Multiple Roles for Blimp-1 in B and T Lymphocytes

  • David Savitsky
  • Luisa Cimmino
  • Tracy Kuo
  • Gislâine A. Martins
  • Kathryn Calame
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 596)


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  1. 1.
    A. D. Keller, T. Maniatis, Identification and characterization of a novel repressor of beta-interferon gene expression, Genes Dev 5(5), 868–879 (1991).PubMedGoogle Scholar
  2. 2.
    C. A. Turner, Jr., D. H. Mack, M. M. Davis, Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells, Cell 77(2), 297–306 (1994).PubMedCrossRefGoogle Scholar
  3. 3.
    B. Ren, K. J. Chee, T. H. Kim, T. Maniatis, PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins, Genes Dev 13(1), 125–137 (1999).PubMedGoogle Scholar
  4. 4.
    J. Yu, C. Angelin-Duclos, J. Greenwood, J. Liao, K. Calame, Transcriptional repression by blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase, Mol Cell Biol 20(7), 2592–2603 (2000).PubMedCrossRefGoogle Scholar
  5. 5.
    I. Gyory, J. Wu, G. Fejer, E. Seto, K. L. Wright, PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing, Nat Immunol 5(3), 299–308 (2004).PubMedCrossRefGoogle Scholar
  6. 6.
    T. C. Kuo, K. L. Calame, B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites, J Immunol 173(9), 5556–5563 (2004).PubMedGoogle Scholar
  7. 7.
    D. H. Chang, G. Cattoretti, K. L. Calame, The dynamic expression pattern of B lymphocyte induced maturation protein-1 (Blimp-1) during mouse embryonic development, Mech Dev 117(1–2), 305–309 (2002).PubMedCrossRefGoogle Scholar
  8. 8.
    D. H. Chang, C. Angelin-Duclos, K. Calame, BLIMP-1: trigger for differentiation of myeloid lineage, Nat Immunol 1(2), 169–176 (2000).PubMedCrossRefGoogle Scholar
  9. 9.
    S. D. Vincent, N. R. Dunn, R. Sciammas, M. Shapiro-Shalef, M. M. Davis, K. Calame, E. K. Bikoff, E. J. Robertson, The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse, Development 132(6), 1315–1325 (2005).PubMedCrossRefGoogle Scholar
  10. 10.
    Y. Ohinata, B. Payer, D. O’Carroll, K. Ancelin, Y. Ono, M. Sano, S. C. Barton, T. Obukhanych, M. Nussenzweig, A. Tarakhovsky, M. Saitou, M. A. Surani, Blimp1 is a critical determinant of the germ cell lineage in mice, Nature 436(7048), 207–213 (2005).PubMedCrossRefGoogle Scholar
  11. 11.
    F. S. de Souza, V. Gawantka, A. P. Gomez, H. Delius, S. L. Ang, C. Niehrs, The zinc finger gene Xblimp1 controls anterior endomesodermal cell fate in Spemann’s organizer, Embo J 18(21), 6062–6072 (1999).PubMedCrossRefGoogle Scholar
  12. 12.
    T. Ng, F. Yu, S. Roy, A homologue of the vertebrate SET domain and zinc finger protein Blimp-1 regulates terminal differentiation of the tracheal system in the Drosophila embryo, Dev Genes Evol, (2006).Google Scholar
  13. 13.
    L. Hernandez-Lagunas, I. F. Choi, T. Kaji, P. Simpson, C. Hershey, Y. Zhou, L. Zon, M. Mercola, K. B. Artinger, Zebrafish narrowminded disrupts the transcription factor prdm1 and is required for neural crest and sensory neuron specification, Dev Biol 278(2), 347–357 (2005).PubMedCrossRefGoogle Scholar
  14. 14.
    T. P. Wilm, L. Solnica-Krezel, Essential roles of a zebrafish prdm1/blimp1 homolog in embryo patterning and organogenesis, Development 132(2), 393–404 (2005).PubMedCrossRefGoogle Scholar
  15. 15.
