Identification of Bach2 as a B-cell-specific partner for small Maf proteins that negatively regulate the immunoglobulin heavy chain gene 3' enhancer

EMBO Journal

Volumn 17, Issue 19, 1998, Pages 5734-5743

  Muto, Akihiko ^a,b   Hoshino, Hideto ^a,b   Madisen, Linda ^c   Yanai, Nobuaki ^d   Obinata, Masuo ^d   Karasuyama, Hajime ^e   Hayashi, Norio ^a   Nakauchi, Hiromitsu ^b   Yamamoto, Masayuki ^b   Groudine, Mark ^c   Igarashi, Kazuhiko ^a  

^a TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c USA   (United States)

^d TOHOKU UNIVERSITY   (Japan)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

B cell; Immunoglobulin; Maf; Transcription factor

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; RETINOID X RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CONTROLLED STUDY; ENHANCER REGION; HEMATOPOIETIC CELL; IMMUNOGLOBULIN GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRESSOR GENE;

B-LYMPHOCYTES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION; GENES, IMMUNOGLOBULIN; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN HEAVY CHAINS; LEUCINE ZIPPERS; MAFK TRANSCRIPTION FACTOR; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MAF; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0032189224     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.19.5734     Document Type: Article

References (68)

1. Albagli, O., Dhordain, P., Deweindt, C., Lecocq, G. and Leprince, D. (1995) The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ., 6, 1193-1198.
2. Alt, F., Rosenberg, N., Lewis, S., Thomas, E. and Baltimore, D. (1981) Organization and reorganization of immunoglobulin genes in A-MuLV-transformed cells: rearrengement of heavy but not light chain genes. Cell, 27, 381-390.
3. Amati, B. and Land, H. (1994) Myc-Max-Mad: a transcnption factor network controlling cell cycleprogression, differentiation and death. Curr. Opin. Genet. Dev., 4, 102-108.
4. Andrews, N.C. and Faller, D.V. (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cellls. Nucleic Acids Res., 19, 2499.
5. Andrews, N.C., Erdjument-Bromage, H., Davidson, M.B., Tempst, P. and Orkin, S.H. (1993a) Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature, 362, 772-728.
6. Andrews, N.C., Kotkow, K.J., Ney, P.A., Erdjument-Bromage, H., Tempst, P. and Orkin, S.H. (1993b) The ubiquitous subunit of erythroid transcription factor NF-E2 is a small basic-leucine zipper protein related to the v-maf oncogene. Proc. Natl Acad. Sci. USA, 90, 11488-11492.
7. Arulampalam, V., Eckhardt, L. and Pettersson, S. (1997) The enhancer shift: a model to explain the developmental control of IgH gene expression in B-lineage cells. Immunol. Today, 18, 549-554.
8. Barberis, A., Widenhorn, K., Vitelli, L. and Busslinger, M. (1990) A novel B-cell lineage-specific transcription factor present at early but not late stage of differentiation. Genes Dev., 4, 849-859.
9. Blank, V. and Andrews, N.C. (1997) The Maf transcription factors: regulators of differentiation. Trends Biochem. Sci., 22, 437-441.
10. Blank, V., Kim, M.J. and Andrews, N.C. (1997) Human MafG is a functional partner for p45 NF-E2 in activating globin gene expression. Blood, 89, 3925-3935.
11. Carmen, A.A., Rundlett, S.E. and Grunstein, M. (1996) HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex. J. Biol. Chem., 271, 15837-15844.
