Nuclear Receptors TR2 and TR4 Recruit Multiple Epigenetic Transcriptional Corepressors That Associate Specifically with the Embryonic β-Type Globin Promoters in Differentiated Adult Erythroid Cells

REFERENCES

• Aerbajinai, W., J. Zhu, C. Kumkhaek, K. Chin, and G. P. Rodgers. 2009. SCF induces γ-globin gene expression by regulating downstream transcription factor COUP-TFII. Blood 114:187–194.
   PubMedGoogle Scholar
• Banzon, V., et al. 2011. siDNMT1 increases γ-globin expression in chemical inducer of dimerization (CID)-dependent mouse βYAC bone marrow cells and in baboon erythroid progenitor cell cultures. Exp. Hematol. 39:26–36 e1.
   PubMedGoogle Scholar
• Borg, J., et al. 2010. Haploinsufficiency for the erythroid transcription factor KLF1 causes hereditary persistence of fetal hemoglobin. Nat. Genet. 42:801–805.
   PubMed Web of Science ®Google Scholar
• Bulger, M., et al. 2003. A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse β-globin locus. Mol. Cell. Biol. 23:5234–5244.
   PubMedGoogle Scholar
• Cao, H. 2004. Pharmacological induction of fetal hemoglobin synthesis using histone deacetylase inhibitors. Hematology 9:223–233.
   PubMedGoogle Scholar
• Chen, L. M., et al. 2008. Subfertility with defective folliculogenesis in female mice lacking testicular orphan nuclear receptor 4. Mol. Endocrinol. 22:858–867.
   PubMedGoogle Scholar
• de Boer, E., et al. 2003. Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 100:7480–7485.
   PubMed Web of Science ®Google Scholar
• Delcuve, G. P., M. Rastegar, and J. R. Davie. 2009. Epigenetic control. J. Cell Physiol. 219:243–250.
   PubMed Web of Science ®Google Scholar
• Fathallah, H., R. S. Weinberg, Y. Galperin, M. Sutton, and G. F. Atweh. 2007. Role of epigenetic modifications in normal globin gene regulation and butyrate-mediated induction of fetal hemoglobin. Blood 110:3391–3397.
   PubMed Web of Science ®Google Scholar
• Filipe, A., et al. 1999. Regulation of embryonic/fetal globin genes by nuclear hormone receptors: a novel perspective on hemoglobin switching. EMBO J. 18:687–697.
   PubMedGoogle Scholar
• Forsberg, E. C., et al. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. U. S. A. 97:14494–14499.
   PubMedGoogle Scholar
• Franco, P. J., M. Farooqui, E. Seto, and L. N. Wei. 2001. The orphan nuclear receptor TR2 interacts directly with both class I and class II histone deacetylases. Mol. Endocrinol. 15:1318–1328.
   PubMedGoogle Scholar
• Frietze, S., H. O'Geen, K. R. Blahnik, V. X. Jin, and P. J. Farnham. 2010. ZNF274 recruits the histone methyltransferase SETDB1 to the 3′ ends of ZNF genes. PLoS One 5:e15082.
   PubMedGoogle Scholar
• Fuks, F., W. A. Burgers, A. Brehm, L. Hughes-Davies, and T. Kouzarides. 2000. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat. Genet. 24:88–91.
   PubMed Web of Science ®Google Scholar
• Garcia-Bassets, I., et al. 2007. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128:505–518.
   PubMed Web of Science ®Google Scholar
• Giarratana, M. C., et al. 2005. Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat. Biotechnol. 23:69–74.
   PubMed Web of Science ®Google Scholar
• Glass, C. K., and M. G. Rosenfeld. 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14:121–141.
   PubMed Web of Science ®Google Scholar
• Goren, A., et al. 2006. Fine tuning of globin gene expression by DNA methylation. PLoS One 1:e46.
   PubMedGoogle Scholar
• Gupta, P., P. C. Ho, S. G. Ha, Y. W. Lin, and L. N. Wei. 2009. HDAC3 as a molecular chaperone for shuttling phosphorylated TR2 to PML: a novel deacetylase activity-independent function of HDAC3. PLoS One 4:e4363.
