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Class Switch Recombination: An Emerging Mechanism

  • A. L. Kenter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 290)

Abstract

Class switch recombination (CSR) has been the least well understood of the Ig gene DNA rearrangements. The discovery that activation-induced deaminase (AID) is a pivotal player in CSR as well as somatic hypermutation (SHM) and its variant, gene conversion, represents a sea change in our understanding of these processes. The recognition that AID directly deaminates ssDNA has provided a springboard toward the emergence of a model that explains the initiation of these events. Nonhomologous end joining (NHEJ), the main pathway for the repair of double-strand breaks in mammalian cells plays a key role in the resolution of CSR transactions. Mediators of general double-strand break repair are also involved in CSR and are mutated in several immunodeficiency diseases. A global picture of the mechanism of CSR is emerging and is providing new insights toward understanding the genetic events that underlie B cell cancers.

Keywords

Base Excision Repair Primary Immunodeficiency Disease Class Switch Recombination Nijmegen Breakage Syndrome Histone Hyperacetylation 
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.

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References

  1. Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D (2000) Cell 103:667–678PubMedGoogle Scholar
  2. Alt FW, Rosenberg N, Casanova RJ, Thomas E, Baltimore D (1982) Nature 296:325–331PubMedGoogle Scholar
  3. Andegeko Y, Moyal L, Mittelman L, Tsarfaty I, Shiloh Y, Rotman G (2001) J Biol Chem 276:38224–38230PubMedGoogle Scholar
  4. Arakawa H, Hauschild J, Buerstedde JM (2002) Science 295:1301–1306PubMedGoogle Scholar
  5. Bachl J, Carlson C, Gray-Schopfer V, Dessing M, Olsson C (2001) J Immunol 166:5051–5057PubMedGoogle Scholar
  6. Bardwell PD, Martin A, Wong E, Li Z, Edelmann W, Scharff MD (2003) J Immunol 170:1620–1624PubMedGoogle Scholar
  7. Barreto V, Reina-San-Martin B, Ramiro AR, McBride KM, Nussenzweig MC (2003) Mol Cell 12:501–508PubMedGoogle Scholar
  8. Becker-Catania SG, Gatti RA (2001) Adv Exp Med Biol 495:191–198PubMedGoogle Scholar
  9. Betz AG, Milstein C, Gonzalez-Fernandez A, Pannell R, Larson T, Neuberger MS (1994) Cell 77:239–248PubMedGoogle Scholar
  10. Bosma GC, Kim J, Urich T, Fath DM, Cotticelli MG, Ruetsch NR, Radic MZ, Bosma MJ (2002) J Exp Med 196:1483–1495PubMedGoogle Scholar
  11. Bottaro A, Lansford R, Xu L, Zhang J, Rothman P, Alt F (1994) EMBO J 13:665–674PubMedGoogle Scholar
  12. Bottaro A, Young F, Chen J, Serwe M, Sablitzky F, Alt FW (1998) Int Immunol 10:799–806PubMedGoogle Scholar
  13. Bransteitter R, Pham P, Scharff MD, Goodman MF (2003) Proc Natl Acad Sci USA 100:4102–4107PubMedGoogle Scholar
  14. Bross L, Fukita Y, McBlane F, Demolliere C, Rajewsky K, Jacobs H (2000) Immunity 13:589–597PubMedGoogle Scholar
  15. Brown EJ, Baltimore D (2003) Genes Dev 17:615–628PubMedGoogle Scholar
