Alternative splicing regulates Prdm1/Blimp-1 DNA binding activities and corepressor interactions

Molecular and Cellular Biology

Volumn 32, Issue 17, 2012, Pages 3403-3413

  Morgan, Marc A J ^a   Mould, Arne W ^a   Li, Li ^a   Robertson, Elizabeth J ^a   Bikoff, Elizabeth K ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; COREPRESSOR PROTEIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HYBRID PROTEIN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA BINDING; DNA SPLICING; EMBRYO; EMBRYONIC STEM CELL; EXON; FEMALE; GENE DELETION; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN INTERACTION; ZINC FINGER MOTIF;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; CO-REPRESSOR PROTEINS; DENDRITIC CELLS; DNA; EMBRYO, MAMMALIAN; EXONS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; MICE; MOLECULAR SEQUENCE DATA; PLASMA CELLS; PROTEIN BINDING; PROTEIN ISOFORMS; TRANSCRIPTION FACTORS;

MUS;

EID: 84866277623     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00174-12     Document Type: Article

References (86)

1. Ancelin K, et al. 2006. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol. 8:623-630.
2. Bickmore WA, et al. 1992. Modulation of DNA binding specificity by alternative splicing of the Wilms tumor wt1 gene transcript. Science 257: 235-237.
3. Bikoff EK, Morgan MA, Robertson EJ. 2009. An expanding job description for Blimp-1/PRDM1. Curr. Opin. Genet. Dev. 19:379-385.
4. Caballero R, et al. 2007. Combinatorial effects of splice variants modulate function of Aiolos. J. Cell Sci. 120:2619-2630.
5. Caricasole A, et al. 1996. RNA binding by the Wilms tumor suppressor zinc finger proteins. Proc. Natl. Acad. Sci. U. S. A. 93:7562-7566.
6. Chan YH, et al. 2009. Absence of the transcriptional repressor Blimp-1 in hematopoietic lineages reveals its role in dendritic cell homeostatic development and function. J. Immunol. 183:7039-7046.
7. Cobb BS, et al. 2000. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 14:2146-2160.
8. Costello I, et al. 2011. The T-box transcription factor Eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat. Cell Biol. 13:1084-1091.
9. D'Costa K, et al. 2009. Blimp1 is limiting for transformation in a mouse plasmacytoma model. Blood 113:5911-5919.
10. de la Mata M, et al. 2003. A slow RNA polymerase II affects alternative splicing in vivo. Mol. Cell 12:525-532.
11. DiFeo A, Martignetti JA, Narla G. 2009. The role of KLF6 and its splice variants in cancer therapy. Drug Resist. Updat. 12:1-7.
12. Doody GM, Stephenson S, McManamy C, Tooze RM. 2007. PRDM1/ BLIMP-1 modulates IFN-gamma-dependent control of the MHC class I antigen-processing and peptide-loading pathway. J. Immunol. 179:7614-7623.
13. Doody GM, et al. 2010. An extended set of PRDM1/BLIMP1 target genes links binding motif type to dynamic repression. Nucleic Acids Res. 38: 5336-5350.
14. Eckert D, et al. 2008. Expression of BLIMP1/PRMT5 and concurrent histone H2A/H4 arginine 3 dimethylation in fetal germ cells, CIS/IGCNU and germ cell tumors. BMC Dev. Biol. 8:106. doi:10.1186/1471-213X-8-106.
15. Fox AH, et al. 1999. Transcriptional cofactors of the FOG family interact with GATA proteins by means of multiple zinc fingers. EMBO J. 18:2812-2822.
16. Friesen WJ, et al. 2001. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 21:8289-8300.
17. Guderian G, et al. 2011. RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J. Biol. Chem. 286:1976-1986.
18. Gyory I, Fejer G, Ghosh N, Seto E, Wright KL. 2003. Identification of a functionally impaired positive regulatory domain I binding factor 1 transcription repressor in myeloma cell lines. J. Immunol. 170:3125-3133.
19. Gyory I, Wu J, Fejer G, Seto E, Wright KL. 2004. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 5:299-308.
20. Haber DA, et al. 1991. Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc. Natl. Acad. Sci. U. S. A. 88:9618-9622.
21. Hahm K, et al. 1994. The lymphoid transcription factor LyF-1 is encoded by specific, alternatively spliced mRNAs derived from the Ikaros gene. Mol. Cell. Biol. 14:7111-7123.
22. Harper J, Mould A, Andrews RM, Bikoff EK, Robertson EJ. 2011. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc. Natl. Acad. Sci. U. S. A. 108:10585-10590.