   PubMedGoogle Scholar
• Harju-Baker, S., F. C. Costa, H. Fedosyuk, R. Neades, and K. R. Peterson. 2008. Silencing of Aγ-globin gene expression during adult definitive erythropoiesis mediated by GATA-1-FOG-1-Mi2 complex binding at the −566 GATA site. Mol. Cell. Biol. 28:3101–3113.
   PubMed Web of Science ®Google Scholar
• Heinzel, T., et al. 1997. A complex containing N-CoR, mSin3, and histone deacetylase mediates transcriptional repression. Nature 387:43–48.
   PubMed Web of Science ®Google Scholar
• Hong, W., et al. 2005. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 24:2367–2378.
   PubMed Web of Science ®Google Scholar
• Hsu, M., R. Mabaera, C. H. Lowrey, D. I. Martin, and S. Fiering. 2007. CpG hypomethylation in a large domain encompassing the embryonic β-like globin genes in primitive erythrocytes. Mol. Cell. Biol. 27:5047–5054.
   PubMedGoogle Scholar
• Im, H., et al. 2003. Dynamic regulation of histone H3 methylated at lysine 79 within a tissue-specific chromatin domain. J. Biol. Chem. 278:18346–18352.
   PubMed Web of Science ®Google Scholar
• Ishitani, K., et al. 2003. p54nrb acts as a transcriptional coactivator for activation function 1 of the human androgen receptor. Biochem. Biophys. Res. Commun. 306:660–665.
   PubMedGoogle Scholar
• Jones, P. L., et al. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19:187–191.
   PubMed Web of Science ®Google Scholar
• Jung, D. J., S. Y. Na, D. S. Na, and J. W. Lee. 2002. Molecular cloning and characterization of CAPER, a novel coactivator of activating protein-1 and estrogen receptors. J. Biol. Chem. 277:1229–1234.
   PubMed Web of Science ®Google Scholar
• Khavari, P. A., C. L. Peterson, J. W. Tamkun, D. B. Mendel, and G. R. Crabtree. 1993. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:170–174.
   PubMed Web of Science ®Google Scholar
• Kiefer, C. M., C. Hou, J. A. Little, and A. Dean. 2008. Epigenetics of β-globin gene regulation. Mutat. Res. 647:68–76.
   PubMedGoogle Scholar
• Kim, E., et al. 2003. Disruption of TR4 orphan nuclear receptor reduces the expression of liver apolipoprotein E/C-I/C-II gene cluster. J. Biol. Chem. 278:46919–46926.
   PubMed Web of Science ®Google Scholar
• Kim, J. K., M. Samaranayake, and S. Pradhan. 2009. Epigenetic mechanisms in mammals. Cell. Mol. Life Sci. 66:596–612.
   PubMed Web of Science ®Google Scholar
• Kingsley, P. D., et al. 2006. “Maturational” globin switching in primary primitive erythroid cells. Blood 107:1665–1672.
   PubMedGoogle Scholar
• Le Douarin, B., et al. 1996. A possible involvement of TIF1α and TIF1β in the epigenetic control of transcription by nuclear receptors. EMBO J. 15:6701–6715.
   PubMed Web of Science ®Google Scholar
• Lee, C. H., C. Chinpaisal, and L. N. Wei. 1998. Cloning and characterization of mouse RIP140, a corepressor for nuclear orphan receptor TR2. Mol. Cell. Biol. 18:6745–6755.
   PubMed Web of Science ®Google Scholar
• Lee, C. H., C. Chinpaisal, and L. N. Wei. 1998. A novel nuclear receptor heterodimerization pathway mediated by orphan receptors TR2 and TR4. J. Biol. Chem. 273:25209–25215.
   PubMed Web of Science ®Google Scholar
• Lee, M. G., et al. 2006. Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26:6395–6402.
   PubMed Web of Science ®Google Scholar
• Lee, M. G., C. Wynder, N. Cooch, and R. Shiekhattar. 2005. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437:432–435.
   PubMed Web of Science ®Google Scholar
• Lee, Y. F., H. J. Lee, and C. Chang. 2002. Recent advances in the TR2 and TR4 orphan receptors of the nuclear receptor superfamily. J. Steroid Biochem. Mol. Biol. 81:291–308.
   PubMedGoogle Scholar
• Le Guezennec, X., et al. 2006. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol. Cell. Biol. 26:843–851.
