Development of T Lymphocytes

  • Benjamin A. Schwarz
  • Avinash Bhandoola


The goal of this chapter is to introduce readers to the cellular and molecular basis of T-cell differentiation. We have divided T-cell development into three major stages (early T-lineage development, β or γδ selection, positive and negative selection). These correlate with specific subsets of thymocytes (ETP-DN3, DN3-DP, DP-SP thymocytes), specific locations within the thymus (cortex, subcapsular zone, cortex and medulla), T-cell receptor rearrangement events (no functional rearrangements, β or γδ rearrangements, α rearrangements), and lineage fate decisions (T-lineage commitment, αβ vs. γδ, CD4 vs. CD8). Models for each developmental decision and the molecular players are presented.


Negative Selection Recombination Signal Sequence Subcapsular Zone Tcrb Locus Thymus Settling 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adolfsson, J., Borge, O.J., Bryder, D., Theilgaard-Monch, K., Astrand-Grundstrom, I., Sitnicka, E., Sasaki, Y., and Jacobsen, S. E. 2001. Immunity 15: 659–669.PubMedGoogle Scholar
  2. Adolfsson, J., Mansson, R., Buza-Vidas, N., Hultquist, A., Liuba, K., Jensen, C.T., Bryder, D., Yang, L., Borge, O.J., Thoren, L.A., Anderson, K., Sitnicka, E., Sasaki, Y., Sigvardsson, M., and Jacobsen, S. E. 2005. Cell 121:295–306.PubMedGoogle Scholar
  3. Aifantis, I., Mandal, M., Sawai, K., Ferrando, A., and Vilimas, T. 2006. Immunol Rev 209:159–169.PubMedGoogle Scholar
  4. Akashi, K., Kondo, M., von Freeden-Jeffry, U., Murray, R., and Weissman, I.L. 1997. Cell 89:1033–1041.PubMedGoogle Scholar
  5. Akashi, K., Traver, D., Miyamoto, T., and Weissman, I.L. 2000. Nature 404:193–197.PubMedGoogle Scholar
  6. Aliahmad, P. and Kaye, J. 2008. J Exp Med 205:245–256.PubMedGoogle Scholar
  7. Allman, D., Sambandam, A., Kim, S., Miller, J. P., Pagan, A., Well, D., Meraz, A., and Bhandoola, A. 2003. Nat Immunol 4:168–174.PubMedGoogle Scholar
  8. 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., and Mathis, D. 2002. Science 298:1395–1401.PubMedGoogle Scholar
  9. Ardavin, C., Wu, L., Li, C.L., and Shortman, K. 1993. Nature 362:761–763.PubMedGoogle Scholar
  10. Ashton-Rickardt, P.G., Bandeira, A., Delaney, J.R., Van Kaer, L., Pircher, H.P., Zinkernagel, R.M., and Tonegawa, S. 1994. Cell 76:651–663.PubMedGoogle Scholar
  11. Aster, J.C., Pear, W.S., and Blacklow, S.C. 2008. Annu Rev Pathol 3:587–613.PubMedGoogle Scholar
  12. Bell, J.J. and Bhandoola, A. 2008. Nature 452:764–767.PubMedGoogle Scholar
  13. Bendelac, A., Savage, P.B., and Teyton, L. 2007. Annu Rev Immunol 25:297–336.PubMedGoogle Scholar
  14. Benz, C. and Bleul, C.C. 2005. J Exp Med 202:21–31.PubMedGoogle Scholar
  15. Bhandoola, A., von Boehmer, H., Petrie, H.T., and Zuniga-Pflucker, J.C. 2007. Immunity 26:678–689.PubMedGoogle Scholar
  16. Borowski, C., Martin, C., Gounari, F., Haughn, L., Aifantis, I., Grassi, F., and von Boehmer, H. 2002. Curr Opin Immunol 14:200–206.PubMedGoogle Scholar
  17. Borowski, C., Li, X., Aifantis, I., Gounari, F., and von Boehmer, H. 2004. J Exp Med 199:607–615.PubMedGoogle Scholar
