EBF1 acts as a powerful repressor of Blimp-1 gene expression in immature B cells

Biochemical and Biophysical Research Communications

Volumn 422, Issue 4, 2012, Pages 780-785

  Kikuchi, Hidehiko ^a   Nakayama, Masami ^a   Takami, Yasunari ^a   Kuribayashi, Futoshi ^b   Nakayama, Tatsuo ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

Author keywords

Blimp 1; DT40; EBF1; Gene targeting; Immature b cell

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; MESSENGER RNA; PROTEIN EARLY B CELL FACTOR 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; GENE EXPRESSION; GENE OVEREXPRESSION; IN VIVO STUDY; NONHUMAN; PLASMA CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; PROTEIN SYNTHESIS; RECEPTOR DOWN REGULATION; TRANSCRIPTION REGULATION; ZINC FINGER MOTIF;

5' UNTRANSLATED REGIONS; ANIMALS; B-LYMPHOCYTES; BASE SEQUENCE; CELL LINE; CHICKENS; CHROMATIN IMMUNOPRECIPITATION; DOWN-REGULATION; GENE EXPRESSION REGULATION; HELIX-LOOP-HELIX MOTIFS; MOLECULAR SEQUENCE DATA; REPRESSOR PROTEINS; UP-REGULATION; ZINC FINGERS;

MUS;

EID: 84862300234     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.05.099     Document Type: Article

References (43)