  16. Buerstedde JM, Arakawa H, Watahiki A, Carninci PP, Hayashizaki YY, Korn B, Plachy J (2002) Nucleic Acids Res 30:230–231PubMedGoogle Scholar
  17. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ (2001) J Biol Chem 276:42462–42467PubMedGoogle Scholar
  18. Casellas R, Nussenzweig A, Wuerffel R, Pelanda R, Reichlin A, Suh H, Qin X-F, Besmer E, Kenter A, Rajewsky K, Nussenzweig MC (1998) EMBO J 17:2404–2411PubMedGoogle Scholar
  19. Catalan N, Selz F, Imai K, Revy P, Fischer A, Durandy A (2003) J Immunol 171:2504–2509PubMedGoogle Scholar
  20. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, Redon C, Pilch DR, Olaru A, Eckhaus M, Camerini-Otero RD, Tessarollo L, Livak F, Manova K, Bonner WM, Nussenzweig MC, Nussenzweig A (2002) Science 296:922–927PubMedGoogle Scholar
  21. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A (2003) Nat Cell Biol 5:675–679PubMedGoogle Scholar
  22. Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW (2003) Nature 422:726–730PubMedGoogle Scholar
  23. Chen X, Kinoshita K, Honjo T (2001) Proc Natl Acad Sci USA 98:13860–13865PubMedGoogle Scholar
  24. Chu G (1997) J Biol Chem 272:24097–24100PubMedGoogle Scholar
  25. Chua KF, Alt FW, Manis JP (2002) J Exp Med 195:F37–F41PubMedGoogle Scholar
  26. Cogne M, Lansford R, Bottaro A, Zhang J, Gorman J, Young F, Cheng HL, Alt FW (1994) Cell 77:737–747PubMedGoogle Scholar
  27. Crawford TO (1998) Semin Pediatr Neurol 5:287–294PubMedGoogle Scholar
  28. Daniels GA, Lieber MR ( 1995) Nucl Acids Res 23:5006–5011PubMedGoogle Scholar
  29. Deenick EK, Hasbold J, Hodgkin PD (1999) J Immunol 163:4707–4714PubMedGoogle Scholar
  30. Dickerson SK, Market E, Besmer E, Papavasiliou FN (2003) J Exp Med 197:1291–1296PubMedGoogle Scholar
  31. Digweed M, Reis A, Sperling K (1999) Bioessays 21:649–656PubMedGoogle Scholar
  32. Doi T, Kinoshita K, Ikegawa M, Muramatsu M, Honjo T (2003) Proc Natl Acad Sci USA 100:2634–2638PubMedGoogle Scholar
  33. Du J, Zu Y, Shanmugam A, Kenter AL (1997) Nuc Acids Res 25:3066–3073Google Scholar
  34. Dudley DD, Manis JP, Zarrin AA, Kaylor L, Tian M, Alt FW (2002) Proc Natl Acad Sci USA 99:9984–9989PubMedGoogle Scholar
  35. Dunnick W, Stavnezer J (1990) Mol Cell Biol 10:397–400PubMedGoogle Scholar
  36. Dunnick W, Wilson M, Stavnezer J (1989) Mol Cell Biol 9:1850–1856PubMedGoogle Scholar
  37. Dunnick W, Hertz GZ, Scappino L, Gritzmacher C (1993) Nuc Acids Res 21:365–372Google Scholar
  38. Ehrenstein MR, Neuberger MS (1999) EMBO J 18:3484–3490PubMedGoogle Scholar
  39. Ehrenstein MR, Rada C, Jones AM, Milstein C, Neuberger MS (2001) Proc Natl Acad Sci USA 98:14553–14558PubMedGoogle Scholar
  40. Eto T, Kinoshita K, Yoshikawa K, Muramatsu M, Honjo T (2003) Proc Natl Acad Sci USA 100:12895–12898PubMedGoogle Scholar
  41. Faili A, Aoufouchi S, Flatter E, Gueranger Q, Reynaud CA, Weill JC (2002a) Nature 419:944–947PubMedGoogle Scholar
  42. Faili A, Aoufouchi S, Gueranger Q, Zober C, Leon A, Bertocci B, Weill JC, Reynaud CA (2002b) Nat Immunol 3:815–821PubMedGoogle Scholar
  43. Friedberg EC, Feaver WJ, Gerlach VL (2000) Proc Natl Acad Sci USA 97:5681–5683PubMedGoogle Scholar