  18. Bouillet, P., Purton, J.F., Godfrey, D.I., Zhang, L.C., Coultas, L., Puthalakath, H., Pellegrini, M., Cory, S., Adams, J. M., and Strasser, A. 2002. Nature 415:922–926.PubMedGoogle Scholar
  19. Brugnera, E., Bhandoola, A., Cibotti, R., Yu, Q., Guinter, T.I., Yamashita, Y., Sharrow, S.O., and Singer, A. 2000. Immunity 13:59–71.PubMedGoogle Scholar
  20. Bruno, L., Fehling, H.J., and von Boehmer, H. 1996. Immunity 5:343–352.PubMedGoogle Scholar
  21. 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., and Jameson, S.C. 2006. Nature 442:299–302.PubMedGoogle Scholar
  22. Carlyle, J.R. and Zuniga-Pflucker, J.C. 1998. Immunity 9:187–197.PubMedGoogle Scholar
  23. Ceredig, R. and Rolink, T. 2002. Nat Rev Immunol 2:888–897.PubMedGoogle Scholar
  24. Ceredig, R., Bosco, N., and Rolink, A. G. 2007. Eur J Immunol 37:830–837.PubMedGoogle Scholar
  25. Christensen, J. L. and Weissman, I.L. 2001. Proc Natl Acad Sci USA 98:14541–14546.PubMedGoogle Scholar
  26. Ciofani, M. and Zuniga-Pflucker, J.C. 2005. Nat Immunol 6:881–888.PubMedGoogle Scholar
  27. Ciofani, M. and Zuniga-Pflucker, J.C. 2007. Annu Rev Cell Dev Biol 23:463–493.PubMedGoogle Scholar
  28. Ciofani, M., Knowles, G.C., Wiest, D.L., von Boehmer, H., and Zuniga-Pflucker, J.C. 2006. Immunity 25:105–116.PubMedGoogle Scholar
  29. Cyster, J.G. 2005. Annu Rev Immunol 23:127–159.PubMedGoogle Scholar
  30. Dakic, A., Metcalf, D., Di Rago, L., Mifsud, S., Wu, L., and Nutt, S.L. 2005. J Exp Med 201:1487–1502.PubMedGoogle Scholar
  31. Donskoy, E. and Goldschneider, I. 1992. J Immunol 148:1604–1612.PubMedGoogle Scholar
  32. Doyle, C. and Strominger, J.L. 1987. Nature 330:256–259.PubMedGoogle Scholar
  33. Dudley, E.C., Petrie, H.T., Shah, L.M., Owen, M.J., and Hayday, A.C. 1994. Immunity 1:83–93.PubMedGoogle Scholar
  34. Dunon, D., Courtois, D., Vainio, O., Six, A., Chen, C. H., Cooper, M.D., Dangy, J.P., and Imhof, B.A. 1997. J Exp Med 186:977–988.PubMedGoogle Scholar
  35. Egerton, M., Scollay, R., and Shortman, K. 1990. Proc Natl Acad Sci USA 87:2579–2582.PubMedGoogle Scholar
  36. El Andaloussi, A., Graves, S., Meng, F., Mandal, M., Mashayekhi, M., and Aifantis, I. 2006. Nat Immunol 7:418–426.Google Scholar
  37. Ellmeier, W., Sunshine, M.J., Losos, K., and Littman, D.R. 1998. Immunity 9:485–496.PubMedGoogle Scholar
  38. Engel, I. and Murre, C. 2004. EMBO J 23:202–211.PubMedGoogle Scholar
  39. Fehling, H.J., Krotkova, A., Saint-Ruf, C., and von Boehmer, H. 1995. Nature 375:795–798.PubMedGoogle Scholar
  40. Fontenot, J.D., Gavin, M.A., and Rudensky, A.Y. 2003. Nat Immunol 4:330–336.PubMedGoogle Scholar
  41. Forsberg, E. C., Serwold, T., Kogan, S., Weissman, I.L., and Passegue, E. 2006. Cell 126:415–426.PubMedGoogle Scholar
  42. Fowlkes, B.J., Edison, L., Mathieson, B.J., and Chused, T.M. 1985. J Exp Med 162:802–822.PubMedGoogle Scholar
  43. Foy, T. M., Page, D.M., Waldschmidt, T.J., Schoneveld, A., Laman, J.D., Masters, S. R., Tygrett, L., Ledbetter, J. A., Aruffo, A., Claassen, E., Xu, J.C., Flavell, R.A., Oehen, S., Hedrick, S.M., and Noelle, R. J. 1995. J Exp Med 182:1377–1388.PubMedGoogle Scholar