12. Caterina, J.J., Donze, D., Sun, C.W., Ciavatta, D.J. and Towns, T.M. (1994) Cloning and functional characterization of LCK-F1: a bZIP transcription factor that activates erythroid-specific, human globin gene expression. Nucleic Acids Res., 12, 2383-2391.
13. Chan, J.Y., Han, X.-L. and Kan, Y.W. (1993) Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl Acad. Sci. USA, 90, 11371-11375.
14. Chauveau, C. and Cogne, M. (1996) Palindromic structure of the IgH 3′ locus control region. Nature Genet., 14, 15-16.
15. Chen, Z., Brand, N.J., Chen, A., Chen, S.J., Tong, J.H., Wang, Z.Y., Waxman, S., and Zelent, A. (1993) Fusion between a novel Kruppel-like zinc finger gene and the retinoic acid receptor-α locus due to a variant t(11;17) translocation associated with acute promyelocytic leukemia. EMBO J., 12, 1161-1167.
16. Dhordain, P., Albagli, O., Lin, R.J., Ansieau, S., Quief, S., Leutz, A., Kerckaert, J., Evans, R.M. and Leprince, D. (1997) Corepressor SMRT binds the BTB/POZ repressing domain of the LAZ3/BCL6 oncoprotein. Proc. Natl Acad. Sci. USA, 94, 10762-10767.
17. Engel, J.D. (1994) Meticulous AP-1 factors. Nature, 367, 516-517.
18. Fitzsimmons, D. and Hagman, J. (1996) Regulation of gene expression at early stages of B-cell and T-cell differentiation. Curr. Opin. Immunol., 8, 166-174.
19. Fujiwara, K.T., Kataoka, K. and Nishizawa, M. (1993) Two new members of the maf oncogene family, mafK and mafF, encode nuclear b-Zip proteins lacking putative trans-activator domain. Oncogene, 8, 2371-2380.
20. Georgopoulos, K. (1997) Transcription factors required for lymphoid lineage commitment. Curr. Opin. Immunol., 9, 222-227.
21. Grant, P.A., Thompson, C.B. and Petterson, S. (1995) IgM receptor-mediated transactivation of the IgH 3′ enhancer couples a novel Elf-1-AP-1 protein complex to the developmental control of enhancer function. EMBO J., 14, 4501-4513.
22. Grignani, F. et al. (1998) Fusion proteins of the retinoic acid receptor-a recruit histone deacetylase in promyelocytic leukemia. Nature, 391, 815-818.
23. Hagman, J., Belanger, C., Travis, A., Truck, C.W. and Grosscheld, R. (1993) Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev., 7, 760-773.
24. Hardy, R.R., Dangl, J.L., Hayakawa, K., Jager, G., Herzenberg, L.A. and Herzenberg, L.A. (1986) Frequent 1 light chain gene rearrangement and expression in a Ly-1 B lymphoma with a productive κ chain allele. Proc. Natl Acad. Sci. USA, 83, 1438-1442.
25. Hardy, R.R., Carmack, C.E., Shinton, S.A., Kemp, J.D. and Hayakawa, K. (1991) Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med., 173, 1213-1225.
26. Ho, I.-C., Hodge, M.R., Rooney, J.W. and Glimcher, L.H. (1996) The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell, 85, 973-983.
27. Hu, M., Krause, D., Greaves, M., Sharkis, S., Dexter, M., Heyworth, C. and Enver, T. (1997) Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev., 11, 774-785.
28. Igarashi, K., Kataoka, K., Itoh, K., Hayashi, N., Nishizawa, M. and Yamamoto, M. (1994) Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature, 367, 568-572.
29. Igarashi, K., Itoh, K., Hayashi, N., Nishizawa, M. and Yamamoto, M. (1995a) Conditional expression of the ubiquitous transcription factor MafK induces erythroleukemia cell differentiation. Proc. Natl Acad. Sci. USA, 92, 7445-7449.
30. Igarashi, K., Itoh, K., Motohashi, H., Hayashi, N., Matuzaki, Y., Nakauchi, H., Nishizawa, M. and Yamamoto, M. (1995b) Activity and expression of murine small Maf family protein MafK. J. Biol. Chem., 270, 7615-7624.