  44. Fukita Y, Jacobs H, Rajewsky K (1998) Immunity 9:105–114PubMedGoogle Scholar
  45. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, Sedelnikova OA, Pilch DR, Rogakou EP, Celeste A, Chen HT, Nussenzweig A, Aladjem MI, Bonner WM, Pommier Y (2003) J Biol Chem 278:20303–20312PubMedGoogle Scholar
  46. Golding GB, Gearhart PJ, Glickman BW (1987) Genetics 115:169–176PubMedGoogle Scholar
  47. Gritzmacher CA (1989) Crit Rev Immunol 9:173–200PubMedGoogle Scholar
  48. Gu H, Zou YR, Rajewsky K (1993) Cell 73:1155–1164PubMedGoogle Scholar
  49. Harriman GR, Bradley A, Das S, Rogers-Fani P, Davis AC (1996) J Clin Invest 97:477–485PubMedGoogle Scholar
  50. Harris RS, Petersen-Mahrt SK, Neuberger MS (2002) Mol Cell 10:1247–53PubMedGoogle Scholar
  51. Hesslein DC, Schatz D (2001) Adv Immunol 78:169–232PubMedGoogle Scholar
  52. Hodgkin PD, Lee JH, Lyons AB (1996) J Exp Med 184:277–281PubMedGoogle Scholar
  53. Honjo T, Kinoshita K, Muramatsu M (2002) Annu Rev Immunol 20:165–196PubMedGoogle Scholar
  54. Hummel M, Berry JK, Dunnick W (1987) J Immunol 138:3539–3548PubMedGoogle Scholar
  55. Imai K, Catalan N, Plebani A, Marodi L, Sanal O, Kumaki S, Nagendran V, Wood P, Glastre C, Sarrot-Reynauld F, Hermine O, Forveille M, Revy P, Fischer A, Durandy A (2003a) J Clin Invest 112:136–142PubMedGoogle Scholar
  56. Imai K, Slupphaug G, Lee WI, Revy P, Nonoyama S, Catalan N, Yel L, Forveille M, Kavli B, Krokan HE, Ochs HD, Fischer A, Durandy A (2003b) Nat Immunol 4:1023–1028PubMedGoogle Scholar
  57. Jung S, Rajewsky K, Radbruch A (1993) Science 259:984–987PubMedGoogle Scholar
  58. Kenter AL (1999) J Exp Med 190:307–310PubMedGoogle Scholar
  59. Kenter AL (2003) Curr Opin Immunol 15:190–198PubMedGoogle Scholar
  60. Kenter AL, Tredup J (1991) Mol Cell Biol 11:4398–4404PubMedGoogle Scholar
  61. Kenter AL, Wuerffel R, Dominguez C, Shanmugam A, Zhang H (2004) J Exp Med 199:617–627PubMedGoogle Scholar
  62. Khamlichi AA, Pinaud E, Decourt C, Chauveau C, Cogne M (2000) Adv Immunol 75:317–345PubMedGoogle Scholar
  63. Kinoshita K, Tashiro J, Lee C-G, Honjo T (1998) Immunity 9:849–858PubMedGoogle Scholar
  64. Kobayashi J, Tauchi H, Sakamoto S, Nakamura A, Morishima K, Matsuura S, Kobayashi T, Tamai K, Tanimoto K, Komatsu K (2002) Curr Biol 12:1846–1851PubMedGoogle Scholar
  65. Krangel MS (2003) Nat Immunol 4:624–630PubMedGoogle Scholar
  66. Lebecque SG, Gearhart PJ (1990) J Exp Med 172:1717–1727PubMedGoogle Scholar
  67. Lee CG, Kinoshita K, Arudchandran A, Cerritelli SM, Crouch RJ, Honjo T (2001) J Exp Med 194:365–374PubMedGoogle Scholar
  68. Lee CG, Kondo S, Honjo T (1998) Curr Biol 8:227–230PubMedGoogle Scholar
  69. Lieber MR, Ma Y, Pannicke U, Schwarz K (2003) Nat Rev Mol Cell Biol 4:712–720PubMedGoogle Scholar
  70. Lindahl T (2000) Mutat Res 462:129–135PubMedGoogle Scholar
  71. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G, Recillas-Targa F, Prioleau MN (2001a) Science 293:2453–2455PubMedGoogle Scholar
  72. Litt MD, Simpson M, Recillas-Targa F, Prioleau MN, Felsenfeld G (2001b) EMBO J 20:2224–2235PubMedGoogle Scholar