  44. Franco, C.B., Scripture-Adams, D.D., Proekt, I., Taghon, T., Weiss, A.H., Yui, M.A., Adams, S.L., Diamond, R.A., and Rothenberg, E.V. 2006. Proc Natl Acad Sci USA 103:11993–11998.PubMedGoogle Scholar
  45. Fugmann, S.D., Lee, A.I., Shockett, P.E., Villey, I.J., and Schatz, D.G. 2000. Annu Rev Immunol 18:495–527.PubMedGoogle Scholar
  46. Gao, J.X., Zhang, H., Bai, X.F., Wen, J., Zheng, X., Liu, J., Zheng, P., and Liu, Y. 2002. J Exp Med 195:959–971.PubMedGoogle Scholar
  47. Gartner, F., Alt, F.W., Monroe, R., Chu, M., Sleckman, B.P., Davidson, L., and Swat, W. 1999. Immunity 10:537–546.PubMedGoogle Scholar
  48. Georgopoulos, K. 2002. Nat Rev Immunol 2:162–174.PubMedGoogle Scholar
  49. Godfrey, D.I., Kennedy, J., Suda, T., and Zlotnik, A. 1993. J Immunol 150:4244–4252.PubMedGoogle Scholar
  50. Goldrath, A.W. and Bevan, M.J. 1999. Nature 402:255–262.PubMedGoogle Scholar
  51. Goldschneider, I., Komschlies, K.L., and Greiner, D.L. 1986. J Exp Med 163:1–17.PubMedGoogle Scholar
  52. Goodman, J.W., and Hodgson, G. S. 1962. Blood 19:702–714.PubMedGoogle Scholar
  53. Growney, J.D., Shigematsu, H., Li, Z., Lee, B.H., Adelsperger, J., Rowan, R., Curley, D.P., Kutok, J.L., Akashi, K., Williams, I.R., Speck, N.A., and Gilliland, D.G. 2005. Blood 106:494–504.PubMedGoogle Scholar
  54. Guo, J., Hawwari, A., Li, H., Sun, Z., Mahanta, S.K., Littman, D.R., Krangel, M.S., and He, Y.W. 2002. Nat Immunol 3:469–476.PubMedGoogle Scholar
  55. Hattori, N., Kawamoto, H., Fujimoto, S., Kuno, K., and Katsura, Y. 1996. J Exp Med 184:1137–1147.PubMedGoogle Scholar
  56. Hayday, A.C. and Pennington, D. J. 2007. Nat Immunol 8:137–144.PubMedGoogle Scholar
  57. Hayes, S.M. and Love, P.E. 2006. Immunol Rev 209:170–175.PubMedGoogle Scholar
  58. Hayes, S.M. and Love, P.E. 2007. Immunol Rev 215:8–14.PubMedGoogle Scholar
  59. Hayes, S.M., Li, L., and Love, P.E. 2005. Immunity 22:583–593.PubMedGoogle Scholar
  60. He, X., He, X., Dave, V.P., Zhang, Y., Hua, X., Nicolas, E., Xu, W., Roe, B. A., and Kappes, D.J. 2005. Nature 433:826–833.PubMedGoogle Scholar
  61. He, X., Park, K., Wang, H., He, X., Zhang, Y., Hua, X., Li, Y., and Kappes, D.J. 2008. Immunity 28:346–358.PubMedGoogle Scholar
  62. Heinzel, K., Benz, C., Martins, V.C., Haidl, I.D., and Bleul, C.C. 2007. J Immunol 178:858–868.PubMedGoogle Scholar
  63. Hernandez-Hoyos, G., Anderson, M.K., Wang, C., Rothenberg, E.V., and Alberola-Ila, J. 2003. Immunity 19:83–94.PubMedGoogle Scholar
  64. Hernandez-Munain, C., Sleckman, B.P., and Krangel, M.S. 1999. Immunity 10:723–733.PubMedGoogle Scholar
  65. Ho, I.C. and Pai, S.Y. 2007. Cell Mol Immunol 4:15–29.PubMedGoogle Scholar
  66. Hogquist, K.A., Baldwin, T.A., and Jameson, S.C. 2005. Nat Rev Immunol 5:772–782.PubMedGoogle Scholar
  67. Hori, S., Nomura, T., and Sakaguchi, S. 2003. Science 299:1057–1061.PubMedGoogle Scholar
  68. Huesmann, M., Scott, B., Kisielow, P., and von Boehmer, H. 1991. Cell 66:533–540.PubMedGoogle Scholar
  69. Huseby, E.S., White, J., Crawford, F., Vass, T., Becker, D., Pinilla, C., Marrack, P., and Kappler, J.W. 2005. Cell 122:247–260.PubMedGoogle Scholar
