Immunologic Research

, Volume 15, Issue 3, pp 246–257 | Cite as

Fas expression and apoptosis in human B cells

  • Elaine Schattner
  • Steven M. Friedman


Mechanisms of B cell apoptosis are critical in reducing aberrant B cell proliferations such as those that arise in autoimmune disease and in B cell malignancies. The physiologic interaction of CD4+ helper T cells and B lymphocytes has been extensively studied over the past two decades. Although CD4+ T cells are considered primarily to offer positive costimulatory signals for B cell differentiation into active immunoglobulin-secreting cells, recent studies have shown that CD4+ T cells are crucial in downregulating the humoral immune response. In the course of cognate interaction between CD40 ligand (CD40L)-bearing CD4+ T cells and CD40-expressing germinal center B cells, CD40 ligation results in augmented Fas expression at the B cell surface. Like CD40L, Fas ligand is expressed on activated CD4+ Th1 cells and when bound to Fas receptor on the B cell surface, initiates an apoptotic signal in that cell. Thus, CD4+ T cells limit the growth of autologous germinal center B cells by first inducing Fas expression and then instigating a death signal via Fas ligand. In this work, we will consider these observations about CD4+ T-cell-induced, Fas-mediated B cell death in the context of other factors that affect apoptosis in B cells, normal and malignant.

Key Words

B cells Apoptosis Fas/Fas L Lymphoma CD40/CD40L 


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  1. 1.
    Trauth BC, Klas C, Peters AM, Matzku S, Moller P, Falk W, Debatin KM, Krammer PH: Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989;245:301–305.PubMedCrossRefGoogle Scholar
  2. 2.
    Yonchara S, Ishii A, Yonehara M: A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med 1989;169:1747–1756.CrossRefGoogle Scholar
  3. 3.
    Oehm A, Behrmann I, Falk W, Pawlita M, Maier G, Klas C, Li-Weber M, Richards S, Dhein J, Trauth BC, Ponsting H, Krammer PH: Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. J Biol Chem 1992;267: 10709–10715.PubMedGoogle Scholar
  4. 4.
    Itoh N, Yonehara S, Ishii A, Yonehara M, Mizushima S, Sameshima M, Hase A, Seto Y, Nagata S: The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991; 66:233–243.PubMedCrossRefGoogle Scholar
  5. 5.
    Schulze-Osthoff K: The Fas/APO-1 receptor and its deadly ligand. Trends Cell Biol 1994;4:421–426.PubMedCrossRefGoogle Scholar
  6. 6.
    Inazawa J, Itoh N, Abe T, Nagata S: Assignment of the human Fas antigen gene (Fas) to 10q24.1. Genomics 1992;14:821–822.PubMedCrossRefGoogle Scholar
  7. 7.
    Lichter P, Walczak H, Weitz S, Behrmann I, Krammer PH: The human APO-1 (APT) antigen maps to 10q23, a region that is syntenic with mouse chromosome 19. Genomics 1992;14:179–180.PubMedCrossRefGoogle Scholar
  8. 8.
    White, K, Grether ME, Abrams JM, Young L, Farrell K, Steller H: Genetic control of programmed cell death in Drosophila. Science 1994; 264:677–683.PubMedCrossRefGoogle Scholar
  9. 9.
    Steller H: Mechanisms and genes of cellular suicide. Science 1995;267: 1445–1449.PubMedCrossRefGoogle Scholar
  10. 10.
    Golstein P, Marguet D, Depraetere V: Homology between reaper and the cell death domains of Fas and TNFR1. Cell 1995;81:185–186.PubMedCrossRefGoogle Scholar
  11. 11.
    Chinnaiyan AM, O'Rourke K, Tewari M, Dixit VM: FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 1995;81:505–512.PubMedCrossRefGoogle Scholar
  12. 12.
    Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC: Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994; 371:346–347.PubMedCrossRefGoogle Scholar
  13. 13.