    D. E. Schliephake, A. Schimpl, Blimp-1 overcomes the block in IgM secretion in lipopolysaccharide/anti-mu F(ab’)2-co-stimulated B lymphocytes, Eur J Immunol 26(1), 268–271 (1996).PubMedCrossRefGoogle Scholar
  16. 16.
    J. F. Piskurich, K. I. Lin, Y. Lin, Y. Wang, J. P. Ting, K. Calame, BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells, Nat Immunol 1(6), 526–532 (2000).PubMedCrossRefGoogle Scholar
  17. 17.
    Y. Lin, K. Wong, K. Calame, Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation, Science 276(5312), 596–599 (1997).PubMedCrossRefGoogle Scholar
  18. 18.
    E. J. Messika, P. S. Lu, Y. J. Sung, T. Yao, J. T. Chi, Y. H. Chien, M. M. Davis, Differential effect of B lymphocyte-induced maturation protein (Blimp-1) expression on cell fate during B cell development, J Exp Med 188(3), 515–525 (1998).PubMedCrossRefGoogle Scholar
  19. 19.
    M. Shapiro-Shelef, K. I. Lin, L. J. McHeyzer-Williams, J. Liao, M. G. McHeyzer-Williams, K. Calame, Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells, Immunity 19(4), 607–620 (2003).PubMedCrossRefGoogle Scholar
  20. 20.
    A. L. Shaffer, M. Shapiro-Shelef, N. N. Iwakoshi, A. H. Lee, S. B. Qian, H. Zhao, X. Yu, L. Yang, B. K. Tan, A. Rosenwald, E. M. Hurt, E. Petroulakis, N. Sonenberg, J. W. Yewdell, K. Calame, L. H. Glimcher, L. M. Staudt, XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation, Immunity 21(1), 81–93 (2004).PubMedCrossRefGoogle Scholar
  21. 21.
    K. I. Lin, C. Angelin-Duclos, T. C. Kuo, K. Calame, Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells, Mol Cell Biol 22(13), 4771–4780 (2002).PubMedCrossRefGoogle Scholar
  22. 22.
    A. M. Reimold, P. D. Ponath, Y. S. Li, R. R. Hardy, C. S. David, J. L. Strominger, L. H. Glimcher, Transcription factor B cell lineage-specific activator protein regulates the gene for human X-box binding protein 1, J Exp Med 183(2), 393–401 (1996).PubMedCrossRefGoogle Scholar
  23. 23.
    C. Angelin-Duclos, G. Cattoretti, K. I. Lin, K. Calame, Commitment of B lymphocytes to a plasma cell fate is associated with Blimp-1 expression in vivo, J Immunol 165(10), 5462–5471 (2000).PubMedGoogle Scholar
  24. 24.
    G. Cattoretti, C. Angelin-Duclos, R. Shaknovich, H. Zhou, D. Wang, B. Alobeid, PRDM1/Blimp-1 is expressed in human B-lymphocytes committed to the plasma cell lineage, J Pathol 206(1), 76–86 (2005).PubMedCrossRefGoogle Scholar
  25. 25.
    A. Kallies, J. Hasbold, D. M. Tarlinton, W. Dietrich, L. M. Corcoran, P. D. Hodgkin, S. L. Nutt, Plasma cell ontogeny defined by quantitative changes in blimp-1 expression, J Exp Med 200(8), 967–977 (2004).PubMedCrossRefGoogle Scholar
  26. 26.
    D. J. Driver, L. J. McHeyzer-Williams, M. Cool, D. B. Stetson, M. G. McHeyzer-Williams, Development and maintenance of a B220- memory B cell compartment, J Immunol 167(3), 1393–1405 (2001).PubMedGoogle Scholar
  27. 27.