  70. Igarashi, H., Gregory, S., Yokota, T., Sakaguchi, N., and Kincade, P. 2002. Immunity 17: 117–130.PubMedGoogle Scholar
  71. Ikawa, T., Kawamoto, H., Goldrath, A.W., and Murre, C. 2006. J Exp Med 203:1329–1342.PubMedGoogle Scholar
  72. Ikuta, K. and Weissman, I.L. 1992. Proc Natl Acad Sci USA 89:1502–1506.PubMedGoogle Scholar
  73. Ioannidis, V., Beermann, F., Clevers, H., and Held, W. 2001. Nat Immunol 2:691–697.PubMedGoogle Scholar
  74. Iwasaki, H., Somoza, C., Shigematsu, H., Duprez, E.A., Iwasaki-Arai, J., Mizuno, S., Arinobu, Y., Geary, K., Zhang, P., Dayaram, T., Fenyus, M.L., Elf, S., Chan, S., Kastner, P., Huettner, C.S., Murray, R., Tenen, D.G., and Akashi, K. 2005. Blood 106:1590–1600.PubMedGoogle Scholar
  75. Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R., and Havran, W. 2002. Science 296:747–749.PubMedGoogle Scholar
  76. Jenkinson, S.R., Intlekofer, A.M., Sun, G., Feigenbaum, L., Reiner, S.L., and Bosselut, R. 2007. J Exp Med 204:267–272.PubMedGoogle Scholar
  77. Jordan, M.S., Boesteanu, A., Reed, A.J., Petrone, A.L., Holenbeck, A.E., Lerman, M.A., Naji, A., and Caton, A.J. 2001. Nat Immunol 2:301–306.PubMedGoogle Scholar
  78. Kappes, D.J., He, X., and He, X. 2006. Immunol Rev 209:237–252.PubMedGoogle Scholar
  79. Kaye, J., Hsu, M.L., Sauron, M.E., Jameson, S.C., Gascoigne, N.R., and Hedrick, S.M. 1989. Nature 341:746–749.PubMedGoogle Scholar
  80. Kenins, L., Gill, J.W., Boyd, R.L., Hollander, G.A., and Wodnar-Filipowicz, A. 2008. J Exp Med 205:523–531.PubMedGoogle Scholar
  81. Kioussis, D. and Ellmeier, W. 2002. Nat Rev Immunol 2:909–919.PubMedGoogle Scholar
  82. Kondo, M., Weissman, I.L., and Akashi, K. 1997. Cell 91:661–672.PubMedGoogle Scholar
  83. Krangel, M.S. 2007. Nat Immunol 8:687–694.PubMedGoogle Scholar
  84. Krueger, A. and von Boehmer, H. 2007. Immunity 26:105–116.PubMedGoogle Scholar
  85. Kurobe, H., Liu, C., Ueno, T., Saito, F., Ohigashi, I., Seach, N., Arakaki, R., Hayashi, Y., Kitagawa, T., Lipp, M., Boyd, R.L., and Takahama, Y. 2006. Immunity 24:165–177.PubMedGoogle Scholar
  86. Kyewski, B.A. 1987. J Exp Med 166:520–538.PubMedGoogle Scholar
  87. Lai, A.Y., and Kondo, M. 2007. Proc Natl Acad Sci USA 104:6311–6316.PubMedGoogle Scholar
  88. Laiosa, C.V., Stadtfeld, M., and Graf, T. 2006a. Annu Rev Immunol 24:705–738.Google Scholar
  89. Laiosa, C.V., Stadtfeld, M., Xie, H., de Andres-Aguayo, L., and Graf, T. 2006b. Immunity 25:731–744.Google Scholar
  90. Lambolez, F., Kronenberg, M., and Cheroutre, H. 2007. Immunol Rev 215:178–188.PubMedGoogle Scholar
  91. Laufer, T.M., DeKoning, J., Markowitz, J. S., Lo, D., and Glimcher, L. H. 1996. Nature 383:81–85.PubMedGoogle Scholar
  92. Lauritsen, J.P., Haks, M.C., Lefebvre, J.M., Kappes, D.J., and Wiest, D.L. 2006. Immunol Rev 209:176–190.PubMedGoogle Scholar
  93. Lesley, J., Hyman, R., and Schulte, R. 1985. Cell Immunol 91:397–403.PubMedGoogle Scholar
  94. Li, Z., Dordai, D. I., Lee, J., and Desiderio, S. 1996. Immunity 5:575–589.PubMedGoogle Scholar
  95. Lind, E. F., Prockop, S.E., Porritt, H.E., and Petrie, H.T. 2001. J Exp Med 194:127–134.PubMedGoogle Scholar