    Enari M, Hug H, Nagata S: Involvement of an ICE-like protease in Fasmediated apoptosis. Nature 1995; 375:78–81.PubMedCrossRefGoogle Scholar
  14. 14.
    Los M, Van de Craen M, Penning LC, Schenk H, Westendorp M, Baeuerle PA, Droge W, Krammer PH, Fiers W, Schulze-Osthoff K: Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 1995;375:81–83.PubMedCrossRefGoogle Scholar
  15. 15.
    Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen SS, Dixit VM: Yama/CPP32 beta, a mammalian homolog of CED-3, is acrm A-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995;81:801–809.PubMedCrossRefGoogle Scholar
  16. 16.
    Duan H, Chinnaiyan AM, Hudson PL, Wing JP, He W-W, Dixit VM: ICE-LAP3, a novel mammalian homologue of theCaenorhabditis elegans cell death protein CED 3 is activated during Fas- and tumor necrosis factor-induced apoptosis. J Biol Chem 1996;271:1621–1625.PubMedCrossRefGoogle Scholar
  17. 17.
    Schlegel J, Peters I, Orrenius S, Miller DK, Thornberry NA, Yamin TT, Nicholson DW: CPP 32/apopain is a key interleukin 1 beta converting enzyme-like protease involved in Fasmediated apoptosis J Biol Chem 1996;271:1841–1844.PubMedCrossRefGoogle Scholar
  18. 18.
    Tewari M, Dixit VM: Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxviruscrm A gene Product. J Biol Chem 1995; 270:3255–3260.PubMedCrossRefGoogle Scholar
  19. 19.
    Bump NJ, Hackett M, Hugunin M, Seshagiri S, Brady K, Chen P, Ferenz C, Franklin S, Ghayur T, Li P, Licari P, Mankovich J, Shi L, Greenberg, AH, Miller LK, Wong WW: Inhibition of ICE family proteases by baculovrius antiapoptotic protein p35. Science 1995;269:1885–1888.PubMedCrossRefGoogle Scholar
  20. 20.
    Beldler DR, Tewari M, Friesen PD, Poirier G, Dixit VM: The baculovirus p35 protein inhibits Fas- and tumor necrosis factor-induced apoptosis. J Biol Chem 1995;270:16526–16528.CrossRefGoogle Scholar
  21. 21.
    Suda T, Takahashi T, Golstein P, Nagata S: Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 1993;75:1169–1178.PubMedCrossRefGoogle Scholar
  22. 22.
    Takahashi T, Tanaka M, Inazawa J, Abe T, Suda T, Nagata S: Human Fas ligand: Gene structure, chromosomal location and species specificity. Int Immunol 1994;6:1567–1574.PubMedCrossRefGoogle Scholar
  23. 23.
    Sidman CL, Marshall JD, von Boehmer H: Transgenic T cell receptor interactions in the lymphoproliferative and autoimmune syndromes ofIpr andgld mutant mice. Eur J Immunol 1992;22:499–504.PubMedCrossRefGoogle Scholar
  24. 24.
    Rouvier E, Luciani MF, Golstein P: Fas involvement in Ca2+-independent T cell-mediated cytotoxicity. J Exp Med 1993;177:195–200.PubMedCrossRefGoogle Scholar
  25. 25.
    Hanabuchi S, Koyanagi M, Kawasaki A, Shinohara N, Matsuzawa A, Nishimura Y, Kobayashi Y, Yonehara S, Yagita H, Okumura K: Fas and its ligand in a general mechanism of T cell-mediated cytotoxicity. Proc Natl Acad Sci USA 1994; 91:4930–4934.PubMedCrossRefGoogle Scholar
  26. 26.
    Dhein J, Walczak H, Baumler C, Debatin K-M, Krammer PH: Autocrine T cell suicide mediated by APO-1/(Fas/CD95). Nature 1995; 373:438–441.PubMedCrossRefGoogle Scholar
  27. 27.