    C. Tunyaplin, M. A. Shapiro, K. L. Calame, Characterization of the B lymphocyte-induced maturation protein-1 (Blimp-1) gene, mRNA isoforms and basal promoter, Nucleic Acids Res 28(24), 4846–4855 (2000).PubMedCrossRefGoogle Scholar
  28. 28.
    K. Ozaki, R. Spolski, R. Ettinger, H. P. Kim, G. Wang, C. F. Qi, P. Hwu, D. J. Shaffer, S. Akilesh, D. C. Roopenian, H. C. Morse, 3rd, P. E. Lipsky, W. J. Leonard, Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6, J Immunol 173(9), 5361–5371 (2004).PubMedGoogle Scholar
  29. 29.
    R. Reljic, S. D. Wagner, L. J. Peakman, D. T. Fearon, Suppression of signal transducer and activator of transcription 3-dependent B lymphocyte terminal differentiation by BCL-6, J Exp Med 192(12), 1841–1848 (2000).PubMedCrossRefGoogle Scholar
  30. 30.
    F. H. Vasanwala, S. Kusam, L. M. Toney, A. L. Dent, Repression of AP-1 function: a mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene, J Immunol 169(4), 1922–1929 (2002).PubMedGoogle Scholar
  31. 31.
    C. Tunyaplin, A. L. Shaffer, C. D. Angelin-Duclos, X. Yu, L. M. Staudt, K. L. Calame, Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation, J Immunol 173(2), 1158–1165 (2004).PubMedGoogle Scholar
  32. 32.
    L. M. Corcoran, J. Hasbold, W. Dietrich, E. Hawkins, A. Kallies, S. L. Nutt, D. M. Tarlinton, P. Matthias, P. D. Hodgkin, Differential requirement for OBF-1 during antibody-secreting cell differentiation, J Exp Med 201(9), 1385–1396 (2005).PubMedCrossRefGoogle Scholar
  33. 33.
    A. L. Shaffer, K. I. Lin, T. C. Kuo, X. Yu, E. M. Hurt, A. Rosenwald, J. M. Giltnane, L. Yang, H. Zhao, K. Calame, L. M. Staudt, Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program, Immunity 17(1), 51–62 (2002).PubMedCrossRefGoogle Scholar
  34. 34.
    K. I. Lin, Y. Lin, K. Calame, Repression of c-myc is necessary but not sufficient for terminal differentiation of B lymphocytes in vitro, Mol Cell Biol 20(23), 8684–8695 (2000).PubMedCrossRefGoogle Scholar
  35. 35.
    P. Oppezzo, G. Dighiero, What do somatic hypermutation and class switch recombination teach us about chronic lymphocytic leukaemia pathogenesis? Curr Top Microbiol Immunol 294, 71–89 (2005).PubMedGoogle Scholar
  36. 36.
    H. Gonda, M. Sugai, Y. Nambu, T. Katakai, Y. Agata, K. J. Mori, Y. Yokota, A. Shimizu, The balance between Pax5 and Id2 activities is the key to AID gene expression, J Exp Med 198(9), 1427–1437 (2003).PubMedCrossRefGoogle Scholar
  37. 37.
    L. D. Erickson, B. G. Durell, L. A. Vogel, B. P. O’Connor, M. Cascalho, T. Yasui, H. Kikutani, R. J. Noelle, Short-circuiting long-lived humoral immunity by the heightened engagement of CD40, J Clin Invest 109(5), 613–620 (2002).PubMedCrossRefGoogle Scholar
  38. 38.
    M. K. Slifka, M. Matloubian, R. Ahmed, Bone marrow is a major site of long-term antibody production after acute viral infection, J Virol 69(3), 1895–1902 (1995).PubMedGoogle Scholar
  39. 39.
    R. A. Manz, M. Lohning, G. Cassese, A. Thiel, A. Radbruch, Survival of long-lived plasma cells is independent of antigen, Int Immunol 10(11), 1703–1711 (1998).PubMedCrossRefGoogle Scholar
  40. 40.