  96. Liu, C., Ueno, T., Kuse, S., Saito, F., Nitta, T., Piali, L., Nakano, H., Kakiuchi, T., Lipp, M., Hollander, G.A., and Takahama, Y. 2005. Blood 105:31–39.PubMedGoogle Scholar
  97. Liu, C., Saito, F., Liu, Z., Lei, Y., Uehara, S., Love, P., Lipp, M., Kondo, S., Manley, N., and Takahama, Y. 2006. Blood 108:2531–2539.PubMedGoogle Scholar
  98. Lo, D. and Sprent, J. 1986. Nature 319:672–675.PubMedGoogle Scholar
  99. Mackarehtschian, K., Hardin, J.D., Moore, K.A., Boast, S., Goff, S.P., and Lemischka, I.R. 1995. Immunity 3:147–161.PubMedGoogle Scholar
  100. Maeda, T., Merghoub, T., Hobbs, R.M., Dong, L., Maeda, M., Zakrzewski, J., van den Brink, M.R., Zelent, A., Shigematsu, H., Akashi, K., Teruya-Feldstein, J., Cattoretti, G., and Pandolfi, P.P. 2007. Science 316:860–866.PubMedGoogle Scholar
  101. Maillard, I., Fang, T., and Pear, W.S. 2005. Annu Rev Immunol 23:945–974.PubMedGoogle Scholar
  102. Maillard, I., Koch, U., Dumortier, A., Shestova, O., Xu, L., Sai, H., Pross, S.E., Aster, J.C., Bhandoola, A., Radtke, F., and Pear, W.S. 2008. Cell Stem Cell 2:356–366.PubMedGoogle Scholar
  103. Martin, C.H., Aifantis, I., Scimone, M.L., Von Andrian, U.H., Reizis, B., Von Boehmer, H., and Gounari, F. 2003. Nat Immunol 4:866–873.PubMedGoogle Scholar
  104. Mathieu, N., Hempel, W.M., Spicuglia, S., Verthuy, C., and Ferrier, P. 2000. J Exp Med 192:625–636.PubMedGoogle Scholar
  105. Mathis, D. and Benoist, C. 2007. Nat Rev Immunol 7:645–650.PubMedGoogle Scholar
  106. Matloubian, M., Lo, C.G., Cinamon, G., Lesneski, M.J., Xu, Y., Brinkmann, V., Allende, M.L., Proia, R.L., and Cyster, J. G. 2004. Nature 427:355–360.PubMedGoogle Scholar
  107. McCaughtry, T.M., Wilken, M.S., and Hogquist, K.A. 2007. J Exp Med 204:2513–2520.PubMedGoogle Scholar
  108. Melichar, H.J., Narayan, K., Der, S. D., Hiraoka, Y., Gardiol, N., Jeannet, G., Held, W., Chambers, C.A., and Kang, J. 2007. Science 315:230–233.PubMedGoogle Scholar
  109. Michie, A.M., Carlyle, J.R., and Zuniga-Pflucker, J.C. 1998. J Immunol 160:1735–1741.PubMedGoogle Scholar
  110. Miller, J. F. and Osoba, D. 1967. Physiol Rev 47:437–520.PubMedGoogle Scholar
  111. Morrison, S.J., Uchida, N., and Weissman, I.L. 1995. Annu Rev Cell Dev Biol 11:35–71.PubMedGoogle Scholar
  112. Nikolich-Zugich, J., Slifka, M.K., and Messaoudi, I. 2004. Nat Rev Immunol 4:123–132.PubMedGoogle Scholar
  113. Norment, A.M., Salter, R.D., Parham, P., Engelhard, V.H., and Littman, D.R. 1988. Nature 336:79–81.PubMedGoogle Scholar
  114. Ogawa, M., Matsuzaki, Y., Nishikawa, S., Hayashi, S., Kunisada, T., Sudo, T., Kina, T., and Nakauchi, H. 1991. J Exp Med 174:63–71.PubMedGoogle Scholar
  115. Pai, S. Y., Truitt, M.L., Ting, C.N., Leiden, J.M., Glimcher, L.H., and Ho, I. C. 2003. Immunity 19:863–875.PubMedGoogle Scholar
  116. Pearse, M., Wu, L., Egerton, M., Wilson, A., Shortman, K., and Scollay, R. 1989. Proc Natl Acad Sci USA 86:1614–1618.PubMedGoogle Scholar
  117. Penit, C. and Vasseur, F. 1988. J Immunol 140:3315–3323.PubMedGoogle Scholar
  118. Perry, S.S., Welner, R.S., Kouro, T., Kincade, P.W., and Sun, X.H. 2006. J Immunol 177:2880–2887.PubMedGoogle Scholar