31. Igarashi, K., Hoshino, H., Muto, A., Suwabe, N., Nishikawa, S., Nakauchi, H. and Yamamoto, M. (1998) Multivalent DNA binding complex generated by small Maf and Bach1 as a possible biochemical basis for β-globin locus control region complex. J. Biol. Chem., 273, 11783-11790.
32. Itoh, K., Igarashi, K., Hayashi, N., Nishizawa, M. and Yamamoto, M. (1995) Cloning and characterization of a novel erythroid-derived CNC family transcription factor heterodimerizing with the small Maf family proteins. Mol. Cell. Biol., 15, 4184-4193.
33. Johnsen, O., Murphy, P., Prydz, H. and Kolsto, A.B. (1998) Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res., 26, 512-520.
34. Kataoka, K., Nishizawa, M. and Kawa, S. (1993) Structure-function analysis of the maf oncogene product, a member of the b-zip protein family. J. Virol., 67, 2133-2141.
35. Kataoka, K., Fujiwara, K.T., Noda, M. and Nishizawa, M. (1994a) MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol. Cell. Biol., 14, 7581-7591.
36. Kataoka, K., Noda, M. and Nishizawa, M. (1994b) Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol. Cell. Biol., 14, 700-712.
37. Kataoka, K., Igarashi, K., Itoh, K., Fujiwara, K.T., Noda, M., Yamamoto, M. and Nishizawa, M. (1995) Small Maf proteins heterodimerize with Fos and potentially act as competitive repressors of NF-E2 transcription factor. Mol. Cell Biol., 15, 2180-2190.
38. Kearney, J.F., Radbruch, A., Liesegang, B. and Rajewsky, K. (1979) A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J. Immunol., 123, 1548-1550.
39. Kim, K.J., Knellopoulos-Lngevin, C., Merwin, R.M., Sachs, D.H. and Asofsky, R. (1979) Establishment and characterization of BALB/c lymphoma lines with B cell propreties. J. Immunol., 122, 549-554.
40. + cells by a clonal bone marrow stromal cell line. Exp. Hematol., 26, 280-287.
41. Li, Y.-S., Wasserman, R., Hayakawa, K. and Hardy, R.R. (1996) Identification of earliest B lineage stage in mouse bone marrow. Immunity, 5, 527-535.
42. Lieberson, R., Giannini, S.L., Birshtein, B.K. and Eckhardt, L.A. (1991) An enhancer at the 3′ end of the mouse immunoglobulin heavy chain locus. Nucleic Acids Res., 19, 933-937.
43. Lin, R.J., Nagy, L., Inoue, S., Shao, W., Miller, W.H.,Jr and Evans, R.M. (1998) Role of the histone deacetylase complex in acute promyelocytic leukemia. Nature, 391, 811-814.
44. Luna, L., Johnsen, O., Skartlien, A.H., Pedeutour, F., Turc-Carel, C., Prydz, H. and Kolsto, A. (1994) Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics, 22, 553-562.
45. Lynes, M.A., Lanier, L.L., Babcock, G.F., Wettstein, P.J. and Haughton, G. (1978) Antigen-induced murine B cell lymphomas I. Induction and characterization of CH1 and CH2. J. Immunol., 121, 2352-2357.
46. Madisen, L. and Groudine, M. (1994) Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt's lymphoma cells. Genes Dev., 8, 2212-2226.
47. Matthias, P. and Baltimore, D. (1993) The immunoglobulin heavy chain locus contains another B-cell-specific enhancer close to the a constant region. Mol. Cell. Biol. 13, 1547-1553.
48. Mills, F.C., Harindranath, N., Mitchell, M. and Max, E.E. (1997) Enhancer complexes located downstream of both human immunoglobulin Cα genes. J. Exp. Med., 186, 845-858.
49. Mizushima, S. and Nagata, S. (1990) pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res., 18, 5332.