    Brunner T, Mogil RJ, LaFace D, Yoo NJ, Mahboubl A, Echeverri F, Martin SJ, Force WR, Lynch DH, Ware CF, Green DR: Cell-autonomous Fac (CD95)/Fas ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 1995;373:441–444.PubMedCrossRefGoogle Scholar
  28. 28.
    Ju S-T, Panka DJ, Cul H, Ettinger R, El-Khatib M, Sherr DH, Stanger BZ, Marshak-Rothstein A: Fas (CD95)/FasL interactions required for programmed cell death after T cell activation. Nature 1995;373: 444–448.PubMedCrossRefGoogle Scholar
  29. 29.
    Alderson MR, Tough TW, Davis-Smith T, Braddy S, Falk B, Schooley KA, Goodwin RG, Smith CA, Ramsdell F, Lynch DH: Fas ligand mediates activation-induced cell death in human T lymphocytes. J Exp Med 1995;181:71–77.PubMedCrossRefGoogle Scholar
  30. 30.
    Takahashi T, Tanaka M, Brannan CI, Jenkins NA, Copeland NG, Suda T, Nagata S: Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 1994;76:969–976.PubMedCrossRefGoogle Scholar
  31. 31.
    Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S: Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 1992;356:314–317.PubMedCrossRefGoogle Scholar
  32. 32.
    Drappa J, Brot N, Elkon KB: The Fas protein is expressed at high levels on CD4+CD8+ thymocytes and activated mature lymphocytes in normal mice but not in the lupus prone strain, MRL/lpr. Proc Natl Acad Sci USA 1993;90:10340–10344.PubMedCrossRefGoogle Scholar
  33. 33.
    Rieux-Laucat F, Le Deist F, Hivroz C, Roberts IA, Debatin KM, Fischer A, de Villartay JP: Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995;2685:1347–1349.CrossRefGoogle Scholar
  34. 34.
    Fisher GH, Rosenberg FJ, Straus SE, Dale JK, Middelton LA, Lin AY, Strober W, Lenardo MJ, Puck JM: Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 1995;81:935–946.PubMedCrossRefGoogle Scholar
  35. 35.
    Drappa J, Vaishnaw AK, Sullivan K, Chu J-L, Elkon KB: The Canale Smith syndrome: An inherited autoimmune disorder associated with defective lymphocyte apoptosis and mutations in the Fas gene, submitted.Google Scholar
  36. 36.
    Meller P, Henne C, Leithauser F, Eichelmann A, Schmidt A, Brüderlein S, Dhein J, Krammer, P: Coregulation of the APO-1 antigen with intercellular adhesion molecule-1 (CD54) in tonsillar B cells and coordinate expression in follicular center B cells and in follicular center and mediastinal B cell lymphomas. Blood 1993;81:2067–2075.Google Scholar
  37. 37.
    Falk MH, Trauth BC, Debatin K-M, Klas C, Gregory CD, Rickinson AB, Calender A, Lenoir GM, Ellwart JW, Krammer PH, Bornkamm GW: Expression of the APO-1 antigen in Burkitt lymphoma cell lines correlates with a shift towards a lymphoblastoid phenotype. Blood 1992;79:3300–3306.PubMedGoogle Scholar
  38. 38.
    Mapara MY, Bargou R, Zugck C, Dohner H, Ustaoglu F, Jonker RR, Krammer PH, Dorken B: APO-1 mediated apoptosis or proliferation in human chronic B lymphocytic leukemia: Correlation withbcl-2 oncogene expression. Eur J Immunol 1993;23:702–708.PubMedCrossRefGoogle Scholar
  39. 39.
    Daniel PT, Krammer PH: Activation induces sensitivity toward APO-1 (CD95)-mediated apoptosis in human B cells. J Immunol 1994; 152:5624–5632.PubMedGoogle Scholar
  40. 40.
