Epigenetic Regulation of the Blimp-1 Gene (Prdm1) in B Cells Involves Bach2 and Histone Deacetylase 3

Journal of Biological Chemistry

Volumn 291, Issue 12, 2016, Pages 6316-6330

  Tanaka, Hiromu ^a   Muto, Akihiko ^a,b   Shima, Hiroki ^a,b   Katoh, Yasutake ^a   Sax, Nicolas ^a,b   Tajima, Shinya ^a   Brydun, Andrey ^a   Ikura, Tsuyoshi ^c   Yoshizawa, Naoko ^d   Masai, Hisao ^d   Hoshikawa, Yutaka ^e   Noda, Tetsuo ^e   Nio, Masaki ^a   Ochiai, Kyoko ^a,b   Igarashi, Kazuhiko ^a,b  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^e CANCER INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AIRSHIPS; ALKYLATION; CELLS; GENE EXPRESSION; GENES; NUCLEIC ACIDS; PROTEINS; TRANSCRIPTION;

CHROMATIN IMMUNOPRECIPITATION; EPIGENETIC MODIFICATION; EPIGENETIC REGULATION; HISTONE DEACETYLASES; MASTER REGULATORS; PLASMA CELL DIFFERENTIATION; RECOGNITION ELEMENT; TERMINAL DIFFERENTIATION;

CYTOLOGY;

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BTB AND CNC HOMOLOGUE 2; HISTONE DEACETYLASE 3; HISTONE H3; HISTONE H4; LEUCINE ZIPPER PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; NUCLEAR COREPRESSOR 1; NUCLEAR PROTEIN; RAP1 INTERACTING FACTOR HOMOLOG; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; TRANSDUCIN BETA LIKE 1X LINKED; UNCLASSIFIED DRUG; BACH2 PROTEIN, MOUSE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; HISTONE; HISTONE DEACETYLASE; NCOR1 PROTEIN, MOUSE; PRDM1 PROTEIN, MOUSE; RECEPTOR INTERACTING PROTEIN 140; RIF1 PROTEIN, MOUSE; TELOMERE BINDING PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; B LYMPHOCYTE; BAL17 CELL LINE; BINDING AFFINITY; BINDING SITE; BLIMP 1 GENE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA STRUCTURE; EMBRYO; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC REGULATION; HISTONE ACETYLATION; HISTONE DEACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INTRON; LYMPHOID CELL LINE; MAF RECOGNITION ELEMENT; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ACETYLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; ACETYLATION; ANIMAL; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN PROCESSING; TUMOR CELL LINE;

ACETYLATION; ANIMALS; B-LYMPHOCYTES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE, TUMOR; EPIGENESIS, GENETIC; GENE SILENCING; HEK293 CELLS; HISTONE DEACETYLASES; HISTONES; HUMANS; MICE; NUCLEAR RECEPTOR CO-REPRESSOR 1; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; TELOMERE-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84958207428     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.713842     Document Type: Article

References (51)

