Spi-C has opposing effects to PU.1 on gene expression in progenitor B cells

Journal of Immunology

Volumn 177, Issue 4, 2006, Pages 2195-2207

  Schweitzer, Brock L ^a   Huang, Kelly J ^a   Kamath, Meghana B ^a   Emelyanov, Alexander V ^b   Birshtein, Barbara K ^b   DeKoter, Rodney P ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; HISTONE H3; INTERLEUKIN 7; LYSINE; RETROVIRUS VECTOR; STEM CELL FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR SPI C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SEQUENCE; ENHANCER REGION; FETUS LIVER; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROMOTER REGION;

EID: 33746932517     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.4.2195     Document Type: Article

References (64)

1. Rolink, A., A. Kudo, and F. Melchers. 1991. Long-term proliferating early pre-B-cell lines and clones with the potential to develop to surface immunoglobulin-positive, mitogen-reactive B-cells in vitro and in vivo. Biochem. Soc. Trans. 19: 275-276.
2. Fleming, H. E., and C. J. Paige. 2002. Cooperation between IL-7 and the pre-B cell receptor: a key to B cell selection. Semin. Immunol. 14: 423-430.
3. Singh, H., K. L. Medina, and J. M. Pongubala. 2005. Contingent gene regulatory networks and B cell fate specification. Proc. Natl. Acad. Sci. USA 102: 4949-4953.
4. Henderson, A. J., and K. L. Calame. 1995. Lessons in transcriptional regulation learned from studies on immunoglobulin genes. Crit. Rev. Eukaryot. Gene Expr. 5: 255-280.
5. Lennon, G. G., and R. P. Perry. 1985. C μ-containing transcripts initiate heterogeneously within the IgH enhancer region and contain a novel 5′-nontranslatable exon. Nature 318: 475-478.
6. Khamlichi, A. A., E. Pinaud, C. Decourt, C. Chauveau, and M. Cogne. 2000. The 3′ IgH regulatory region: a complex structure in a search for a function. Adv. Immunol. 75: 317-345.
7. Michaelson, J. S., S. L. Giannini, and B. K. Birshtein. 1995. Identification of 3′ α-hs4, a novel Ig heavy chain enhancer element regulated at multiple stages of B cell differentiation. Nucleic Acids Res. 23: 975-981.
8. Saleque, S., M. Singh, R. D. Little, S. L. Giannini, J. S. Michaelson, and B. K. Birshtein. 1997. Dyad symmetry within the mouse 3′ IgH regulatory region includes two virtually identical enhancers (C α3′E and hs3). J. Immunol. 158: 4780-4787.
9. Pinaud, E., A. A. Khamlichi, C. Le Morvan, M. Drouet, V. Nalesso, M. Le Bert, and M. Cogne. 2001. Localization of the 3′ IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15: 187-199.
10. Akbarali, Y., P. Oettgen, J. Boltax, and T. A. Libermann. 1996. ELF-1 interacts with and transactivates the IgH enhancer pi site. J. Biol. Chem. 271: 26007-26012.
11. Nelsen, B., G. Tian, B. Erman, J. Gregoire, R. Maki, B. Graves, and R. Sen. 1993. Regulation of lymphoid-specific immunoglobulin μ heavy chain gene enhancer by ETS-domain proteins. Science 261: 82-86.
12. Rivera, R. R., M. H. Stuiver, R. Steenbergen, and C. Murre. 1993. Ets proteins: new factors that regulate immunoglobulin heavy-chain gene expression. Mol. Cell. Biol. 13: 7163-7169.
13. Grant, P. A., C. B. Thompson, and S. Pettersson. 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.
14. Linderson, Y., D. Eberhard, S. Malin, A. Johansson, M. Busslinger, and S. Pettersson. 2004. Corecruitment of the Grg4 repressor by PU.1 is critical for Pax5-mediated repression of B-cell-specific genes. EMBO Rep. 5: 291-296.