  119. Peschon, J.J., Morrissey, P.J., Grabstein, K.H., Ramsdell, F.J., Maraskovsky, E., Gliniak, B.C., Park, L.S., Ziegler, S.F., Williams, D.E., Ware, C.B., et al. 1994. J Exp Med 180:1955–1960.PubMedGoogle Scholar
  120. Petrie, H.T. and Zuniga-Pflucker, J. C. 2007. Annu Rev Immunol 25:649–679.PubMedGoogle Scholar
  121. Petrie, H.T., Pearse, M., Scollay, R., and Shortman, K. 1990. Eur J Immunol 20:2813–2815.PubMedGoogle Scholar
  122. Petrie, H.T., Livak, F., Schatz, D.G., Strasser, A., Crispe, I.N., and Shortman, K. 1993. J Exp Med 178:615–622.PubMedGoogle Scholar
  123. Porritt, H.E., Gordon, K., and Petrie, H.T. 2003. J Exp Med 198:957–962.PubMedGoogle Scholar
  124. Porritt, H.E., Rumfelt, L.L., Tabrizifard, S., Schmitt, T. M., Zuniga-Pflucker, J.C., and Petrie, H.T. 2004. Immunity 20:735–745.PubMedGoogle Scholar
  125. Prockop, S.E. and Petrie, H.T. 2004. J Immunol 173:1604–1611.PubMedGoogle Scholar
  126. Pui, J.C., Allman, D., Xu, L., DeRocco, S., Karnell, F. G., Bakkour, S., Lee, J.Y., Kadesch, T., Hardy, R.R., Aster, J.C., and Pear, W. S. 1999. Immunity 11:299–308.PubMedGoogle Scholar
  127. Radtke, F., Wilson, A., Stark, G., Bauer, M., van Meerwijk, J., MacDonald, H.R., and Aguet, M. 1999. Immunity 10:547–558.PubMedGoogle Scholar
  128. Reizis, B. and Leder, P. 2001. J Exp Med 194:979–990.PubMedGoogle Scholar
  129. Reizis, B. and Leder, P. 2002. Genes Dev 16:295–300.PubMedGoogle Scholar
  130. Rodewald, H.R. 2008. Annu Rev Immunol 26:355–388.PubMedGoogle Scholar
  131. Rodewald, H.R., Kretzschmar, K., Takeda, S., Hohl, C., and Dessing, M. 1994. EMBO J 13:4229–4240.PubMedGoogle Scholar
  132. Rodewald, H.R., Waskow, C., and Haller, C. 2001. J Exp Med 193:1431–1437.PubMedGoogle Scholar
  133. Rossi, F.M., Corbel, S.Y., Merzaban, J.S., Carlow, D.A., Gossens, K., Duenas, J., So, L., Yi, L., and Ziltener, H.J. 2005. Nat Immunol 6:626–634.PubMedGoogle Scholar
  134. Rothenberg, E.V., Moore, J.E., and Yui, M.A. 2008. Nat Rev Immunol 8:9–21.PubMedGoogle Scholar
  135. Rumfelt, L. L., Zhou, Y., Rowley, B.M., Shinton, S.A., and Hardy, R.R. 2006. J Exp Med 203:675–687.PubMedGoogle Scholar
  136. Sambandam, A., Maillard, I., Zediak, V. P., Xu, L., Gerstein, R.M., Aster, J.C., Pear, W.S., and Bhandoola, A. 2005. Nat Immunol 6:663–670.PubMedGoogle Scholar
  137. Sawada, S., Scarborough, J.D., Killeen, N., and Littman, D.R. 1994. Cell 77:917–929.PubMedGoogle Scholar
  138. Schlissel, M.S., Durum, S.D., and Muegge, K. 2000. J Exp Med 191:1045–1050.PubMedGoogle Scholar
  139. Schmitt, T.M. and Zuniga-Pflucker, J. C. 2002. Immunity 17:749–756.PubMedGoogle Scholar
  140. Schmitt, T.M., Ciofani, M., Petrie, H. T., and Zuniga-Pflucker, J.C. 2004. J Exp Med 200:469–479.PubMedGoogle Scholar
  141. Schwarz, B.A. and Bhandoola, A. 2004. Nat Immunol 5:953–960.PubMedGoogle Scholar
  142. Schwarz, B.A. and Bhandoola, A. 2006. Immunol Rev 209:47–57.PubMedGoogle Scholar
  143. Schwarz, B.A., Sambandam, A., Maillard, I., Harman, B.C., Love, P.E., and Bhandoola, A. 2007. J Immunol 178:2008–2017.PubMedGoogle Scholar
  144. Scimone, M.L., Aifantis, I., Apostolou, I., von Boehmer, H., and von Andrian, U.H. 2006. Proc Natl Acad Sci USA 103:7006–7011.PubMedGoogle Scholar
