaguchi K., Nakamura M., Itoh T., Immunosuppressant FTY720 inhibits thymocyte emigration. European Journal of Immunology 2000 30 5 1435 1444 2-s2.0-0034105487 (Pubitemid 30311974)
111. Sinclair L. V., Finlay D., Feijoo C., Cornish G. H., Gray A., Ager A., Okkenhaug K., Hagenbeek T. J., Spits H., Cantrell D. A., Phosphatidylinositol-3- OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nature Immunology 2008 9 6 513 521 (Pubitemid 351560520)
112. Barbee S. D., Alberola-Ila J., Phosphatidylinositol 3-kinase regulates thymic exit. Journal of Immunology 2005 174 3 1230 1238 2-s2.0-12444283647
113. Schnell F. J., Kersh G. J., Control of recent thymic emigrant survival by positive selection signals and early growth response gene 1. Journal of Immunology 2005 175 4 2270 2277 2-s2.0-23444444199 (Pubitemid 41113834)
114. Temchura V. V., Frericks M., Nacken W., Esser C., Role of the aryl hydrocarbon receptor in thymocyte emigration in vivo. European Journal of Immunology 2005 35 9 2738 2747 2-s2.0-26044458205 10.1002/eji.200425641 (Pubitemid 41404057)
115. Vivinus-Nebot M., Rousselle P., Breittmayer J.-P., Cenciarini C., Berrih-Aknin S., Spong S., Nokelainen P., Cottrez F., Marinkovich M. P., Bernard A., Mature human thymocytes migrate on laminin-5 with activation of metalloproteinase-14 and cleavage of CD44. Journal of Immunology 2004 172 3 1397 1406 2-s2.0-9144231190 (Pubitemid 38116781)
116. Cotta-de-Almeida V., Serra Villa-Verde D. M., Lepault F., Pléau J.-M., Dardenne M., Savino W., Impaired migration of NOD mouse thymocytes: a fibronectin receptor-related defect. European Journal of Immunology 2004 34 6 1578 1587 2-s2.0-3242722496 10.1002/eji.200324765 (Pubitemid 39256039)
117. Ushiki T., Takeda M., Three-dimensional ultrastructure of the perivascular space in the rat thymus. Archives of Histology and Cytology 1997 60 1 89 99 2-s2.0-0030908237 (Pubitemid 27251361)
118. Henry L., Durrant T. E., Anderson G., Pericapillary collagen in the human thymus: implications for the concept of the "blood-thymus" barrier. Journal of Anatomy 1992 181 1 39 46 2-s2.0-0026453308
119. Kato S., Schoefl G. I., Microvasculature of normal and involuted mouse thymus. Light- and electron-microscopic study. Acta Anatomica 1989 135 1 1 11 2-s2.0-0024307952 (Pubitemid 19146477)
120. Savino W., Carnaud C., Luan J.-J., Bach J.-F., Dardenne M., Characterization of the extracellular matrix-containing giant perivascular spaces in the NOD mouse thymus. Diabetes 1993 42 1 134 140 2-s2.0-0027470447 (Pubitemid 23013805)
121. Stutman O., Intrathymic and extrathymic T cell maturation. Immunological Reviews 1978 42 138 184 2-s2.0-0018197430 (Pubitemid 9099364)
122. Boursalian T. E., Golob J., Soper D. M., Cooper C. J., Fink P. J., Continued maturation of thymic emigrants in the periphery. Nature Immunology 2004 5 4 418 425 2-s2.0-9144228777 10.1038/ni1049 (Pubitemid 38500091)
123. Lee C.-K., Kim K., Welniak L. A., Murphy W. J., Muegge K., Durum S. K., Thymic emigrants isolated by a new method possess unique phenotypic and functional properties. Blood 2001 97 5 1360 1369 2-s2.0-0035282765 10.1182/blood.V97.5.1360 (Pubitemid 32183760)
124. Kelly K. A., Scollay R., Analysis of recent thymic emigrants with subset- and maturity-related markers. International Immunology 1990 2 5 419 425 2-s2.0-0025331311 (Pubitemid 20170082)
125. Tough D. F., Sprent J., Turnover of naive- and memory-phenotype T cells. Journal of Experimental Medicine 1994 179 4 1127 1135 2-s2.0-0028267677 (Pubitemid 24091771)
126. McHeyzer-Williams L. J., McHeyzer-Williams M. G., Developmentally distinct Th cells control plasma cell production in vivo. Immunity 2004 20 2 231 242 2-s2.0-1342287073 10.1016/S1074-7613(04)00028-7 (Pubitemid 38258398)
127. + lymphocytes to the small-intestinal mucosa. Journal of Clinical Investigation 2002 110 8 1113 1121 2-s2.0-0036802422 10.1172/JCI200215988 (Pubitemid 35215892)
128. Johansson-Lindbom B., Svensson M., Wurbel M.-A., Malissen B., Márquez G., Agace W., Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. Journal of Experimental Medicine 2003 198 6 963 969 2-s2.0-0141449950 10.1084/jem.20031244 (Pubitemid 37152933)
129. + recent thymic emigrants home to and efficiently repopulate the small intestine epithelium. Nature Immunology 2006 7 5 482 488 2-s2.0-33646010039 10.1038/ni1319
130. +8- T helper lymphocytes requires post-thymic development. Journal of Immunology 1991 147 3 851 859 2-s2.0-0025871972
131. Hendricks D. W., Fink P. J., Recent thymic emigrants are biased against the T-helper type 1 and toward the T-helper type 2 effector lineage. Blood 2011 117 4 1239 1249 2-s2.0-79251556549 10.1182/blood-2010-07-299263