15. Hagman, J., and R. Grosschedl. 1992. An inhibitory carboxyl-tenninal domain in Fts-1 and Ets-2 mediates differential binding of ETS family factors to promoter sequences of the inb-1 gene. Proc. Natl. Acad. Sci. USA 89: 8889-8893.
16. Himmelmann, A., A. Riva, G. L. Wilson, B. P. Lucas, C. Thevenin, and J. H. Kehrl. 1997. PU.1/Pip and basic helix loop helix zipper transcription factors interact with binding sites in the CD20 promoter to help confer lineage- and stage-specific expression of CD20 in B lymphocytes. Blood 90: 3984-3995.
17. Muller, S., P. Sideras, C. I. Smith, and K. G. Xanthopoulos. 1996. Cell specific expression of human Bruton's agammaglobulinemia tyrosine kinase gene (Btk) is regulated by Spl- and Spi-1/PU.1-family members. Oncogene 13: 1955-1964.
18. Shin, M. K., and M. E. Koshland. 1993. Ets-related protein PU.1 regulates expression of the immunoglobulin J-chain gene through a novel Ets-binding clement. Genes Dev. 1: 2006-2015.
19. Ying, H., J. F. Chang, and J. R. Parnes. 1998. PU.1/Spi-1 is essential for the B cell-specific activity of the mouse CD72 promoter. J. Immunol. 160: 2287-2296.
20. Eisenbeis, C. F., H. Singh, and U. Storb. 1993. PU.1 is a component of a multiprotein complex which binds an essential site in the murine immunoglobulin λ 2-4 enhancer. Mol. Cell. Biol. 13: 6452-6461.
21. Nikolajczyk, B. S., J. A. Sanchez, and R. Sen. 1999. ETS protein-dependent accessibility changes at the immunoglobulin μ heavy chain enhancer. Immunity 11: 11-20.
22. Pongubala, J. M., S. Nagulapalli, M. J. Klemsz, S. R. McKercher, R. A. Maki, and M. L. Atchison. 1992. PU.1 recruits a second nuclear factor to a site important for immunoglobulin κ 3′ enhancer activity. Mol. Cell. Biol. 12: 368-378.
23. Schwarzenbach, H., J. W. Newell, and P. Matthias. 1995. Involvement of the Ets family factor PU.1 in the activation of immunoglobulin promoters. J. Biol. Chem. 270: 898-907.
24. Iwasoki, H., C. Somoza, H. Shigematsu, E. A. Duprez, J. Iwasaki-Arai, S. Mizuno, Y. Arinobu, K. Geary, P. Zhang, T. Dayaram, et al. 2005. Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation. Blood 106: 1590-1600.
25. Medina, K. L., J. M. Pongubala, K. L. Reddy, D. W. Lancki, R. Dekoter, M. Kieslinger, R. Grosschedl, and H. Singh. 2004. Assembling a gene regulatory network for specification of the B cell fate. Dev. Cell 7: 607-617.
26. Polli, M., A. Dakic, A. Light, L. Wu, D. M. Tarlinton, and S. L. Nutt. 2005. The development of functional B lymphocytes in conditional PU.1 knock-out mice. Blood 106: 2083-2090.
27. Ye, M., O. Ermakova, and T. Graf. 2005. PU.1 is not strictly required for B cell development and its absence induces a B-2 to B-1 cell switch. J. Exp. Med. 202: 1411-1422.
28. DeKoter, R. P., H. J. Lee, and H. Singh. 2002. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity 16: 297-309.
29. Schweitzer, B. L., and R. P. DeKoter. 2004. Analysis of gene expression and Ig transcription in PU.1/Spi-B-deficient progenitor B cell lines. J Immunol. 172: 144-154.
30. Bemark, M., A. Martensson, D. Liberg, and T. Leanderson. 1999. Spi-C, a novel Ets protein that is temporally regulated during B lymphocyte development. J. Biol. Chem. 274: 10259-10267.