1. Igarashi, K., Ochiai, K., Itoh-Nakadai, A., and Muto, A. (2014) Orchestration of plasma cell differentiation by Bach2 and its gene regulatory network. Immunol. Rev. 261, 116-125
2. 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., and Staudt, L. M. (2002) Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17, 51-62
3. Shapiro-Shelef, M., Lin, K. I., McHeyzer-Williams, L. J., Liao, J., McHeyzer-Williams, M. G., and Calame, K. (2003) Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19, 607-620
4. Sciammas, R., and Davis, M. M. (2004) Modular nature of Blimp-1 in the regulation of gene expression during B cell maturation. J. Immunol. 172, 5427-5440
5. Kallies, A., Hasbold, J., Tarlinton, D. M., Dietrich, W., Corcoran, L. M., Hodgkin, P. D., and Nutt, S. L. (2004) Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200, 967-977
6. Turner, C. A., Jr., Mack, D. H., and Davis, M. M. (1994) Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77, 297-306
7. Schliephake, D. E., and Schimpl, A. (1996) Blimp-1 overcomes the block in IgM secretion in lipopolysaccharide/anti-F(ab-)2-co-stimulated B lymphocytes. Eur. J. Immunol. 26, 268-271
8. Lin, K. I., Angelin-Duclos, C., Kuo, T. C., and Calame, K. (2002) Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol. Cell. Biol. 22, 4771-4780
9. Calame, K. (2008) Activation-dependent induction of Blimp-1. Curr. Opin. Immunol. 20, 259-264
10. Toyama, H., Okada, S., Hatano, M., Takahashi, Y., Takeda, N., Ichii, H., Takemori, T., Kuroda, Y., and Tokuhisa, T. (2002) Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity 17, 329-339
11. Ye, B. H., Cattoretti, G., Shen, Q., Zhang, J., Hawe, N., de Waard, R., Leung, C., Nouri-Shirazi, M., Orazi, A., Chaganti, R. S., Rothman, P., Stall, A. M., Pandolfi, P. P., and Dalla-Favera, R. (1997) The BCL-6 proto-oncogene controls germinal-center formation and Th2-type inflammation. Nat. Genet. 16, 161-170
12. Tunyaplin, C., Shaffer, A. L., Angelin-Duclos, C. D., Yu, X., Staudt, L. M., and Calame, K. L. (2004) Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation. J. Immunol. 173, 1158-1165
13. Igarashi, K., and Watanabe-Matsui, M. (2014) Wearing red for signaling: the heme-bach axis in heme metabolism, oxidative stress response and iron immunology. Tohoku J. Exp. Med. 232, 229-253
14. 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
15. Ochiai, K., Katoh, Y., Ikura, T., Hoshikawa, Y., Noda, T., Karasuyama, H., Tashiro, S., Muto, A., and Igarashi, K. (2006) Plasmacytic transcription factor Blimp-1 is repressed by Bach2 in B cells. J. Biol. Chem. 281, 38226-38234
16. Ochiai, K., Muto, A., Tanaka, H., Takahashi, S., and Igarashi, K. (2008) Regulation of the plasma cell transcription factor Blimp-1 gene by Bach2 and Bcl6. Int. Immunol. 20, 453-460
17. Muto, A., Hoshino, H., Madisen, L., Yanai, N., Obinata, M., Karasuyama, H., Hayashi, N., Nakauchi, H., Yamamoto, M., Groudine, M., and Igarashi, K. (1998) Identification of Bach2 as a B-cell-specific partner for small Maf proteins that negatively regulate the immunoglobulin heavy chain gene 3-enhancer. EMBO J. 17, 5734-5743
18. Muto, A., Tashiro, S., Nakajima, O., Hoshino, H., Takahashi, S., Sakoda, E., Ikebe, D., Yamamoto, M., and Igarashi, K. (2004) The transcriptional programme of antibody class switching involves the repressor Bach2. Nature 429, 566-571
19. Muto, A., Ochiai, K., Kimura, Y., Itoh-Nakadai, A., Calame, K. L., Ikebe, D., Tashiro, S., and Igarashi, K. (2010) Bach2 represses plasma cell gene regulatory network in B cells to promote antibody class switch. EMBO J. 29, 4048-4061
20. Nakatani, Y., and Ogryzko, V. (2003) Immunoaffinity purification of mammalian protein complexes. Methods Enzymol. 370, 430-444