   PubMed Web of Science ®Google Scholar
• Lehnertz, B., et al. 2003. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13:1192–1200.
   PubMed Web of Science ®Google Scholar
• Liu, N. C., et al. 2007. Loss of TR4 orphan nuclear receptor reduces phosphoenolpyruvate carboxykinase-mediated gluconeogenesis. Diabetes 56:2901–2909.
   PubMed Web of Science ®Google Scholar
• Lopez, R. A., S. Schoetz, K. DeAngelis, D. O'Neill, and A. Bank. 2002. Multiple hematopoietic defects and delayed globin switching in Ikaros null mice. Proc. Natl. Acad. Sci. U. S. A. 99:602–607.
   PubMedGoogle Scholar
• Mabaera, R., et al. 2007. Developmental- and differentiation-specific patterns of human γ- and β-globin promoter DNA methylation. Blood 110:1343–1352.
   PubMed Web of Science ®Google Scholar
• Marcus, S. J., T. R. Kinney, W. H. Schultz, E. E. O'Branski, and R. E. Ware. 1997. Quantitative analysis of erythrocytes containing fetal hemoglobin (F cells) in children with sickle cell disease. Am. J. Hematol. 54:40–46.
   PubMedGoogle Scholar
• Mathur, M., P. W. Tucker, and H. H. Samuels. 2001. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell. Biol. 21:2298–2311.
   PubMedGoogle Scholar
• Mazumdar, A., et al. 2001. Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat. Cell Biol. 3:30–37.
   PubMed Web of Science ®Google Scholar
• Metzger, E., et al. 2005. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437:436–439.
   PubMed Web of Science ®Google Scholar
• Miles, J., et al. 2007. Intergenic transcription, cell-cycle and the developmentally regulated epigenetic profile of the human β-globin locus. PLoS One 2:e630.
   PubMedGoogle Scholar
• Morimoto, R. I. 2002. Dynamic remodeling of transcription complexes by molecular chaperones. Cell 110:281–284.
   PubMedGoogle Scholar
• Nagy, L., et al. 1997. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89:373–380.
   PubMed Web of Science ®Google Scholar
• Nan, X., et al. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389.
   PubMed Web of Science ®Google Scholar
• Needham, M., et al. 1992. LCR/MEL: a versatile system for high-level expression of heterologous proteins in erythroid cells. Nucleic Acids Res. 20:997–1003.
   PubMed Web of Science ®Google Scholar
• Nielsen, A. L., et al. 1999. Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J. 18:6385–6395.
   PubMed Web of Science ®Google Scholar
• O'Geen, H., et al. 2010. Genome-wide binding of the orphan nuclear receptor TR4 suggests its general role in fundamental biological processes. BMC Genomics 11:689.
   PubMedGoogle Scholar
• Omori, A., O. Tanabe, J. D. Engel, A. Fukamizu, and K. Tanimoto. 2005. Adult stage γ-globin silencing is mediated by a promoter direct repeat element. Mol. Cell. Biol. 25:3443–3451.
   PubMed Web of Science ®Google Scholar
• Papadakis, M. N., G. P. Patrinos, P. Tsaftaridis, and A. Loutradi-Anagnostou. 2002. A comparative study of Greek nondeletional hereditary persistence of fetal hemoglobin and β-thalassemia compound heterozygotes. J. Mol. Med. 80:243–247.
   PubMed Web of Science ®Google Scholar
• Rambaud, J., J. Desroches, A. Balsalobre, and J. Drouin. 2009. TIF1β/KAP-1 is a coactivator of the orphan nuclear receptor NGFI-B/Nur77. J. Biol. Chem. 284:14147–14156.
   PubMedGoogle Scholar
• Robertson, K. D., et al. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338–342.
   PubMed Web of Science ®Google Scholar
• Rodriguez, P., et al. 2005. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24:2354–2366.
   PubMed Web of Science ®Google Scholar
• Rodriguez, P., et al. 2006. Isolation of transcription factor complexes by in vivo biotinylation tagging and direct binding to streptavidin beads. Methods Mol. Biol. 338:305–323.
   PubMedGoogle Scholar
• Rosenfeld, M. G., V. V. Lunyak, and C. K. Glass. 2006. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 20:1405–1428.