  145. Scollay, R., Smith, J., and Stauffer, V. 1986. Immunol Rev 91:129–157.PubMedGoogle Scholar
  146. Sebzda, E., Wallace, V.A., Mayer, J., Yeung, R.S., Mak, T.W., and Ohashi, P.S. 1994. Science 263:1615–1618.PubMedGoogle Scholar
  147. Setoguchi, R., Tachibana, M., Naoe, Y., Muroi, S., Akiyama, K., Tezuka, C., Okuda, T., and Taniuchi, I. 2008. Science 319:822–825.PubMedGoogle Scholar
  148. Shin, S., El-Diwany, R., Schaffert, S., Adams, E.J., Garcia, K.C., Pereira, P., and Chien, Y.H. 2005. Science 308:252–255.PubMedGoogle Scholar
  149. Shortman, K. and Wu, L. 1996. Annu Rev Immunol 14:29–47.PubMedGoogle Scholar
  150. Shortman, K., Egerton, M., Spangrude, G.J., and Scollay, R. 1990. Semin Immunol 2:3–12.PubMedGoogle Scholar
  151. Singer, A. and Bosselut, R. 2004. Adv Immunol 83:91–131.PubMedGoogle Scholar
  152. Sitnicka, E., Bryder, D., Theilgaard-Monch, K., Buza-Vidas, N., Adolfsson, J., and Jacobsen, S.E. 2002. Immunity 17:463–472.PubMedGoogle Scholar
  153. Starr, T.K., Jameson, S.C., and Hogquist, K.A. 2003. Annu Rev Immunol 21:139–176.PubMedGoogle Scholar
  154. Sun, G., Liu, X., Mercado, P., Jenkinson, S.R., Kypriotou, M., Feigenbaum, L., Galera, P., and Bosselut, R. 2005. Nat Immunol 6:373–381.PubMedGoogle Scholar
  155. Taghon, T., Yui, M.A., Pant, R., Diamond, R.A., and Rothenberg, E.V. 2006. Immunity 24:53–64.PubMedGoogle Scholar
  156. Taghon, T.N., David, E.S., Zuniga-Pflucker, J.C., and Rothenberg, E.V. 2005. Genes Dev 19: 965–978.PubMedGoogle Scholar
  157. Takeuchi, A., Yamasaki, S., Takase, K., Nakatsu, F., Arase, H., Onodera, M., and Saito, T. 2001. J Immunol 167:2157–2163.PubMedGoogle Scholar
  158. Talebian, L., Li, Z., Guo, Y., Gaudet, J., Speck, M. E., Sugiyama, D., Kaur, P., Pear, W.S., Maillard, I., and Speck, N.A. 2007. Blood 109:11–21.PubMedGoogle Scholar
  159. Tan, J.B., Visan, I., Yuan, J.S., and Guidos, C.J. 2005. Nat Immunol 6:671–679.PubMedGoogle Scholar
  160. Tanigaki, K. and Honjo, T. 2007. Nat Immunol 8:451–456.PubMedGoogle Scholar
  161. Tanigaki, K., Tsuji, M., Yamamoto, N., Han, H., Tsukada, J., Inoue, H., Kubo, M., and Honjo, T. 2004. Immunity 20:611–622.PubMedGoogle Scholar
  162. Taniuchi, I., Osato, M., Egawa, T., Sunshine, M.J., Bae, S.C., Komori, T., Ito, Y., and Littman, D.R. 2002. Cell 111:621–633.PubMedGoogle Scholar
  163. Teh, H.S., Kisielow, P., Scott, B., Kishi, H., Uematsu, Y., Bluthmann, H., and von Boehmer, H. 1988. Nature 335:229–233.PubMedGoogle Scholar
  164. Turka, L.A., Schatz, D.G., Oettinger, M. A., Chun, J.J., Gorka, C., Lee, K., McCormack, W.T., and Thompson, C.B. 1991. Science 253:778–781.PubMedGoogle Scholar
  165. Turner, J.M., Brodsky, M.H., Irving, B.A., Levin, S.D., Perlmutter, R.M., and Littman, D.R. 1990. Cell 60:755–765.PubMedGoogle Scholar
  166. Uehara, S., Grinberg, A., Farber, J.M., and Love, P. E. 2002. J Immunol 168:2811–2819.PubMedGoogle Scholar
  167. Ueno, T., Saito, F., Gray, D.H., Kuse, S., Hieshima, K., Nakano, H., Kakiuchi, T., Lipp, M., Boyd, R.L., and Takahama, Y. 2004. J Exp Med 200:493–505.PubMedGoogle Scholar