50. Moi, P., Chan, K., Asunis, I., Cao, A. and Kan, Y.W. (1994) Isolation of NF-E2-related factor 2 (Nrf2), an NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the β-globin locus control region. Proc. Natl Acad. Sci. USA, 91, 9926-9930.
51. Motohashi, H., Igarashi, K., Onodera, K., Takahashi, S., Ohtani, H., Nakafuku, M., Nishizawa, M., Engel, J.D. and Yamamoto, M. (1996) Mesodermal-versus neuronal-specific expression of MafK is elicited by different promoters. Genes Cells, 1, 223-238.
52. Motohashi, H., Shavit, J.A., Igarashi, K., Yamamoto, M. and Engel, J.D. (1997) The world according to Maf. Nucleic Acids Res., 25, 2953-2959.
53. Ney, P.A. et al. (1993) Purification of the human NF-E2 complex: cDNA cloning of the hematopoietic cell-specific subunit and evidence for an associated partner. Mol. Cell. Biol., 13, 5604-5612.
54. Nishizawa, M., Kataoka, K., Goto, N., Fujiwara, K.T. and Kawai, S. (1989) v-maf, a viral oncogene that encodes a leucine zipper motif. Proc. Natl Acad. Sci. USA, 86, 7711-7715.
55. Oi, V.T., Morrison, S.L., Herzenberg, L.A. and Berg, P. (1983) Immunoglobulin gene expression in transformed lymphoid cells. Immunology, 80, 825-829.
56. Osawa, M., Hanada, K., Hamada, H. and Nakauchi, H. (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science, 273, 242-245.
57. Oyake, T., Itoh, K., Motohashi, H., Hayashi, N., Hoshino, H., Nishizawa, M., Yamamoto, M. and Igarashi, K. (1996) Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol., 16, 6083-6095.
58. Pagano, M., Durst, M., Joswig, S., Draetta, G. and Jansen-Durr, P. (1992) Binding of the human E2F transcription factor to the retinoblastoma protein but not to cyclin A is abolished in HPV-16-immortalized cells. Oncogene, 7, 1681-1686.
59. Pettersson, S., Cook, G.P, Bruggemann, M., Williams, G.T. and Neuberger, M.S. (1990) A second B cell-specific enhancer 3′ of the immunoglobulin heavy-chain locus. Nature, 344, 165-168.
60. Rolink, A. and Melchers, F. (1991) Molecular and cellular origins of B lymphocyte diversity. Cell, 66, 1081-1094.
61. Rosenberg, N. and Baltimore, D. (1978) The effect of helper virus on Abelson virus-induced transformation of lymphoid cells. J. Exp. Med., 147, 1126-1141.
62. Shinkai, Y. et al. (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell, 68, 855-867.
63. Sibley, C.H., Ewald, S.J., Kehry, M.R., Douglas, R.H., Raschke, W.C. and Hood, L.H. (1980) Characterization of multiple immunoglobulin γ-chains synthesized by two clones of a B cell lymphoma. J. Immunol., 125, 2097-2105.
64. Singh, M. and Birshtein, B. (1993) NF-HB (BASF) is a repressor of the murine immunoglobulin heavy chain 3′α enhancer at early stages of B-cell differentiation. Mol. Cell. Biol., 13, 3611-3622.
65. Swaroop, A., Xu, J., Pawar, H., Jackson, A., Scolnick, C. and Agarwal, N. (1992) A conserved retina-specific gene encodes a basic motif/leucine zipper protein. Proc. Natl Acad. Sci. USA, 89, 266-270.
66. Toki, T. et al. (1997) Human small Maf proteins form heterodimers with CNC family transcription factors and recognize NF-E2 motif. Oncogene, 14, 1901-1910.
67. Warner, N.L., Daley, M.J., Richey, J. and Spellman, C. (1979) Flow cytometry analysis of murine B cell lymphoma differentiation. Immunol. Rev., 48, 197-243.
68. Ye, B.H., Lista, F., Coco, F.L., Knowles, D.M., Offit, K., Chaganti, R.S.K. and Dalla-Favera, R. (1993) Alterations of a zinc finger-encoding gene, BCL-6, in diffuse large-cell lymphoma. Science, 262, 747-750.