132. Priyadharshini B., Welsh R. M., Greiner D. L., Gerstein R. M., Brehm M.
133. Makaroff L. E., Hendricks D. W., Niec R. E., Fink P. J., Postthymic maturation influences the CD8 T cell response to antigen. Proceedings of the National Academy of Sciences of the United States of America 2009 106 12 4799 4804 2-s2.0-63849270941 10.1073/pnas.0812354106
134. Joshi N. S., Kaech S. M., Effector CD8 T cell development: a balancing act between memory cell potential and terminal differentiation. Journal of Immunology 2008 180 3 1309 1315 2-s2.0-40749111025
135. Houston E. G. Jr., Fink P. J., MHC drives TCR repertoire shaping, but not maturation, in recent thymic emigrants. Journal of Immunology 2009 183 11 7244 7249 2-s2.0-73349114920 10.4049/jimmunol.0902313
136. Nishio J., Suzuki M., Nanki T., Miyasaka N., Kohsaka H., Development of TCRB CDR3 length repertoire of human T lymphocytes. International Immunology 2004 16 3 423 431 2-s2.0-1542269697 10.1093/intimm/dxh046 (Pubitemid 38313151)
137. Matsutani T., Ohmori T., Ogata M., Soga H., Kasahara S., Yoshioka T., Suzuki R., Itoh T., Comparison of CDR3 length among thymocyte subpopulations: impacts of MHC and BV segment on the CDR3 shortening. Molecular Immunology 2007 44 9 2378 2387 2-s2.0-33846186870 10.1016/j.molimm.2006.10.026 (Pubitemid 46097106)
138. Kyewski B., Klein L., A central role for central tolerance. Annual Review of Immunology 2006 24 571 606 2-s2.0-33646165128 10.1146/annurev.immunol.23. 021704.115601
139. Yin Y., Li Y., Kerzic M. C., Martin R., Mariuzza R. A., Structure of a TCR with high affinity for self-antigen reveals basis for escape from negative selection. EMBO Journal 2011 30 6 1137 1148 2-s2.0-79952750632 10.1038/emboj.2011.21
140. Lukacs-Kornek V., Turley S. J., Self-antigen presentation by dendritic cells and lymphoid stroma and its implications for autoimmunity. Current Opinion in Immunology 2011 23 1 138 145 2-s2.0-79951674014 10.1016/j.coi.2010.11.012
141. Gardner J. M., DeVoss J. J., Friedman R. S., Wong D. J., Tan Y. X., Zhou X., Johannes K. P., Su M. A., Chang H. Y., Krummel M. F., Anderson M. S., Deletional tolerance mediated by extrathymic aire-expressing cells. Science 2008 321 5890 843 847 2-s2.0-49449093723 10.1126/science.1159407
142. Thangavelu G., Parkman J. C., Ewen C. L., Uwiera R. R. E., Baldwin T. A., Anderson C. C., Programmed death-1 is required for systemic self-tolerance in newly generated T cells during the establishment of immune homeostasis. Journal of Autoimmunity 2011 36 3-4 301 312 2-s2.0-79954847245 10.1016/j.jaut.2011.02. 009
143. Houston E. G. Jr., Nechanitzky R., Fink P. J., Cutting edge: contact with secondary lymphoid organs drives postthymic T cell maturation. Journal of Immunology 2008 181 8 5213 5217 2-s2.0-54049122959
144. Houston E. G. J., Boursalian T. E., Fink P. J., Homeostatic signals do not drive post-thymic T cell maturation. Cellular Immunology 2012 274 1-2 39 45 2-s2.0-84859912874 10.1016/j.cellimm.2012.02.005
145. Hsu F.-C., Pajerowski A. G., Nelson-Holte M., Sundsbak R., Shapiro V. S., NKAP is required for T cell maturation and acquisition of functional competency. Journal of Experimental Medicine 2011 208 6 1291 1304 2-s2.0-79958290116 10.1084/jem.20101874
146. Berzins S. P., Boyd R. L., Miller J. F. A. P., The role of the thymus and recent thymic migrants in the maintenance of the adult peripheral lymphocyte pool. Journal of Experimental Medicine 1998 187 11 1839 1848 2-s2.0-0032101049 10.1084/jem.187.11.1839 (Pubitemid 28262447)
147. Elgbratt K., Kurlberg G., Hahn-Zohric M., Hultgren Hörnquist E., Rapid migration of thymic emigrants to the colonic mucosa in ulcerative colitis patients. Clinical and Experimental Immunology 2010 162 2 325 336 2-s2.0-78649309081 10.1111/j.1365-2249.2010.04230.x
148. Armengol M. P., Sabater L., Fernández M., Ruíz M., Alonso N., Otero M. J., Martínez-Cáceres E., Jaraquemada D., Pujol-Borrell R., Influx of recent thymic emigrants into autoimmune thyroid disease glands in humans. Clinical and Experimental Immunology 2008 153 3 338 350 2-s2.0-49649102596 10.1111/j.1365-2249.2008.03706.x