31. Hashimoto, S., H. Nishizumi, R. Hayashi, A. Tsuboi, F. Nagawa, T. Takemori, and H. Sakano. 1999. Prf, a novel Ets family protein that binds to the PU.1 binding motif, is specifically expressed in restricted stages of B cell development. Int. Immunol 11: 1423-1429.
32. Carlsson, R., C. Persson, and T. Leanderson. 2003. SPI-C, a PU-box binding ETS protein expressed temporarily during B-cell development and in macrophages, contains an acidic transactivation domain located to the N-terminus. Mol. Immunol. 39: 1035-1043.
33. Hromas, R., A. Orazi, R. S. Neiman, R. Maki, C. Van Beveran, J. Moore, and M. Klemsz. 1993. Hematopoietic lineage- and stage-restricted expression of the ETS oncogene family member PU.1. Blood 82: 2998-3004.
34. Klemsz, M. J., S. R. McKercher, A. Celada, C. Van Beveren, and R. A. Maki. 1990. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell 61: 113-124.
35. Su, G. H., H. M. Chen, N. Muthusamy, L. A. Garrett-Sinha, D. Baunoch, D. G. Tenen, and M. C. Simon. 1997. Defective B cell receptor-mediated responses in mice lacking the Ets protein. Spi-B. EMBO J. 16: 7118-7129.
36. Brass, A. L., E. Kehrli, C. F. Eisenbeis, U. Storb, and H. Singh. 1996. Pip, a lymphoid-restricted IRF, contains a regulatory domain that is important for autoinhibition and ternary complex formation with the Ets factor PU.1. Genes Dev. 10: 2335-2347.
37. Pear, W. S., J. P. Miller, L. Xu, J. C. Pui, B. Softer, R. C. Quackenbush, A. M. Pendergasl, R. Bronson, J. C. Aster, M. L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-3792.
38. Lindeman, G. J., A. W. Harris, M. L. Bath, R. N. Eisenman, and J. M. Adams. 1995. Overexpressed max is not oncogenic and attenuates myc-induced lymphoproliferation and lymphomagenesis in transgenic mice. Oncogene 10: 1013-1017.
39. Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7: 1063-1066.
40. Schlissel, M., A. Voronova, and D. Baltimore. 1991. Helix-loop-helix transcription factor E47 activates germ-line immunoglobulin heavy-chain gene transcription and rearrangement in a prc-T-cell line. Genes Dev. 5: 1367-1376.
41. Garrett, F. E., A. V. Emelyanov, M. A. Sepulveda, P. Flanagan, S. Volpi, F. Li, D. Loukinov, L. A. Eckhardt, V. V. Lobanenkov, and B. K. Birshtein. 2005. Chromatin architecture near a potential 3′ end of the igh locus involves modular regulation of histone modifications during B-cell development and in vivo occupancy at CTCF sites. Mol. Cell. Biol. 25: 1511-1525.
42. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288: 1439-1441.
43. Melamed, D., J. A. Kench, K. Grabstein, A. Rolink, and D. Nemazee. 1997. A functional B cell receptor transgene allows efficient IL-7-independent maturation of B cell precursors. J. Immunol. 159: 1233-1239.
44. Benschop, R. J., and J. C. Cambier. 1999. B cell development: signal transduction by antigen receptors and their surrogates. Curr. Opin. Immunol. 11: 143-151.
45. Ravetch, J. V., and L. L. Lanier. 2000. Immune inhibitory receptors. Science 290: 84-84.
46. Jegga, A. G., S. P. Sherwood, J. W. Carman, A. T. Pinski, J. L. Phillips, J. P. Pestian, and B. J. Aronow. 2002. Detection and visualization of compositionally similar cis-regulatory element clusters in orthologous and coordinately controlled genes. Genome Res. 12: 1408-1417.
