Defective B cell receptor-mediated responses in mice lacking the Ets protein, Spi-B

EMBO Journal

Volumn 16, Issue 23, 1997, Pages 7118-7129

  Su, Gloria H ^a   Chen, Hui Min ^b   Muthusamy, Natarajan ^a   Garrett Sinha, Lee Ann ^a   Baunoch, David ^a   Tenen, Daniel G ^b   Simon, M Celeste ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

B cell antigen receptor; B lymphocytes; Ets factors; Gene targeting; Germinal centers

Indexed keywords

B LYMPHOCYTE ANTIGEN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2B; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPI B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BODY HEIGHT; CELL DEATH; CELL MATURATION; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CROSS LINKING; GENE LOCUS; GENE MUTATION; GENE TARGETING; GERMINAL CENTER; HEMATOPOIETIC CELL; HUMORAL IMMUNITY; IMMUNIZATION; LIFESPAN; LYMPHOCYTE; MONOCYTE; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE;

EID: 0030683640     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.23.7118     Document Type: Article

References (70)

1. Ahearn, J.M. et al. (1996) Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity, 4, 251-262.
2. Braun, T., Rudnicki, M.A., Aronold, H.-H. and Jaenisch, R. (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell, 71, 369-382.
3. Carter, R. and Fearon, D. (1992) CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science, 256, 105-107.
4. Castigli, E., Alt, F.W., Davidson, L., Bottaro, A., Mizoguchi, E., Bhan, A.K. and Geha, R.S. (1994) CD40-deficient mice generated by recombination-activating gene-2-deficient blastocyst complementation. Proc. Natl Acad. Sci. USA, 91, 12135-12139.
5. Chen, H.-M., Zhang, P., Voso, M., Hohaus, S., Gonzalez, D., Glass, C., Zhang, D.-E. and Tenen, D. (1995) Neutrophils and monocytes express high levels of PU.1 (Spi-1) but not Spi-B. Blood, 85, 2918-2928.
6. Cooke, M.P., Heath, A.W., Shokat, K.M., Zeng, Y., Finkelman, F.D., Linsley, P.S., Howard, M. and Goodnow, C.C. (1994) Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med., 179, 425-438.
7. Corcoran, L.M. and Karvelas, M. (1994) Oct-2 is required early in T cell-independent B cell activation for G1 progression and for proliferation. Immunity, 1, 635-645.
8. Crissman, H.A. and Steinkamp, J.A. (1973) Rapid simultaneous measurement of DNA, protein and cell volume in single cells from large mammalian cell populations. J. Cell Biol., 59, 766-771.
9. Dent, A.L., Shaffer, A.L., Yu, X., Allman, D. and Staudt, L.M. (1997) Control of inflammation, cytokine expression and germinal center formation by BCL-6. Science, 276, 589-592.
10. Eisenbeis, C., Singh, H. and Storb, U. (1993) PU.1 is a component of a multiprotein complex which binds an essential site in the murine immunoglobulin λ2-4 enhancer. Mol. Cell. Biol., 13, 6452-6461.
11. Feinman, R., Qiu, W.Q., Pearse, R.N., Nikolajczyk, B.S., Sen, R., Sheffery, M. and Ravetch, J.V. (1994) PU.1 and an HLH family member contribute to the myeloid-specific expression of the Fc-γRIIIA promoter. EMBO J., 13, 3852-3860.
12. Feldhaus, A.L., Mbangkollo, D., Arvin, K.L., Klug, C.A. and Singh, H. (1992) BLyF, a novel cell-type and stage-specific regulator of the B-lymphocyte gene mb-1. Mol. Cell. Biol., 12, 1126-1133.
13. Fischer, K.-D., Zmuldzinas, A., Gardner, S., Barbacid, M., Bernstein, A. and Guldos, C. (1995) Defective T-cell receptor signalling and positive selection of Vav-deficient CD4+CD8+ thymocytes. Nature, 374, 474-477.