  168. Van Laethem, F., Sarafova, S.D., Park, J.H., Tai, X., Pobezinsky, L., Guinter, T.I., Adoro, S., Adams, A., Sharrow, S. O., Feigenbaum, L., and Singer, A. 2007. Immunity 27:735–750.PubMedGoogle Scholar
  169. von Boehmer, H. 2005. Nat Rev Immunol 5:571–577.Google Scholar
  170. Wada, H., Masuda, K., Satoh, R., Kakugawa, K., Ikawa, T., Katsura, Y., and Kawamoto, H. 2008. Nature 452:768–772.PubMedGoogle Scholar
  171. Wallis, V.J., Leuchars, E., Chwalinski, S., and Davies, A.J. 1975. Transplantation 19:2–11.PubMedGoogle Scholar
  172. Waskow, C., Paul, S., Haller, C., Gassmann, M., and Rodewald, H. 2002. Immunity 17:277–288.PubMedGoogle Scholar
  173. Weng, A.P., Millholland, J.M., Yashiro-Ohtani, Y., Arcangeli, M.L., Lau, A., Wai, C., Del Bianco, C., Rodriguez, C.G., Sai, H., Tobias, J., Li, Y., Wolfe, M.S., Shachaf, C., Felsher, D., Blacklow, S.C., Pear, W.S., and Aster, J.C. 2006. Genes Dev 20:2096–2109.PubMedGoogle Scholar
  174. White, J., Herman, A., Pullen, A.M., Kubo, R., Kappler, J.W., and Marrack, P. 1989. Cell 56:27–35.PubMedGoogle Scholar
  175. Wildt, K. F., Sun, G., Grueter, B., Fischer, M., Zamisch, M., Ehlers, M., and Bosselut, R. 2007. J Immunol 179: 4405–4414.PubMedGoogle Scholar
  176. Wolfer, A., Wilson, A., Nemir, M., MacDonald, H.R., and Radtke, F. 2002. Immunity 16:869–879.PubMedGoogle Scholar
  177. Woolf, E., Xiao, C., Fainaru, O., Lotem, J., Rosen, D., Negreanu, V., Bernstein, Y., Goldenberg, D., Brenner, O., Berke, G., Levanon, D., and Groner, Y. 2003. Proc Natl Acad Sci USA 100:7731–7736.PubMedGoogle Scholar
  178. Wright, D.E., Wagers, A.J., Gulati, A.P., Johnson, F.L., and Weissman, I.L. 2001. Science 294:1933–1936.PubMedGoogle Scholar
  179. Wu, L., Antica, M., Johnson, G.R., Scollay, R., and Shortman, K. 1991a. J Exp Med 174:1617–1627.Google Scholar
  180. Wu, L., Scollay, R., Egerton, M., Pearse, M., Spangrude, G.J., and Shortman, K. 1991b. Nature 349:71–74.Google Scholar
  181. Wurbel, M.A., Malissen, B., and Campbell, J. J. 2006. Eur J Immunol 36:73–81.PubMedGoogle Scholar
  182. Xi, H., Schwartz, R., Engel, I., Murre, C., and Kersh, G. J. 2006. Immunity 24:813–826.PubMedGoogle Scholar
  183. Yamasaki, S. and Saito, T. 2007. Trends Immunol 28:39–43.PubMedGoogle Scholar
  184. Yasutomo, K., Doyle, C., Miele, L., Fuchs, C., and Germain, R. N. 2000. Nature 404:506–510.PubMedGoogle Scholar
  185. Yoshida, T., Ng, S.Y., Zuniga-Pflucker, J.C., and Georgopoulos, K. 2006. Nat Immunol 7: 382–391.PubMedGoogle Scholar
  186. Yu, Q., Erman, B., Bhandoola, A., Sharrow, S.O., and Singer, A. 2003. J Exp Med 197:475–487.PubMedGoogle Scholar
  187. Yu, Q., Park, J. H., Doan, L.L., Erman, B., Feigenbaum, L., and Singer, A. 2006. J Exp Med 203:165–175.PubMedGoogle Scholar
  188. Yucel, R., Karsunky, H., Klein-Hitpass, L., and Moroy, T. 2003. J Exp Med 197:831–844.PubMedGoogle Scholar
  189. Zou, Y.R., Sunshine, M.J., Taniuchi, I., Hatam, F., Killeen, N., and Littman, D.R. 2001. Nat Genet 29:332–336.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Pathology and Laboratory MedicineUniversity of Pennsylvania School of MedicinePhiladelphiaUSA

Personalised recommendations