    Rathmell JC, Cooke MP, Ho WY, Grein J, Townsend SE, Davis MM, Goodnow CC: CD95 (Fas)-dependent climination of self-reactive B cells upon interaction with CD4+T cells. Nature 1995;376:181–184.PubMedCrossRefGoogle Scholar
  41. 41.
    Rothstein TL, Wang JK, Panka DJ, Foote LC, Wang Z, Stanger B, Cui H, Ju S-T, Marshak-Rothstein A: Protection against Fas-dependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature 1995;374:163–165.PubMedCrossRefGoogle Scholar
  42. 42.
    Schattner E, Elkon KB, Yoo D-H, Tumang J, Krammer PH, Crow MK, Friedman SM: CD40 ligation induces Apo-1/Fas expression on human B lymphocytes and facilitates apoptosis through the Apo-1/Fas pathway. J Exp Med 1995;182:1557–1575.PubMedCrossRefGoogle Scholar
  43. 43.
    Garrone P, Neidhardt E-M, Garcia E, Galibert L, van Kooten C, Banchereau J: Fas ligation induces apoptosis of CD40-activated human B lymphocytes. J Exp Med 1995; 182:1265–1273.PubMedCrossRefGoogle Scholar
  44. 44.
    Tumang JR, Posnett DN, Cole BC, Crow MK, Friedman SM: Helper T cell-dependent human B cell differentiation mediated by a mycoplasmal superantigen bridge. J Exp Med 1990;171:2153–2158.PubMedCrossRefGoogle Scholar
  45. 45.
    Friedman SM, Tumang JR, Crow MK: Microbial superantigens as etiopathogenic agents in autoimmunity. Rheum Dis Clin North Am 1993;19:207–222.PubMedGoogle Scholar
  46. 46.
    Schattner E, Yoo D-H, Crow MK, Friedman S: Superantigen-dependent Th-B cell interaction: A model for Th cell-mediated activation and apoptosis of B cells; in Zouali M (ed). Human B-Cell Superantigens. Landes, Bioscience Publishers, 1996, pp 209–221.Google Scholar
  47. 47.
    Gregory CD, Tursz T, Edwards CF, Tetaud C, Talbot M, Caillou B, Rickinson AB, Lipinski M: Identification of a subset of normal B cells with a Burkitt's lymphoma (BL)-like phenotype. J Immunol 1987;139:313–318.PubMedGoogle Scholar
  48. 48.
    Klein G: Epstein-Barr virus strategy in normal and neoplastic B cells. Cell 1994;77:791–793.PubMedCrossRefGoogle Scholar
  49. 49.
    Yellin MJ, Lee JJ, Chess L, Lederman S: A human CD4T cell leukemia subclone with contact-dependent helper function. J Immunol 1991;147:3389–3395.PubMedGoogle Scholar
  50. 50.
    Schattner E, Mascarenhas J, Bishop J, Yoo D-H, Chadburn A, Crow M, Friedman S: CD4+T cell induction of Fas-mediated apoptosis in Burkitt's lymphoma B cells. Blood 1996;88:1375–1382.PubMedGoogle Scholar
  51. 51.
    Stamenkovic I, Clark EA, Seed B: A B-lymphocyte activation molecule related to the nerve growth factor receptor and induced by cytokines in carcinomas. EMBO J 1989;8:1403–1410.PubMedGoogle Scholar
  52. 52.
    Lederman S, Yellin MJ, Krichevsky A, Belko J, Lee JJ, Chess L: Identification of a novel surface protein on activated CD4+T cells that induces contact-dependent B cell differentiation (help). J Exp Med 1992;175:1091–1101.PubMedCrossRefGoogle Scholar
  53. 53.
    Liu Y-J, Joshua DE, Williams GT, Smith CA, Gordon J, MacLennan ICM: Mechanism of antigen-driven selection in germinal centers. Nature 1989;342:929–931.PubMedCrossRefGoogle Scholar
  54. 54.