14. Galson, D., Hensold, J., Bishop, T., Schalling, M., D'Andrea, A., Jones, C., Auron, P. and Houseman, D. (1993) Mouse β-globin DNA-binding protein B1 is identical to a proto-oncogene, the transcription factor Spi-1/Pu.1, and is restricted in expression to hematopoietic cells. Mol. Cell. Biol., 13, 2929-2941.
15. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
16. Grillot, D.A.M., Merino, R., Pena, J.C., Fanslow, W.C., Finkelman, F.D., Thompson, C.B. and Nunez, G. (1996) bcl-x regulated expression during B cell development and activation and modulates lymphocyte survival in transgenic mice. J. Exp. Med., 183, 381-391.
17. Hagman, J. and Grosschedl, R. (1992) An inhibitory carboxyl-terminal domain in Ets-1 and Ets-2 mediates differential binding of ETS family factors to promoter sequences of the mb-1 gene. Proc. Natl Acad. Sci. USA, 89, 8889-8893.
18. Hanks, M., Wurst, W., Anson-Cartwright, L., Auerback, A.B. and Joyner, A.L. (1995) Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science, 269, 679-682.
19. Heydemann, A., Juang, G., Hennessy, K., Parmacek, M.S. and Simon, M.C. (1996) The myeloid cell-specific c-fes promoter is regulated by Sp1, PU.1 and a novel transcription factor. Mol. Cell. Biol., 16, 1676-1686.
20. Hibbs, M.L., Tarlinton, D.M., Armes, J., Grail, D., Hodgson, G., Maglitto, R., Stacker, S.A. and Dunn, A.R. (1995) Multiple defects in the immune system of lyn-deficient mice, culminating in autoimmune disease. Cell, 83, 301-311.
21. Hromas, R., Orazi, A., Neiman, R., Maki, R., Van Beveran, C., Moore, J. and Klemsz, M. (1993) Hematopoietic lineage-and stage-restricted expression of the ETS oncogene family member PU.1. Blood, 82, 2998-3004.
22. Keller, G., Kennedy, M., Papayannopoulou, T. and Wiles, M. (1993) Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol., 13, 473-486.
23. Kim, U., Qin, X.-F., Gong, S., Stevens, S., Luo, Y., Nussenzweig, M. and Roeder, R.G. (1996) The B-cell-specific transcription coactivator OCA-B/OBF-1/Bob-1 is essential for normal production of immunoglobulin isotypes. Nature, 383, 542-547.
24. Klemsz, M., McKercher, S., Celada, A., Van Beveren, C. and Maki, R. (1990) The macrophage and B cell-specific transcription factor PU.1 is related to the Ets oncogene. Cell, 61, 113-124.
25. Kontgen, F., Grumont, R.J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D. and Gerondakis, S. (1995) Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity and interleukin-2 expression. Genes Dev., 9, 1965-1977.
26. Laux, G., Adam, B. and Moreau-Gachelin, F. (1994) The Spi-1/PU.1 and Spi-B ets family transcription factors and the recombination signal binding protein RBP-Jk interact with an Epstein-Barr virus nuclear antigen 2 responsive cis-element. EMBO J., 13, 5624-5632.
27. Lin, Y.H., Shin, E.J., Campbell, M.J. and Niederhuber, J.E. (1995) Transcription of the blk gene in human B lymphocytes is controlled by two promoters. J. Biol. Chem., 270, 25968-25975.
28. Matsumoto, M. et al. (1996) Affinity maturation without germinal centres in lymphotoxin-α-deficient mice. Nature, 382, 462-466.
29. McKercher, S.R. et al. (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J., 15, 5647-5658.
30. Moreau-Gachelin, F. (1994) Spi-1/PU.1: an oncogene of the Ets family. Biochem. Biophys. Acta, 1198, 149-163.
31. Moreau-Gachelin, F., Ray, D., Mattei, M., Tambourin, P. and Tavitian, A. (1989) The putative oncogene Spi-1: murine chromosomal localization and transcriptional activation in murine acute erythroleukemias. Oncogene, 4, 1449-1456.
32. Mortensen, R., Conner, D., Chao, S., Geisterfer-Lowrance, A. and Seidman, J. (1992) Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol., 12, 2391-2394.