23. Hatayama M, et al. 2008. Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain. Hum. Mol. Genet. 17:3459-3473.
24. Hildebrand JD, Soriano P. 2002. Overlapping and unique roles for Cterminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol. Cell. Biol. 22:5296-5307.
25. Horsley V, et al. 2006. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126:597-609.
26. Inaba K, et al. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176:1693-1702.
27. Izutsu K, et al. 2001. The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling. Blood 97:2815-2822.
28. Kajimura S, et al. 2008. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 22:1397-1409.
29. Kallies A, et al. 2004. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200:967-977.
30. Kallies A, et al. 2006. Transcriptional repressor Blimp-1 is essential for T cell homeostasis and self-tolerance. Nat. Immunol. 7:466-474.
31. Kallies A, et al. 2007. Initiation of plasma-cell differentiation is independent of the transcription factor Blimp-1. Immunity 26:555-566.
32. Kallies A, Xin A, Belz GT, Nutt SL. 2009. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 31:283-295.
33. Kallies A, et al. 2011. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 117:1869-1879.
34. Keller AD, Maniatis T. 1991. Identification and characterization of a novel repressor of beta-interferon gene expression. Genes Dev. 5:868-879.
35. Keller AD, Maniatis T. 1992. Only two of the five zinc fingers of the eukaryotic transcriptional repressor PRDI-BF1 are required for sequencespecific DNA binding. Mol. Cell. Biol. 12:1940-1949.
36. Klug CA, et al. 1998. 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. 95:657-662.
37. Klug A. 2010. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79:213-231.
38. Kolasinska-Zwierz P, et al. 2009. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat. Genet. 41:376-381.
39. Kuo TC, Calame KL. 2004. B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites. J. Immunol. 173:5556-5563.
40. Laity JH, Lee BM, Wright PE. 2001. Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11: 39-46.
41. Larsson SH, et al. 1995. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 81: 391-401.
42. Lin Y, Wong K, Calame K. 1997. Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276:596-599.
43. Lin KI, Lin Y, Calame K. 2000. Repression of c-myc is necessary but not sufficient for terminal differentiation of B lymphocytes in vitro. Mol. Cell. Biol. 20:8684-8695.
44. Lin S, Coutinho-Mansfield G, Wang D, Pandit S, Fu XD. 2008. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15:819-826.
45. Luco RF, et al. 2010. Regulation of alternative splicing by histone modifications. Science 327:996-1000.
46. Magnusdottir E, et al. 2007. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. U. S. A. 104:14988-14993.
47. Maniatis T, Tasic B. 2002. Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418:236-243.
48. Martins GA, et al. 2006. Transcriptional repressor Blimp-1 regulates T cell homeostasis and function. Nat. Immunol. 7:457-465.
49. Martins GA, Cimmino L, Liao J, Magnusdottir E, Calame K. 2008. Blimp-1 directly represses Il2 and the Il2 activator Fos, attenuating T cell proliferation and survival. J. Exp. Med. 205:1959-1965.
50. Merkenschlager M. 2010. Ikaros in immune receptor signaling, lymphocyte differentiation, and function. FEBS Lett. 584:4910-4914.
51. Mingot JM, Vega S, Maestro B, Sanz JM, Nieto MA. 2009. Characterization of Snail nuclear import pathways as representatives of C2H2 zinc finger transcription factors. J. Cell Sci. 122:1452-1460.
52. Miranda TB, et al. 2004. Spliceosome Sm proteins D1, D3, and B/B= are asymmetrically dimethylated at arginine residues in the nucleus. Biochem. Biophys. Res. Commun. 323:382-387.
53. Miyauchi Y, et al. 2010. The Blimp1-Bcl6 axis is critical to regulate osteoclast differentiation and bone homeostasis. J. Exp. Med. 207:751-762.
54. Molnar A, Georgopoulos K. 1994. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol. Cell. Biol. 14:8292-8303.