    R. A. Manz, A. Thiel, A. Radbruch, Lifetime of plasma cells in the bone marrow, Nature 388(6638), 133–134 (1997).PubMedCrossRefGoogle Scholar
  41. 41.
    K. Hayakawa, R. R. Hardy, D. R. Parks, L. A. Herzenberg, The “Ly-1 B” cell subpopulation in normal immunodefective, and autoimmune mice, J Exp Med 157(1), 202–218 (1983).PubMedCrossRefGoogle Scholar
  42. 42.
    I. Forster, K. Rajewsky, Expansion and functional activity of Ly-1+ B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice, Eur J Immunol 17(4), 521–528 (1987).PubMedCrossRefGoogle Scholar
  43. 43.
    N. A. Bos, C. G. Meeuwsen, B. S. Wostmann, J. R. Pleasants, R. Benner, The influence of exogenous antigenic stimulation on the specificity repertoire of background immunoglobulin-secreting cells of different isotypes, Cell Immunol 112(2), 371–380 (1988).PubMedCrossRefGoogle Scholar
  44. 44.
    K. Hayakawa, M. Asano, S. A. Shinton, M. Gui, D. Allman, C. L. Stewart, J. Silver, R. R. Hardy, Positive selection of natural autoreactive B cells, Science 285(5424), 113–116 (1999).PubMedCrossRefGoogle Scholar
  45. 45.
    P. X. Shaw, S. Horkko, M. K. Chang, L. K. Curtiss, W. Palinski, G. J. Silverman, J. L. Witztum, Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity, J Clin Invest 105(12), 1731–1740 (2000).PubMedGoogle Scholar
  46. 46.
    K. M. Haas, J. C. Poe, D. A. Steeber, T. F. Tedder, B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae, Immunity 23(1), 7–18 (2005).PubMedCrossRefGoogle Scholar
  47. 47.
    N. Baumgarth, O. C. Herman, G. C. Jager, L. Brown, L. A. Herzenberg, L. A. Herzenberg, Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system, Proc Natl Acad Sci U S A 96(5), 2250–2255 (1999).PubMedCrossRefGoogle Scholar
  48. 48.
    R. Berland, H. H. Wortis, Origins and functions of B-1 cells with notes on the role of CD5, Annu Rev Immunol 20, 253–300 (2002).PubMedCrossRefGoogle Scholar
  49. 49.
    K. R. Alugupalli, J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, R. M. Gerstein, B1b lymphocytes confer T cell-independent long-lasting immunity, Immunity 21(3), 379–390 (2004).PubMedCrossRefGoogle Scholar
  50. 50.
    T. Kawahara, H. Ohdan, G. Zhao, Y. G. Yang, M. Sykes, Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells, J Immunol 171(10), 5406–5414 (2003).PubMedGoogle Scholar
  51. 51.
    A. Itakura, M. Szczepanik, R. A. Campos, V. Paliwal, M. Majewska, H. Matsuda, K. Takatsu, P. W. Askenase, An hour after immunization peritoneal B-1 cells are activated to migrate to lymphoid organs where within 1 day they produce IgM antibodies that initiate elicitation of contact sensitivity, J Immunol 175(11), 7170–7178 (2005).PubMedGoogle Scholar
  52. 52.
    J. R. Tumang, R. Frances, S. G. Yeo, T. L. Rothstein, Spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors, J Immunol 174(6), 3173–3177 (2005).PubMedGoogle Scholar
  53. 53.
    N. Baumgarth, O. C. Herman, G. C. Jager, L. E. Brown, L. A. Herzenberg, J. Chen, B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection, J Exp Med 192(2), 271–280 (2000).PubMedCrossRefGoogle Scholar
  54. 54.
    R. Barrington, M. Zhang, M. Fischer, M. C. Carroll, The role of complement in inflammation and adaptive immunity, Immunol Rev 180, 5–15 (2001).PubMedCrossRefGoogle Scholar
  55. 55.