21. Smith, A. L., Friedman, D. B., Yu, H., Carnahan, R. H., and Reynolds, A. B. (2011) ReCLIP (reversible cross-link immuno-precipitation): an efficient method for interrogation of labile protein complexes. PLoSONE6, e16206
22. Lawrence, A. M., and Besir, H. U. (2009) Staining of proteins in gels with Coomassie G-250 without organic solvent and acetic acid. J. Vis. Exp. 30, 1350
23. Shih, T. A., Roederer, M., and Nussenzweig, M. C. (2002) Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 3, 399-406
24. Ochiai, K., Maienschein-Cline, M., Mandal, M., Triggs, J. R., Bertolino, E., Sciammas, R., Dinner, A. R., Clark, M. R., and Singh, H. (2012) A selfreinforcing regulatory network triggered by limiting IL-7 activates pre-BCR signaling and differentiation. Nat. Immunol. 13, 300-307
25. Yamasaki, C., Tashiro, S., Nishito, Y., Sueda, T., and Igarashi, K. (2005) Dynamic cytoplasmic anchoring of the transcription factor Bach1 by intracellular hyaluronic acid binding protein IHABP. J. Biochem. 137, 287-296
26. Matsuyama, A., Shimazu, T., Sumida, Y., Saito, A., Yoshimatsu, Y., Seigneurin-Berny, D., Osada, H., Komatsu, Y., Nishino, N., Khochbin, S., Horinouchi, S., and Yoshida, M. (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831
27. Sawado, T., Igarashi, K., and Groudine, M. (2001) Activation of-major globin gene transcription is associated with recruitment of NF-E2 to the-globin LCR and gene promoter. Proc. Natl. Acad. Sci. U.S.A. 98, 10226-10231
28. Sun, J., Brand, M., Zenke, Y., Tashiro, S., Groudine, M., and Igarashi, K. (2004) Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc. Natl. Acad. Sci. U.S.A. 101, 1461-1466
29. Yamazaki, S., Ishii, A., Kanoh, Y., Oda, M., Nishito, Y., and Masai, H. (2012) Rif1 regulates the replication timing domains on the human genome. EMBO J. 31, 3667-3677
30. Chapman, J. R., Barral, P., Vannier, J. B., Borel, V., Steger, M., Tomas-Loba, A., Sartori, A. A., Adams, I. R., Batista, F. D., and Boulton, S. J. (2013) RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell 49, 858-871
31. Di Virgilio, M., Callen, E., Yamane, A., Zhang, W., Jankovic, M., Gitlin, A. D., Feldhahn, N., Resch, W., Oliveira, T. Y., Chait, B. T., Nussenzweig, A., Casellas, R., Robbiani, D. F., and Nussenzweig, M. C. (2013) Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 339, 711-715
32. Escribano-Díaz, C., Orthwein, A., Fradet-Turcotte, A., Xing, M., Young, J. T., Tkác, J., Cook, M. A., Rosebrock, A. P., Munro, M., Canny, M. D., Xu, D., and Durocher, D. (2013) A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell 49, 872-883
33. Zimmermann, M., Lottersberger, F., Buonomo, S. B., Sfeir, A., and de Lange, T. (2013) 53BP1 regulates DSB repair using Rif1 to control 5-end resection. Science 339, 700-704
34. Li, J., Wang, J., Wang, J., Nawaz, Z., Liu, J. M., Qin, J., and Wong, J. (2000) Both co-repressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J. 19, 4342-4350
35. Guenther, M. G., Yu, J., Kao, G. D., Yen, T. J., and Lazar, M. A. (2002) Assembly of the SMRT-histone deacetylase 3 repression complex requires the TCP-1 ring complex. Genes Dev. 16, 3130-3135
36. Hoshino, H., Nishino, T. G., Tashiro, S., Miyazaki, M., Ohmiya, Y., Igarashi, K., Horinouchi, S., and Yoshida, M. (2007) Co-repressor SMRT and class II histone deacetylases promote Bach2 nuclear retention and formation of nuclear foci that are responsible for local transcriptional repression. J. Biochem. 141, 719-727
37. Dhordain, P., Albagli, O., Lin, R. J., Ansieau, S., Quief, S., Leutz, A., Kerckaert, J.-P., Evans, R. M., and Leprince, D. (1997) CorepressorSMRTbinds the BTB/POZ repressing domain of the LAZ3/BCL6 oncoprotein. Proc. Natl. Acad. Sci. U.S.A. 94, 10762-10767