    Banchereau J, Bazan F, Blanchard D, Briere F, Galizzi JP, van Kooten C, Liu YJ, Rousset F, Saeland S: The CD40 antigen and its ligand. Annu Rev Immunol 1994;12:881–922.PubMedCrossRefGoogle Scholar
  55. 55.
    Galibert L, Burdin N, de Saint-Vis B, Garrone P, van Kooten C, Banchereau J, Rousset F: CD40 and B cell antigen receptor dual triggering of resting B lymphocytes turns on a partial germinal center phenotype. J Exp Med 1996;183:77–85.PubMedCrossRefGoogle Scholar
  56. 56.
    Lagresle C, Bella C, Daniel PT, Krammer PH, Defrande T: Regulation of germinal center B cell differentiation: Role of the human APO-1/Fas (CD95) molecule. J Immunol 1995;154:5746–5756.PubMedGoogle Scholar
  57. 57.
    Cleary AM, Fortune SM, Yellin MJ, Chess L, Lederman S: Opposing roles of CD95 (Fas/APO-1) and CD40 in the death and rescue of human low density tonsillar B cells. J Immunol 1995;155:3329–3337.PubMedGoogle Scholar
  58. 58.
    Owen-Schaub LB, Yonehara S, Crump WL III, Grimm EA: DNA fragmentation and cell death is selectively triggered in activated human lymphocytes by Fas antigen engagement. Cellular Immunol 1992; 140:197–205.CrossRefGoogle Scholar
  59. 59.
    Miyawaki T, Uehara T, Nibu R, Tsuji T, Yachie A, Yonehara S, Taniguchi N: Differential expression of apoptosis-related Fas antigen on lymphocyte subpopulations in human peripheral blood. J Immunol 1992;149:3753–3758.PubMedGoogle Scholar
  60. 60.
    Fisher DE: Apoptosis in cancer therapy: Crossing the threshold. Cell 1994;78:539–542.PubMedCrossRefGoogle Scholar
  61. 61.
    Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC, Grogan TM, Isaacson PG, Knowles DM, Mason DY, Muller-Hermelink H-K, Pileri SA, Piris MA, Ralfkiaer E, Warnke RA: A revised European-American classification of lymphoid neoplasms: A proposal from the International Lymphoma Study Group. Blood 1994;84:1361–1392.PubMedGoogle Scholar
  62. 62.
    Cherney BW, Bhatia K, Tosato G: A role for deregulatedc-myc expression in apoptosis of Epstein-Barr virus-immortalized B cells. Proc Natl Acad Sci USA 1994;91:12967–12971.PubMedCrossRefGoogle Scholar
  63. 63.
    Onel KB, Tucek-Szabo CL, Ashany D, Lacy E, Nikolic-Zugic J, Elkon KB: Expression and function of the murine CD95/FasR/APO-1 receptor in relation to B cell ontogeny. Eur J Immunol 1995;25:2940–2947.PubMedCrossRefGoogle Scholar
  64. 64.
    Lin A, Dale J, Fleisher T, Fisher G, Rosenberg F, Lenardo M, Puck J, Middelton L, Corden B, Tucker M, Straus S: Familial aggregation of Hodgkin's disease (HD), autoimmune lymphoproliferative syndrome (ALPS) and germline Fas mutations. Blood 1995;86S:271a.Google Scholar
  65. 65.
    Sato T, Irie S, Kitada S, Reed JC: FAP-1: A protein tyrosine phosphatase that associated with Fas. Science 1995;268:411–415.PubMedCrossRefGoogle Scholar
  66. 66.
    Mosialos G, Birkenbach M, Yalamanchili R, Van Arsdale T, Ware C, Kieff E: The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 1995;80:389–399.PubMedCrossRefGoogle Scholar
  67. 67.
    Panayiotidis P, Ganeshaguru K, Foroni L, Hoffbrand AV: Expression and function of the FAS antigen in B chronic lymphocytic leukemia and hairy cell leukemia. Leukemia 1995;9:1227–1232.PubMedGoogle Scholar
  68. 68.