    A. F. Ochsenbein, T. Fehr, C. Lutz, M. Suter, F. Brombacher, H. Hengartner, R. M. Zinkernagel, Control of early viral and bacterial distribution and disease by natural antibodies, Science 286(5447), 2156–2159 (1999).PubMedCrossRefGoogle Scholar
  56. 56.
    H. P. Taylor, N. J. Dimmock, Mechanisms of neutralization of influenza virus by IgM, J Gen Virol 66 (Pt 4), 903–907 (1985).PubMedCrossRefGoogle Scholar
  57. 57.
    L. J. McHeyzer-Williams, M. G. McHeyzer-Williams, Antigen-specific memory B cell development, Annu Rev Immunol 23, 487–513 (2005).PubMedCrossRefGoogle Scholar
  58. 58.
    J. Bell, D. Gray, Antigen-capturing cells can masquerade as memory B cells, J Exp Med 197(10), 1233–1244 (2003).PubMedCrossRefGoogle Scholar
  59. 59.
    J. Choe, H. S. Kim, X. Zhang, R. J. Armitage, Y. S. Choi, Cellular and molecular factors that regulate the differentiation and apoptosis of germinal center B cells. Anti-Ig down-regulates Fas expression of CD40 ligand-stimulated germinal center B cells and inhibits Fas-mediated apoptosis, J Immunol 157(3), 1006–1016 (1996).PubMedGoogle Scholar
  60. 60.
    J. Choe, Y. S. Choi, IL-10 interrupts memory B cell expansion in the germinal center by inducing differentiation into plasma cells, Eur J Immunol 28(2), 508–515 (1998).PubMedCrossRefGoogle Scholar
  61. 61.
    X. Xia, H. K. Lee, S. C. Clark, Y. S. Choi, Recombinant interleukin (IL) 2-induced human B cell differentiation is mediated by autocrine IL6, Eur J Immunol 19(12), 2275–2281 (1989).PubMedCrossRefGoogle Scholar
  62. 62.
    J. Choe, H. S. Kim, R. J. Armitage, Y. S. Choi, The functional role of B cell antigen receptor stimulation and IL-4 in the generation of human memory B cells from germinal center B cells, J Immunol 159(8), 3757–3766 (1997).PubMedGoogle Scholar
  63. 63.
    S. G. Tangye, D. T. Avery, E. K. Deenick, P. D. Hodgkin, Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses, J Immunol 170(2), 686–694 (2003).PubMedGoogle Scholar
  64. 64.
    U. Klein, Y. Tu, G. A. Stolovitzky, J. L. Keller, J. Haddad, Jr., V. Miljkovic, G. Cattoretti, A. Califano, R. Dalla-Favera, Gene expression dynamics during germinal center transit in B cells, Ann N Y Acad Sci 987, 166–172 (2003).PubMedGoogle Scholar
  65. 65.
    J. D. Pound, J. Gordon, Maintenance of human germinal center B cells in vitro, Blood 89(3), 919–928 (1997).PubMedGoogle Scholar
  66. 66.
    L. Li, D. Young, S. F. Wolf, Y. S. Choi, Interleukin-12 stimulates B cell growth by inducing IFN-gamma, Cell Immunol 168(2), 133–140 (1996).PubMedCrossRefGoogle Scholar
  67. 67.
    J. Banchereau, F. Briere, Y. J. Liu, F. Rousset, Molecular control of B lymphocyte growth and differentiation, Stem Cells 12(3), 278–288 (1994).PubMedCrossRefGoogle Scholar
  68. 68.
    G. Bain, I. Engel, E. C. Robanus Maandag, H. P. te Riele, J. R. Voland, L. L. Sharp, J. Chun, B. Huey, D. Pinkel, C. Murre, E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas, Mol Cell Biol 17(8), 4782–4791 (1997).PubMedGoogle Scholar
  69. 69.
    G. Bain, W. J. Romanow, K. Albers, W. L. Havran, C. Murre, Positive and negative regulation of V(D)J recombination by the E2A proteins, J Exp Med 189(2), 289–300 (1999).PubMedCrossRefGoogle Scholar
  70. 70.