55. Morgan MA, et al. 2009. Blimp-1/Prdm1 alternative promoter usage during mouse development and plasma cell differentiation. Mol. Cell. Biol. 29:5813-5827.
56. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457-463.
57. Nishikawa K, et al. 2010. Blimp1-mediated repression of negative regulators is required for osteoclast differentiation. Proc. Natl. Acad. Sci. U. S. A. 107:3117-3122.
58. Ohinata Y, et al. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207-213.
59. Pal S, et al. 2003. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23:7475-7487.
60. Patel SR, Bhumbra SS, Paknikar RS, Dressler GR. 2012. Epigenetic mechanisms of Groucho/Grg/TLE mediated transcriptional repression. Mol. Cell 45:185-195.
61. Perales R, Bentley D. 2009. "Cotranscriptionality" the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36:178-191.
62. Ren B, Chee KJ, Kim TH, Maniatis T. 1999. PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. Genes Dev. 13:125-137.
63. Rho J, et al. 2001. Prmt5, which forms distinct homo-oligomers, is a member of the protein-arginine methyltransferase family. J. Biol. Chem. 276:11393-11401.
64. Robertson EJ, et al. 2007. Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice. Development 134:4335-4345.
65. Rutishauser RL, et al. 2009. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31:296-308.
66. Schmidt D, et al. 2008. Blimp-1Deltaexon7: a naturally occurring Blimp-1 deletion mutant with auto-regulatory potential. Exp. Cell Res. 314:3614-3627.
67. Schreiber E, Matthias P, Muller MM, Schaffner W. 1989. Rapid detection of octamer binding proteins with 'mini-extracts,' prepared from a small number of cells. Nucleic Acids Res. 17:6419.
68. Shapiro-Shelef M, et al. 2003. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19:607-620.
69. Shi Y, et al. 2003. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422:735-738.
70. Shin H, et al. 2009. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 31: 309-320.
71. Sims RJ, 3rd, et al. 2007. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 28:665-676.
72. Smith MA, et al. 2010. PRDM1/Blimp-1 controls effector cytokine production in human NK cells. J. Immunol. 185:6058-6067.
73. Smith MA, et al. 2011. Positive regulatory domain I (PRDM1) and IRF8/ PU.1 counter-regulate MHC class II transactivator (CIITA) expression during dendritic cell maturation. J. Biol. Chem. 286:7893-7904.
74. Soriano P. 1997. The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124: 2691-2700.
75. Su ST, et al. 2009. Involvement of histone demethylase LSD1 in Blimp-1-mediated gene repression during plasma cell differentiation. Mol. Cell. Biol. 29:1421-1431.
76. Tachibana M, et al. 2005. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19:815-826.
77. Tan CP, Nakielny S. 2006. Control of the DNA methylation system component MBD2 by protein arginine methylation. Mol. Cell. Biol. 26: 7224-7235.
78. Tee WW, et al. 2010. Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev. 24: 2772-2777.
79. Teng Y, et al. 2007. AS1411 alters the localization of a complex containing protein arginine methyltransferase 5 and nucleolin. Cancer Res. 67: 10491-10500.
80. Tooze RM, Stephenson S, Doody GM. 2006. Repression of IFN-gamma induction of class II transactivator: a role for PRDM1/Blimp-1 in regulation of cytokine signaling. J. Immunol. 177:4584-4593.
81. Tunyaplin C, Shapiro MA, Calame KL. 2000. Characterization of the B lymphocyte-induced maturation protein-1 (Blimp-1) gene, mRNA isoforms and basal promoter. Nucleic Acids Res. 28:4846-4855.
82. Turner CA, Jr, Mack DH, Davis MM. 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.
83. Vincent SD, et al. 2005. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 132:1315-1325.
84. Wagner KD, Wagner N, Schedl A. 2003. The complex life of WT1. J. Cell Sci. 116:1653-1658.
85. Yu J, Angelin-Duclos C, Greenwood J, Liao J, Calame K. 2000. Transcriptional repression by Blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol. Cell. Biol. 20:2592-2603.
86. Yu W, Li R, Gui B, Shang Y. 2010. sZIP, an alternative splice variant of ZIP, antagonizes transcription repression and growth inhibition by ZIP. J. Biol. Chem. 285:14301-14307.