1. Zhuang Y., Soriano P., Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell 1994, 79:875-884.
2. Lin H., Grosschedl R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 1995, 376:263-267.
3. Urbanek P., Wang Z.Q., Fetka I., Wagner E.F., Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 1994, 79:901-912.
4. Anderson K.L., Smith K.A., Conners K., McKerche S.R., Maki R.A., Torbett B.E. Myeloid development is selectively disrupted in PU.1 null mice. Blood 1998, 91:3702-3710.
5. Klug C.A., Morrison S.J., Masek M., Hahm K., Smale S.T., Weissman I.L. Hematopoietic stem cells and lymphoid progenitors express different Ikaros isoforms, and Ikaros is localized to heterochromatin in immature lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:657-662.
6. Wang J.H., Avitahl N., Cariappa A., Friedrich C., Ikeda T., Renold A., Andrikopoulos K., Liang L., Pillai S., Morgan B.A., Georgopoulos K. Aiolos regulates B cell activation and maturation to effector state. Immunity 1998, 9:543-553.
7. Smith E., Sigvardsson M. The roles of transcription factors in B lymphocytes commitment, development, and transformation. J. Leukoc. Biol. 2004, 75:973-981.
8. Ramirez J., Lukin K., Hagman J. From hematopoietic progenitors to B cells: mechanisms of lineage restriction and commitment. Curr. Opin. Immunol. 2010, 22:177-184.
9. Liao D. Emerging roles of the EBF family of transcription factors in tumor suppression. Mol. Cancer Res. 2009, 7:1893-1901.
10. Lukin K., Fields S., Hartley J., Hagman J. Early B cell factor: regulator of B lineage specification and commitment. Semin. Immunol. 2008, 20:221-227.
11. Sigvardsson M., Clark D.R., Fitzsimmons D., Doyle M., Akerblad P., Breslin T., Bilke S., Li R., Yeamans C., Zhang G., Hagman J. Early B-cell factor, E2A, and Pax5 cooperate to activate the early B cell-specific mb-1 promoter. Mol. Cell. Biol. 2002, 22:8539-8551.
12. O'Riordan M., Grosschedl R. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 1999, 11:21-31.
13. Decker T., Pasca di Magliano M., McManus S., Sun Q., Bonifer C., Tagoh H., Busslinger M. Stepwise activation of enhancer and promoter regions of the B cell commitment gene Pax5 in early lymphopoiesis. Immunity 2009, 30:508-520.
14. Nutt S.L., Kee B.L. The transcriptional regulation of B cell lineage commitment. Immunity 2007, 26:715-725.
15. Thal M.A., Carvalho T.L., He T., Kim H.G., Gao H., Hagman J., Klug C.A. Ebf1-mediated down-regulation of Id2 and Id3 is essential for specification of the B cell lineage. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:552-557.
16. Treiber T., Mandel E.M., Pott S., Gyry I., Firner S., Liu E.T., Grosschedl R. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription-independent poising of chromatin. Immunity 2010, 32:714-725.
17. Gyory I., Boller S., Nechanitzky R., Mandel E., Pott S., Liu E., Grosschedl R. Transcription factor EBF1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev. 2012, 26:668-682.
18. Buerstedde J.M., Takeda S. Increased ration of targeted to random integration after transfection of chicken B cell lines. Cell 1991, 67:179-188.
19. Alinikula J., Lassila O., Nera K.P. DT40 mutants: a model to study transcriptional regulation of B cell development and function. Reviews and Protocols in DT40 Research 2006, 189-205. Springer-Verlag, Berlin. J.M. Buerstedde, S. Takeda (Eds.).
20. Kikuchi H., Barman H.K., Nakayama M., Takami Y., Nakayama T. Participation of histones, histone modifying enzymes and histone chaperons in vertebrate cell functions. Reviews and Protocols in DT40 Research 2006, 225-243. Springer-Verlag, Berlin. J.-M. Buerstedde, S. Takeda (Eds.).
21. Nakayama M., Suzuki H., Yamamoto-Nagamatsu N., Barman H.K., Kikuchi H., Takami Y., Toyonaga K., Yamashita K., Nakayama T. HDAC2 controls IgM H- and L-chain gene expressions via EBF1, Pax5, Ikaros, Aiolos and E2A gene expressions. Genes Cells 2007, 12:359-373.
22. Toyonaga K., Kikuchi H., Yamashita K., Nakayama M., Chijiiwa K., Nakayama T. E2A participates in a fine control of pre-mature B-cell apoptosis mediated by B-cell receptor signaling via transcriptional regulation of survivin, IAP2 and caspase-8 genes. FEBS J. 2009, 276:1418-1428.
23. Kikuchi H., Yamashita K., Nakayama M., Toyonaga K., Tsuneyoshi I., Takasaki M., Nakayama T. Lacking of Aiolos accelerates pre-mature B cell apoptosis mediated by BCR signaling through elevation in cytochrome c release. Biochim. Biophys. Acta 2009, 1793:1304-1314.
24. Kikuchi H., Nakayama M., Takami Y., Kuribayashi F., Nakayama T. Possible involvement of Helios in controlling the immature B cell functions via transcriptional regulation of protein kinase Cs. Results Immunol. 2011, 1:88-94.
25. Kikuchi H., Takami Y., Nakayama T. GCN5: a supervisor in all-inclusive control of vertebrate cell cycle progression through transcription regulation of various cell cycle-related genes. Gene 2005, 347:83-97.
26. Kikuchi H., Nakayama T. GCN5 and BCR signalling collaborate to induce pre-mature B cell apoptosis through depletion of ICAD and IAP2 and activation of caspase activities. Gene 2008, 419:48-55.
27. Kikuchi H., Kuribayashi F., Kiwaki N., Takami Y., Nakayama T. GCN5 regulates the superoxide-generating system in leukocytes via controlling gp91-phox gene expression. J. Immunol. 2011, 186:3015-3022.
28. Kikuchi H., Kuribayashi F., Takami Y., Imajoh-Ohmi S., Nakayama T. GCN5 regulates the activation of PI3K/Akt survival pathway in B cells exposed to oxidative stress via controlling gene expressions of Syk and Btk. Biochem. Biophys. Res. Commun. 2011, 405:657-661.
29. Nutt S.L., Fairfax K.A., Kallies A. BLIMP1 guides the fate of effector B and T cells. Nat. Rev. Immunol. 2007, 7:923-927.
30. Crotty S., Johnston R.J., Schoenberger S.P. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010, 11:114-120.
31. Angelin-Duclos C., Cattoretti G., Lin K.I., Calame K. Commitment of B lymphocytes to a plasma cell fate is associated with Blimp-1 expression in vivo. J. Immunol. 2000, 165:5462-5471.
32. Shapiro-Shelef M., Lin K.I., McHeyzer-Williams L.J., Liao J., McHeyzer-Williams M.G., Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 2003, 19:607-620.
33. Turner C.A., Mack D.H., Davis M.M. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 1994, 77:297-306.
34. Lin Y., Wong K., Calame K. Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 1997, 276:596-599.
35. Lin K.I., Angelin-Duclos C., Kuo T.C., Calame K. Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglibulin M-secreting plasma cells. Mol. Cell. Biol. 2002, 22:4771-4780.
36. Muto A., Ochiai K., Kimura Y., Itoh-Nakadai A., Calame K.L., Ikebe D., Tashiro S., Igarashi K. Bach2 represses plasma cell gene regulatory network in B cells to promote antibody class switch. EMBO J. 2010, 29:4048-4061.
37. Kallies A., Nutt S.L. Bach2: plasma-cell differentiation takes a break. EMBO J. 2010, 29:3896-3897.
38. Shaffer A.L., Lin K.I., Kuo T.C., Yu X., Hurt E.M., Rosenwald A., Giltnane J.M., Yang L., Zhao H., Calame K., Staudt L.M. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002, 17:51-62.
39. Klein B., Tarte K., Jourdan M., Mathouk K., Moreaux J., Jourdan E., Legouffe E., Vos J.D., Rossi J.F. Survival and proliferation factors of normal and malignant plasma cells. Int. J. Hematol. 2003, 78:106-113.
40. Mora-Lopez F., Reales E., Brieva J.A., Campos-Caro A. Human BSAP and BLIMP1 conform an autoregulatory feedback loop. Blood 2007, 110:3150-3157.
41. Hangaishi A., Kurokawa M. Blimp-1 is a tumor suppressor gene in lymphoid malignancies. Int. J. Hematol. 2010, 91:46-53.
42. Nera K.P., Kohonen P., Narvi E., Peippo A., Mustonen L., Terho P., Koskela K., Buerstedde J.M., Lassila O. Loss of Pax5 promotes plasma cell differentiation. Immunity 2006, 24:283-293.
43. Alinikula J., Nera K.P., Junttila S., Lassila O. Alternate pathways for Bcl6-mediated regulation of B cell to plasma cell differentiation. Eur. J. Immunol. 2011, 41:2404-2413.