33. Motoyama, N. et al. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science, 267, 1506-1510.
34. Moulton, K.S., Semple, K., Wu, H. and Glass, K.C. (1994) Cell-specific expression of the macrophage scavenger receptor gene is dependent on PU.1 and a composite AP-1/ets motif. Mol. Cell. Biol., 14, 4408-4418.
35. Muller, S., Sideras, P., Smith, C.I. and Xanthopoulos, K.G. (1997) Cell specific expression of human Bruton's agammaglobulinemia tyrosine kinase gene (Btk) is regulated by Sp1 and Spi-1/PU.1 family members. Oncogene, in press.
36. Muthusamy, N., Barton, K. and Leiden, J.M. (1995) Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature, 377, 639-642.
37. Nelsen, B., Tian, G., Erman, B., Gregoire, J., Maki, R., Graves, B. and Sen, R. (1993) Regulation of lymphoid-specific immunoglobulin m heavy chain gene enhancer by ETS-domain proteins. Science, 261, 82-86.
38. Olson, M., Scott, E.W., Hack, A., Su, G., Singh, H. and Simon, M.C. (1995) PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity, 3, 702-714.
39. Oltvai, Z.N., Milliman, C.L. and Korsmeyer, S.J. (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog. Bax, that accelerates programmed cell death. Cell, 74, 609-619.
40. Omori, S.A. and Wall, R. (1993) Multiple motifs regulate the B-cell-specific promoter of the B29 gene. Proc. Natl Acad. Sci. USA, 90, 11723-11727.
41. Pahl, H., Rosmarin, A. and Tenen, D. (1992) Characterization of the myeloid-specific CD11b promoter. Blood, 79, 865-870.
42. Pahl, H., Scheibe, R., Zang, D., Chen, H.-M., Galson, D., Maki, R. and Tenen, D. (1993) The proto-oncogene PU.1 regulates expression of the myeloid-specific CD11b promoter. J. Biol. Chem., 7, 5014-5020.
43. Perez, C., Coeffier, E., Moreau-Gachelin, F., Wietzerbin, J. and Benech, P. (1994) Involvement of the transcription factor PU.1/Spi-1 in myeloid cell-restricted expression of an interferon-inducible gene encoding the human high-affinity Fcγ receptor. Mol. Cell. Biol., 14, 5023-5031.
44. Pongubala, J., Nagulapalli, S., Klemsz, M., McKercher, S., Maki, R. and Atchison, M. (1992) PU.1 recruits a second nuclear factor to a site important for immunoglobulin kappa 3′ enhancer activity. Mol. Cell. Biol., 12, 368-378.
45. Rathmell, J.C., Cooke, M.P., Ho, W.Y., Grein, J., Townsend, S.E., Davis, M.M. and Goodnow, C.C. (1995) (Fas)-dependent elimination of self-reactive B cells upon interaction with CD4+ T cells. Nature, 376, 181-184.
46. Rathmell, J.C., Townsend, S.E., Xu, J.C., Flavell, R.A. and Goodnow, C.C. (1996) Expansion or elimination of B cells in vivo: Dual roles for CD40-and FAS (CD95)-ligands modulated by the B cell antigen receptor. Cell, 87, 319-329.
47. Ray, D., Bosselut, R., Ghysdael, J., Mattei, M., Tavitian, A. and Moreau-Gachelin, F. (1992) Characterization of Spi-B, a transcription factor related to the putative oncoprotein Spi-1/PU.1. Mol. Cell. Biol., 12, 4297-4304.
48. Ray-Gallet, D., Mao, C., Tavitian, A. and Moreau-Gachelin, F. (1995) DNA binding specificities of Spi-1/PU.1 and Spi-B transcription factors and identification of a Spi-1/Spi-B binding site in the c-fes/c-fps promoter. Oncogene, 11, 303-313.
49. Rosmarin, A., Levy, R. and Tenen, D. (1992) Cloning and analysis of the CD18 promoter. Blood, 79, 2598-2604.
50. Rudnicki, M., Braun, T., Hinuma, S. and Jaenisch, R. (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell, 71, 383-390.
51. Rudnicki, M.A., Schnegelsberg, P.N., Stead, R.H., Braun, T., Arnold, H. and Jaenisch, R. (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell, 75, 1351-1359.