  73. Luby TM, Schrader CE, Stavnezer J, Selsing E (2001) J Exp Med 193:159–168PubMedGoogle Scholar
  74. Ma L, Wortis HH, Kenter AL (2002) J Immunol 168:2835–2846PubMedGoogle Scholar
  75. Madisen L, Groudine M (1994) Genes Dev 8:2212–2226PubMedGoogle Scholar
  76. Manis J, Gu Y, Lansford R, Sonoda E, Ferrini R, Davidson L, Rajewsky K, Alt F (1998a) J Exp Med 187:2081–2089PubMedGoogle Scholar
  77. Manis JP, van der Stoep N, Tian M, Ferrini R, Davidson L, Bottaro A, Alt FW (1998b) J Exp Med 188:1421–1431PubMedGoogle Scholar
  78. Manis JP, Dudley D, Kaylor L, Alt FW (2002a) Immunity 16:607–617PubMedGoogle Scholar
  79. Manis JP, Tian M, Alt FW (2002b) Trends Immunol 23:31–39PubMedGoogle Scholar
  80. Manis JP, Michaelson JS, Birshtein BK, Alt FW (2003) Mol Immunol 39:753–760PubMedGoogle Scholar
  81. Manser T (1987) J Immunol 139:234–238PubMedGoogle Scholar
  82. Martin A, Li Z, Lin DP, Bardwell PD, Iglesias-Ussel MD, Edelmann W, Scharff MD (2003) J Exp Med 198:1171–1178PubMedGoogle Scholar
  83. Martin A, Scharff MD (2002) Proc Natl Acad Sci USA 99:12304–12308PubMedGoogle Scholar
  84. Millar CB, Guy J, Sansom OJ, Selfridge J, MacDougall E, Hendrich B, Keightley PD, Bishop SM, Clarke AR, Bird A (2002) Science 297:403–405PubMedGoogle Scholar
  85. Min IM, Schrader CE, Vardo J, Luby TM, D'Avirro N, Stavnezer J, Selsing E (2003) Immunity 19:515–524PubMedGoogle Scholar
  86. Mostoslavsky R, Alt FW, Bassing CH (2003) Nat Immunol 4:603–606PubMedGoogle Scholar
  87. Muramatsu M, Sankaranand VS, Anant S, Sugai M, Kinoshita K, Davidson NO, Honjo T (1999) J Biol Chem 274:18470–18476PubMedGoogle Scholar
  88. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T (2000) Cell 102:553–563PubMedGoogle Scholar
  89. Nagaoka H, Muramatsu M, Yamamura N, Kinoshita K, Honjo T (2002) J Exp Med 195:529–534PubMedGoogle Scholar
  90. Neddermann P, Gallinari P, Lettieri T, Schmid D, Truong O, Hsuan JJ, Wiebauer K, Jiricny J (1996) J Biol Chem 271:12767–12774PubMedGoogle Scholar
  91. Nilsen H, Rosewell I, Robins P, Skjelbred CF, Andersen S, Slupphaug G, Daly G, Krokan HE, Lindahl T, Barnes DE (2000) Mol Cell 5:1059–1065PubMedGoogle Scholar
  92. Nilsen H, Haushalter KA, Robins P, Barnes DE, Verdine GL, Lindahl T (2001) EMBO J 20:4278–4286PubMedGoogle Scholar
  93. Nilsen H, Stamp G, Andersen S, Hrivnak G, Krokan HE, Lindahl T, Barnes DE (2003) Oncogene 22:5381–5386PubMedGoogle Scholar
  94. Okazaki IM, Kinoshita K, Muramatsu M, Yoshikawa K, Honjo T (2002) Nature 416:340–345PubMedGoogle Scholar
  95. Pan Q, Petit-Frere C, Lahdesmaki A, Gregorek H, Chrzanowska KH, Hammarstrom L (2002) Eur J Immunol 32:1300–1308PubMedGoogle Scholar
  96. Pan-Hammarstrom Q, Dai S, Zhao Y, van Dijk-Hard IF, Gatti RA, Borresen-Dale AL, Hammarstrom L (2003) J Immunol 170:3707–3716PubMedGoogle Scholar
  97. Papavasiliou FN, Schatz DG (2000) Nature 408:216–221PubMedGoogle Scholar
  98. Papavasiliou FN, Schatz DG (2002) J Exp Med 195:1193–1198PubMedGoogle Scholar
  99. Paques F, Haber JE (1997) Mol Cell Biol 17:6765–6771PubMedGoogle Scholar