47. Brass, A. L., A. Q. Zhu, and H. Singh. 1999. Assembly requirements of PU.1-Pip (IRF-4) activator complexes: inhibiting function in vivo using fused dimers. EMBO J. 18: 977-991.
48. Birshtein, B. K., C. Chen, S. Saleque, J. S. Michaelson, M. Singh, and R. D. Little. 1997. Murine and human 3′IgH regulatory sequences. Curr. Top. Microbiol. Immunol. 224: 73-80.
49. Madisen, L., and M. Groudine. 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.
50. Gregor, P. D., B. J. Kobrin, C. Milcarek, and S. L. Morrison. 1986. Sequences 3′ of immunoglobulin heavy chain genes influence their expression. Immunol. Rev. 89: 31-48.
51. Lieberson, R., J. Ong, X. Shi, and L. A. Eckhardt. 1995. Immunoglobulin gene transcription ceases upon deletion of a distant enhancer. EMBO J. 14: 6229-6238.
52. Shi, X., and L. A. Eckhardt. 2001. Deletional analyses reveal an essential role for the hs3b/hs4 IgH 3′ enhancer pair in an Ig-secreting but not an earlier-stage B cell line. Int. Immunol. 13: 1003-1012.
53. H recombination. J. Immunol. 176: 2439-2447.
54. Perlot, T., F. W. Alt, C. H. Bassing H. Suh, and E. Pinaud. 2005. Elucidation of IgH intronic enhancer functions via germ-line deletion. Proc. Natl. Acad. Sci. USA 102: 14362-14367.
55. Workman, J. L., and R. E. Kingston. 1998. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67: 545-579.
56. Corcoran, A. E. 2005. Immunoglobulin locus silencing and allelic exclusion. Semin. Immunol. 17: 141-144.
57. Dahl, R., D. L. Ramirez-Bergeron, S. Rao, and M. C. Simon. 2002. Spi-B can functionally replace PU.1 in myeloid but not lymphoid development. EMBO J. 21: 2220-2230.
58. Rosenbauer, F., B. M. Owens, L. Yu, J. R. Tumang, U. Steidl, J. L. Kutok, L. K. Clayton, K. Wagner, M. Scheller, H. Iwasaki, et al. 2006. Lymphoid cell growth and transformation are suppressed by a key regulatory element of the gene encoding PU.1. Nat. Genet. 38: 27-37.
59. Nult, S. L., D. Metcalf, A. D'Amico, M. Polli, and L. Wu. 2005. Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J. Exp. Med. 201: 221-231.
60. Berclaz, P. Y., Y. Shibata, J. A. Whitsett, and B. C. Trapnell. 2002. GM-CSF, via PU.1, regulates alveolar macrophage FcγR-mediated phagocytosis and the IL-18/IFN-γ-mediated molecular connection between innate and adaptive immunity in the lung. Blood 100: 4193-4200.
61. Takai, T. 2002. Roles of Fc receptors in autoimmunity. Nat. Rev. Immunol. 2: 580-584.
62. Le Clech, M., E. Chalhoub, C. Dohet, V. Roure, S. Fichelson, F. Moreau-Gachelin, and D. Mathieu. 2006. PU.1/Spi-1 binds to the human TAL-1 silencer to mediate its activity. J. Mol. Biol. 355: 9-19.
63. Suzuki, M., T. Yamada, F. Kihara-Negishi, T. Sakurai, E. Hara, D. G. Tenen, N. Hozumi, and T. Oikawa. 2006. Site-specific DNA methylation by a complex of PU.1 and Dnmt3a/b. Oncogene 25: 2477-2488.
64. Bain, M., M. Mendelson, and J. Sinclair. 2003. Ets-2 repressor factor (ERF) mediates repression of the human cytomegalovirus major immediate-early promoter in undifferentiated nonpermissive cells. J. Gen. Virol. 84: 41-49.