52. Schubart, D.B., Rolink, A., Kosco-Vilbois, M.H., Botteri, F. and Matthias, P. (1996) B-cell-specific coactivator OBF-1/OCA-B/Bob1 required for immune response and germinal centre formation. Nature, 383, 538-542.
53. Schuetze, S., Stenberg, P. and Kabat, D. (1993) The ETS-related transcription factor PU.1 immoralizes erythroblasts. Mol. Cell. Biol., 13, 5670-5678.
54. Scott, E.W., Simon, M.C., Anastasi, J. and Singh, H. (1994) Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science, 265, 1573-1577.
55. Scott, E.W., Fisher, R., Olson, M., Simon, M.C. and Singh, H. (1997) PU.1 functions in a cell-autonomous manner to control the differentiation of multipotential lymphoid-myeloid progenitors. Immunity, 6, 437-447.
56. Sha, W.C., Liou, H.-C., Tuomanen, E.I. and Baltimore, D. (1995) Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell. 80, 321-330.
57. Shin, M. and Koshland, M. (1993) Ets-related protein PU.1 regulates expression of the immunoglobulin J-chain gene through a novel Ets-binding element. Genes Dev., 7, 2006-2015.
58. Sideras, P. et al. (1994) Genomic organization of mouse and human Bruton's agammaglobulinemia tyrosine kinase (Btk) loci. J. Immunol., 153, 5607-5617.
59. Smith, L.A., Gonzalez, D.A., Hohaus, S. and Tenen, D.G. (1994) The myeloid specific granulocyte colony stimulating factor (G-CSF) receptor promoter contains a functional site for the myeloid transcription factor PU.1 (Spi-1). Blood, 84, 372a.
60. Su, G.H., Ip, H.S., Cobb, B.S., Lu, M.-M., Chen, H.-M. and Simon, M.C. (1996) The Ets protein Spi-B is expressed exclusively in B cells and T cells during development. J. Exp. Med., 184, 203-214.
61. Swat, W., Dessing, M., von Boehmer, H. and Kisielow, P. (1993) CD69 expression during selection and maturation of CD4+8+ thymocytes. Eur. J. Immunol., 23, 739-746.
62. Tarakhovsky, A., Turner, M., Schaal, S., Mee, P.J., Duddy, L.P., Rajewsky, K. and Tybulewicz, V.L.J. (1995) Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav. Nature, 374, 467-470.
63. Testi, R., Phillips, J.H. and Lanier, L.L. (1989) Leu 23 induction as an early marker of functional CD3/T cell antigen receptor triggering. Requirement for receptor cross-linking, prolonged elevation of intracellular (Ca++) and stimulation of protein kinase C. J. Immunol., 142, 1854-1860.
64. Tybulewicz, V., Crawford, C., Jackson, P., Bronson, R. and Mulligan, R. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell, 65, 1153-1163.
65. Valentine, M.A., Czerrnik, A.J., Rachie, N., Hidaka, H., Fisher, C.L., Cambier, J.C. and Bomsztyk, K. (1995) Anti-immunoglobulin M activates nuclear calcium/calmodulin-dependent protein kinase II in human B lymphocytes. J. Exp. Med., 182, 1943-1949.
66. Veis, D.J., Sorenson, C.M., Shutter, J.R. and Korsmeyer, S.J. (1993) Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys and hypopigmented hair. Cell, 75, 229-240.
67. Wasylyk, B., Hahn, S. and Giovane, A. (1993) The Ets family of transcription factors. Eur. J. Biochem., 211, 7-18.
68. Xu, J., Foy, T.M., Laman, J.J.T.J.W., Elsemore, J., Noelle, R.J. and Flavell, R.A. (1994) Mice deficient for the CD40 ligand. Immunity, 1, 423-431.
69. Zhang, D.-E., Hetherington, C., Chen, J.-M. and Tene, D. (1994) The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol., 14, 373-381.
70. Zhang, R., Alt, F.W., Davidson, L., Orkin, S.H. and Swat, W. (1995) Defective signalling through the T-and B-cell antigen receptors in lymphoid cells lacking the vav proto-oncogene. Nature, 374, 470-473.