  100. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM (2000) Curr Biol 10:886–895PubMedGoogle Scholar
  101. Peters A, Storb U (1996) Immunity 4:57–65PubMedGoogle Scholar
  102. Petersen S, Casellas R, Reina-San-Martin B, Chen HT, Difilippantonio MJ, Wilson PC, Hanitsch L, Celeste A, Muramatsu M, Pilch DR, Redon C, Ried T, Bonner WM, Honjo T, Nussenzweig MC, Nussenzweig A (2001) Nature 414:660–665PubMedGoogle Scholar
  103. Petersen-Mahrt SK, Harris RS, Neuberger MS (2002) Nature 418:99–103PubMedGoogle Scholar
  104. Pham P, Bransteitter R, Petruska J, Goodman MF (2003) Nature 424:103–107PubMedGoogle Scholar
  105. Qiu G, Harriman GR, Stavnezer J (1999) Int Immunol 11:37–46PubMedGoogle Scholar
  106. Rada C, Yelamos J, Dean W, Milstein C (1997) Eur J Immunol 27:3115–120PubMedGoogle Scholar
  107. Rada C, Williams GT, Nilsen H, Barnes DE, Lindahl T, Neuberger MS (2002) Curr Biol 12:1748–1755PubMedGoogle Scholar
  108. Ramiro AR, Stavropoulos P, Jankovic M, Nussenzweig MC (2003) Nat Immunol 4:452–456PubMedGoogle Scholar
  109. Reaban ME, Griffin JA (1990) Nature 348:342–344PubMedGoogle Scholar
  110. Reaban ME, Lebowitz J, Griffin JA (1994) J Biol Chem 269:21850–21857PubMedGoogle Scholar
  111. Reina-San-Martin B, Difilippantonio S, Hanitsch L, Masilamani RF, Nussenzweig A, Nussenzweig MC (2003) J Exp Med 197:1767–1778PubMedGoogle Scholar
  112. Revy P, Muto T, Levy Y, Geissmann F, Plebani A, Sanal O, Catalan N, Forveille M, Dufourcq-Labelouse R, Gennery A, Tezcan I, Ersoy F, Kayserili H, Ugazio AG, Brousse N, Muramatsu M, Notarangelo LD, Kinoshita K, Honjo T, Fischer A, Durandy A (2000) Cell 102:565–575PubMedGoogle Scholar
  113. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) J Biol Chem 273:5858–5868PubMedGoogle Scholar
  114. Rogozin IB, Kolchanov NA (1992) Biochim Biophys Acta 1171:11–18PubMedGoogle Scholar
  115. Sale JE, Neuberger MS (1998) Immunity 9:859–869PubMedGoogle Scholar
  116. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Sfez S et al. (1995) Science 268:1749–1753PubMedGoogle Scholar
  117. Schrader CE, Edelmann W, Kucherlapati R, Stavnezer J (1999) J Exp Med 190:323–330PubMedGoogle Scholar
  118. Schrader CE, Vardo J, Stavnezer J (2002) J Exp Med 195:367–373PubMedGoogle Scholar
  119. Schrader CE, Bradley SP, Vardo J, Mochegova SN, Flanagan E, Stavnezer J (2003a) EMBO J 22:5893–5903PubMedGoogle Scholar
  120. Schrader CE, Vardo J, Stavnezer J (2003b) J Exp Med 197:1377–1383PubMedGoogle Scholar
  121. Seidl KJ, Bottaro A, Vo A, Zhang J, Davidson L, Alt FW (1998) Int Immunol 10:1683–1692PubMedGoogle Scholar
  122. Shanmugam A, Shi M-J, Yauch L, Stavnezer J, Kenter A (2000) J Exp Med 191:1365–1380PubMedGoogle Scholar
  123. Shiloh Y (2003) Nat Rev Cancer 3:155–168PubMedGoogle Scholar
  124. Shinkura R, Tian M, Smith M, Chua K, Fujiwara Y, Alt FW (2003) Nat Immunol 4:435–441PubMedGoogle Scholar
  125. Sleckman BP, Gorman JR, Alt FW (1996) Annu Rev Immunol 14:459–481PubMedGoogle Scholar
  126. Smith GC, Jackson SP (1999) Genes Dev 13:916–934PubMedGoogle Scholar
  127. Smith H, Sowden M (1996) Trends Genet 12:418–424PubMedGoogle Scholar