    Shima Y, Nishimoto N, Ogata A, Fujii Y, Yoshizaki K, Kishimoto T: Myeloma cells express Fas antigen/Apo-1 (CD95) but only some are sensitive to anti-Fas antibody resulting in apoptosis. Blood 1995;85:757–764.PubMedGoogle Scholar
  69. 69.
    Westendorf JJ, Lammert JM, Jelinek DF: Expression and function of Fas (APO-1/CD95) in patient myeloma cells and myeloma cell lines. Blood 1995;85:3566–3576.PubMedGoogle Scholar
  70. 70.
    Xerri L, Carbuccia N, Parc P, Hassoun J, Birg F: Frequent expression of FAS/APO-1 in Hodgkin's disease and anaplastic large cell lymphomas. Histopathology 1995;27:235–241.PubMedCrossRefGoogle Scholar
  71. 71.
    Korsemeyer SJ:bcl-2 initiates a new category of oncogenes: Regulators of cell death. Blood 1992;80:879–886.Google Scholar
  72. 72.
    Oltvai ZN, Milliman CL, Korsmeyer SJ:bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993;74:609–619.PubMedCrossRefGoogle Scholar
  73. 73.
    Oltvai ZN, Korsmeyer SJ: Check-points of dueling dimers foil death wishes. Cell 1994;79:189–192.PubMedCrossRefGoogle Scholar
  74. 74.
    Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB:bcl-x, abcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993;74:597–608.PubMedCrossRefGoogle Scholar
  75. 75.
    Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ: Bad, a heterodimeric partner forbcl-XL andbcl-2, displaces Bax and promotes cell death. Cell 1995;80:285–291.PubMedCrossRefGoogle Scholar
  76. 76.
    Itoh N, Tsujimoto Y, Nagata S: Effect ofbcl-2 on Fas antigen-mediated cell death. J Immunol 1993; 151:621–627.PubMedGoogle Scholar
  77. 77.
    Jaattela M, Benedict M, Tewari M, Shayman JA, Dixit VM:bcl-x andbcl-2 inhibit TNF and Fas-induced apoptosis and activation of phospholipase A2 in breast carcinoma cells. Oncogene 1995;10:2297–2305.PubMedGoogle Scholar
  78. 78.
    Weller M, Malipiero U, Aguzzi A, Reed JC, Fontana A: Protooncogenebcl-2 gene transfer abrogates Fas/APO-I antibody-mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J Clin Invest 1995;95:2633–2643.PubMedCrossRefGoogle Scholar
  79. 79.
    Strasser A, Harris AW, Huang DC, Krammer PH, Cory S:bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J 1995;14:6136–6147.PubMedGoogle Scholar
  80. 80.
    Memon SA, Moreno MB, Petrak D, Zacharchuk CM:bcl-2 blocks glucocorticoid-but not Fas- or activation-induced apoptosis in a T cell hybridoma. J Immunol 1995;155:4644–4652.PubMedGoogle Scholar
  81. 81.
    Lacronique V, Mignon A, Fabre M, Viollet B, Rouquet N, Moiina T, Porteu A, Henrion A, Bouscary D, Varlet P, Joulin V, Kahn A:bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 1996;2:80–86.PubMedCrossRefGoogle Scholar
  82. 82.
    Wang Z, Karras JG, Howard RG, Rothstein TL: Induction ofbcl-x by CD40 engagement rescues slg-induced apoptosis in murine B cells. J Immunol 1995;155:3722–3725.PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 1995

Authors and Affiliations

  • Elaine Schattner
    • 1
  • Steven M. Friedman
    • 2
  1. 1.Division of Hematology-Oncology, Department of MedicineThe New York HospitalNew YorkUSA
  2. 2.Division of Rheumatology, The Hospital for Special SurgeryCornell University Medical CollegeNew YorkUSA

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