    O. Williams, H. J. Brady, The role of molecules that mediate apoptosis in T-cell selection, Trends Immunol 22(2), 107–111 (2001).PubMedCrossRefGoogle Scholar
  71. 71.
    R. R. Rivera, C. P. Johns, J. Quan, R. S. Johnson, C. Murre, Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3, Immunity 12(1), 17–26 (2000).PubMedCrossRefGoogle Scholar
  72. 72.
    B. Combadiere, C. Reis e Sousa, C. Trageser, L. X. Zheng, C. R. Kim, M. J. Lenardo, Differential TCR signaling regulates apoptosis and immunopathology during antigen responses in vivo, Immunity 9(3), 305–313 (1998).PubMedCrossRefGoogle Scholar
  73. 73.
    F. Powrie, R. Correa-Oliveira, S. Mauze, R. L. Coffman, Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity, J Exp Med 179(2), 589–600 (1994).PubMedCrossRefGoogle Scholar
  74. 74.
    D. Kontoyiannis, M. Pasparakis, T. T. Pizarro, F. Cominelli, G. Kollias, Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies, Immunity 10(3), 387–398 (1999).PubMedCrossRefGoogle Scholar
  75. 75.
    S. Wirtz, S. Finotto, S. Kanzler, A. W. Lohse, M. Blessing, H. A. Lehr, P. R. Galle, M. F. Neurath, Cutting edge: chronic intestinal inflammation in STAT-4 transgenic mice: characterization of disease and adoptive transfer by TNF- plus IFN-gamma-producing CD4+ T cells that respond to bacterial antigens, J Immunol 162(4), 1884–1888 (1999).PubMedGoogle Scholar
  76. 76.
    G. A. Hollander, S. J. Simpson, E. Mizoguchi, A. Nichogiannopoulou, J. She, J. C. Gutierrez-Ramos, A. K. Bhan, S. J. Burakoff, B. Wang, C. Terhorst, Severe colitis in mice with aberrant thymic selection, Immunity 3(1), 27–38 (1995).PubMedCrossRefGoogle Scholar
  77. 77.
    F. Powrie, Immune regulation in the intestine: a balancing act between effector and regulatory T cell responses, Ann N Y Acad Sci 1029, 132–141 (2004).PubMedCrossRefGoogle Scholar
  78. 78.
    G. Bouma, W. Strober, The immunological and genetic basis of inflammatory bowel disease, Nat Rev Immunol 3(7), 521–533 (2003).PubMedCrossRefGoogle Scholar
  79. 79.
    S. Huber, C. Schramm, H. A. Lehr, A. Mann, S. Schmitt, C. Becker, M. Protschka, P. R. Galle, M. F. Neurath, M. Blessing, Cutting edge: TGF-beta signaling is required for the in vivo expansion and immunosuppressive capacity of regulatory CD4+CD25+ T cells, J Immunol 173(11), 6526–6531 (2004).PubMedGoogle Scholar
  80. 80.
    L. Fahlen, S. Read, L. Gorelik, S. D. Hurst, R. L. Coffman, R. A. Flavell, F. Powrie, T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells, J Exp Med 201(5), 737–746 (2005).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • David Savitsky
    • 1
  • Luisa Cimmino
    • 2
  • Tracy Kuo
    • 3
  • Gislâine A. Martins
    • 4
  • Kathryn Calame
    • 4
  1. 1.Department of Biological SciencesColumbia University College of Physicians and SurgeonsNew YorkUSA
  2. 2.Institute of Human NutritionColumbia University College of Physicians and SurgeonsNew YorkUSA
  3. 3.Departments of Microbiology and Biochemistry & Molecular BiophysicsColumbia University College of Physicians and SurgeonsNew YorkUSA
  4. 4.Departments of MicrobiologyColumbia University College of Physicians and SurgeonsNew YorkUSA

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