  128. Snapper C, Zelazowski P, Rosas F, Kehry F, Tian M, Baltimore D, Sha W (1996) J Immunol 156:183–191PubMedGoogle Scholar
  129. Snapper C, Marcu KB, Zelazowski P (1997) Immunity 6:217–223PubMedGoogle Scholar
  130. Stavnezer J (2000) Curr Top Microbiol Immunol 245:127–168PubMedGoogle Scholar
  131. Stewart GS, Maser RS, Stankovic T, Bressan DA, Kaplan MI, Jaspers NG, Raams A, Byrd PJ, Petrini JH, Taylor AM (1999) Cell 99:577–587PubMedGoogle Scholar
  132. Sugawara N, Paques F, Colaiacovo M, Haber J (1997) Proc Natl Acad Sci 94:9214–9219PubMedGoogle Scholar
  133. Ta VT, Nagaoka H, Catalan N, Durandy A, Fischer A, Imai K, Nonoyama S, Tashiro J, Ikegawa M, Ito S, Kinoshita K, Muramatsu M, Honjo T (2003) Nat Immunol 4:843–848PubMedGoogle Scholar
  134. Tangye SG, Ferguson A, Avery DT, Ma CS, Hodgkin PD (2002) J Immunol 169:4298–4306PubMedGoogle Scholar
  135. Tauchi H, Matsuura S, Kobayashi J, Sakamoto S, Komatsu K, Nakamura A, Morishima K, Kobayashi T, Tamai K, Tanimoto K (2002) Oncogene 21:8967–8980PubMedGoogle Scholar
  136. Tian M, Alt FW (2000) J Biol Chem 275:24163–24172PubMedGoogle Scholar
  137. Tumas-Brundage K, Manser T (1997) J Exp Med 185:239–250PubMedGoogle Scholar
  138. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y (2003) EMBO J 22:5612–5621PubMedGoogle Scholar
  139. Ward IM, Chen J (2001) J Biol Chem 276:47759–47762PubMedGoogle Scholar
  140. Wegner R-D, Chrzanowska KH, Stumm M (1999) Ataxia-telangiectasia variants (Nijmegen breakage syndrome) In “Primary immunodeficiency diseases.” (Ochs HD, Smith CIE, Puck J.M (eds) Oxford University Press, New York, pp 324–334Google Scholar
  141. Whitmore C, Prowse DM, Haughton G, Arnold L (1991) Intl Immunol 3:95–103Google Scholar
  142. Winter E, Krawinkel U, Radbruch A (1987) EMBO J 6:1663–1671PubMedGoogle Scholar
  143. Woo CJ, Martin A, Scharff MD (2003) Immunity 19:479–489PubMedGoogle Scholar
  144. Wuerffel RA, Du J, Thompson RJ, Kenter AL (1997) J Immunol 159:4139–4144PubMedGoogle Scholar
  145. Wuerffel RA, Ma L, Kenter AL (2001) J Immunol 166:4552–4559PubMedGoogle Scholar
  146. Yoshikawa K, Okazaki IM, Eto T, Kinoshita K, Muramatsu M, Nagaoka H, Honjo T (2002) Science 296:2033–2036PubMedGoogle Scholar
  147. Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR (2003) Nat Immunol 4:442–451PubMedGoogle Scholar
  148. Zan H, Cerutti A, Dramitinos P, Schaffer A, Li Z, Casali P (1999) J Immunol 162:3437–3447PubMedGoogle Scholar
  149. Zelazowski P, Carrasco D, Rosas F, Moorman M, Bravo R, Snapper C (1997) J Immunol 159:3133–3139PubMedGoogle Scholar
  150. Zhang J, Bottaro A, Li S, Stewart V, Alt FW (1993) EMBO J 12:3529–3537PubMedGoogle Scholar
  151. Zhu Y, Nonoyama S, Morio T, Muramatsu M, Honjo T, Mizutani S (2003) J Med Dent Sci 50:41–46PubMedGoogle Scholar

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© Springer-Verlag 2005

Authors and Affiliations

  • A. L. Kenter
    • 1
  1. 1.Department of Microbiology and ImmunologyUniversity of Illinois College of MedicineChicagoUSA

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