38. Polo, J. M., Dell'Oso, T., Ranuncolo, S. M., Cerchietti, L., Beck, D., Da Silva, G. F., Prive, G. G., Licht, J. D., and Melnick, A. (2004) Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nat. Med. 10, 1329-1335
39. Minami, J., Suzuki, R., Mazitschek, R., Gorgun, G., Ghosh, B., Cirstea, D., Hu, Y., Mimura, N., Ohguchi, H., Cottini, F., Jakubikova, J., Munshi, N. C., Haggarty, S. J., Richardson, P. G., Hideshima, T., and Anderson, K. C. (2014) Histone deacetylase 3 as a novel therapeutic target in multiple myeloma. Leukemia 28, 680-689
40. Law, I. K., Liu, L., Xu, A., Lam, K. S., Vanhoutte, P. M., Che, C. M., Leung, P. T., and Wang, Y. (2009) Identification and characterization of proteins interacting with SIRT1 and SIRT3: implications in the anti-Aging and metabolic effects of sirtuins. Proteomics 9, 2444-2456
41. Goehler, H., Lalowski, M., Stelzl, U., Waelter, S., Stroedicke, M., Worm, U., Droege, A., Lindenberg, K. S., Knoblich, M., Haenig, C., Herbst, M., Suopanki, J., Scherzinger, E., Abraham, C., Bauer, B., et al. (2004)Aprotein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol. Cell 15, 853-865
42. Dan, J., Liu, Y., Liu, N., Chiourea, M., Okuka, M., Wu, T., Ye, X., Mou, C., Wang, L., Wang, L., Yin, Y., Yuan, J., Zuo, B., Wang, F., Li, Z., et al. (2014) Rif1 maintains telomere length homeostasis of ESCs by mediating heterochromatin silencing. Dev. Cell 29, 7-19
43. Hargreaves, D. C., and Crabtree, G. R. (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396-420
44. Osakabe, A., Tachiwana, H., Matsunaga, T., Shiga, T., Nozawa, R. S., Obuse, C., and Kurumizaka, H. (2010) Nucleosome formation activity of human somatic nuclear autoantigenic sperm protein (sNASP). J. Biol. Chem. 285, 11913-11921
45. Roychoudhuri, R., Hirahara, K., Mousavi, K., Clever, D., Klebanoff, C. A., Bonelli, M., Sciumé, G., Zare, H., Vahedi, G., Dema, B., Yu, Z., Liu, H., Takahashi, H., Rao, M., Muranski, P., et al. (2013) BACH2 represses effector programs to stabilize T(reg)-mediated immune homeostasis. Nature 498, 506-510
46. Tsukumo, S., Unno, M., Muto, A., Takeuchi, A., Kometani, K., Kurosaki, T., Igarashi, K., and Saito, T. (2013) Bach2 maintains T cells in a naive state by suppressing effector memory-related genes. Proc. Natl. Acad. Sci. U.S.A. 110, 10735-10740
47. Hu, G., and Chen, J. (2013) A genome-wide regulatory network identifies key transcription factors for memory CD8-T-cell development. Nat. Commun. 4, 2830
48. Kim, E. H., Gasper, D. J., Lee, S. H., Plisch, E. H., Svaren, J., and Suresh, M. (2014) Bach2 regulates homeostasis of Foxp3-regulatory T cells and protects against fatal lung disease in mice. J. Immunol. 192, 985-995
49. Kuwahara, M., Suzuki, J., Tofukuji, S., Yamada, T., Kanoh, M., Matsumoto, A., Maruyama, S., Kometani, K., Kurosaki, T., Ohara, O., Nakayama, T., and Yamashita, M. (2014) The Menin-Bach2 axis is critical for regulating CD4 T-cell senescence and cytokine homeostasis. Nat. Commun. 5, 3555
50. Vahedi, G., Kanno, Y., Furumoto, Y., Jiang, K., Parker, S. C., Erdos, M. R., Davis, S. R., Roychoudhuri, R., Restifo, N. P., Gadina, M., Tang, Z., Ruan, Y., Collins, F. S., Sartorelli, V., and O'Shea, J. J. (2015) Super-enhancers delineate disease-Associated regulatory nodes in T cells. Nature 520, 558-562
51. Nakamura, A., Ebina-Shibuya, R., Itoh-Nakadai, A., Muto, A., Shima, H., Saigusa, D., Aoki, J., Ebina, M., Nukiwa, T., and Igarashi, K. (2013) Transcription repressor Bach2 is required for pulmonary surfactant homeostasis and alveolar macrophage function. J. Exp. Med. 210, 2191-2204