   PubMed Web of Science ®Google Scholar
• Rountree, M. R., K. E. Bachman, and S. B. Baylin. 2000. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet. 25:269–277.
   PubMed Web of Science ®Google Scholar
• Ryan, R. F., et al. 1999. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19:4366–4378.
   PubMed Web of Science ®Google Scholar
• Rybak, J. N., et al. 2005. In vivo protein biotinylation for identification of organ-specific antigens accessible from the vasculature. Nat. Methods 2:291–298.
   PubMed Web of Science ®Google Scholar
• Saleque, S., J. Kim, H. M. Rooke, and S. H. Orkin. 2007. Epigenetic regulation of hematopoietic differentiation by Gfi-1 and Gfi-1b is mediated by the cofactors CoREST and LSD1. Mol. Cell 27:562–572.
   PubMed Web of Science ®Google Scholar
• Sankaran, V. G., et al. 2011. MicroRNA-15a and -16-1 act via MYB to elevate fetal hemoglobin expression in human trisomy 13. Proc. Natl. Acad. Sci. U. S. A. 108:1519–1524.
   PubMed Web of Science ®Google Scholar
• Sankaran, V. G., et al. 2008. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322:1839–1842.
   PubMed Web of Science ®Google Scholar
• Saunthararajah, Y., D. Lavelle, and J. DeSimone. 2004. DNA hypo-methylating agents and sickle cell disease. Br. J. Haematol. 126:629–636.
   PubMed Web of Science ®Google Scholar
• Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850–858.
   PubMed Web of Science ®Google Scholar
• Shi, Y., et al. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953.
   PubMed Web of Science ®Google Scholar
• Shi, Y. J., et al. 2005. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 19:857–864.
   PubMed Web of Science ®Google Scholar
• Stamatoyannopoulos, G., and F. Grosveld. 2001. Hemoglobin switching, p. 135–182. In Stamatoyannopoulos, G., et al. (ed.), Molecular basis of blood diseases, 3rd ed. W. B. Saunders Publishing Company, Philadelphia, PA.
   Google Scholar
• Tanabe, O., et al. 2002. An embryonic/fetal β-type globin gene repressor contains a nuclear receptor TR2/TR4 heterodimer. EMBO J. 21:3434–3442.
   PubMed Web of Science ®Google Scholar
• Tanabe, O., et al. 2007. Embryonic and fetal β-globin gene repression by the orphan nuclear receptors, TR2 and TR4. EMBO J. 26:2295–2306.
   PubMed Web of Science ®Google Scholar
• Tanabe, O., et al. 2007. The TR2 and TR4 orphan nuclear receptors repress Gata1 transcription. Genes Dev. 21:2832–2844.
   PubMed Web of Science ®Google Scholar
• Tanimoto, K., Q. Liu, F. Grosveld, J. Bungert, and J. D. Engel. 2000. Context-dependent EKLF responsiveness defines the developmental specificity of the human ε-globin gene in erythroid cells of YAC transgenic mice. Genes Dev. 14:2778–2794.
   PubMedGoogle Scholar
• Tsai, N. P., et al. 2009. Activation of testicular orphan receptor 4 by fatty acids. Biochim. Biophys. Acta 1789:734–740.
   PubMedGoogle Scholar
• van Dijk, T. B., et al. 2010. Fetal globin expression is regulated by Friend of Prmt1. Blood 116:4349–4352.
   PubMed Web of Science ®Google Scholar
• Wang, J., et al. 2009. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat. Genet. 41:125–129.
   PubMed Web of Science ®Google Scholar
• Wang, J., et al. 2006. A protein interaction network for pluripotency of embryonic stem cells. Nature 444:364–368.
   PubMed Web of Science ®Google Scholar
• Wang, Y., et al. 2009. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138:660–672.
   PubMed Web of Science ®Google Scholar
• Wilson, A. C., K. LaMarco, M. G. Peterson, and W. Herr. 1993. The VP16 accessory protein HCF is a family of polypeptides processed from a large precursor protein. Cell 74:115–125.
   PubMed Web of Science ®Google Scholar
• Xie, S., et al. 2009. TR4 nuclear receptor functions as a fatty acid sensor to modulate CD36 expression and foam cell formation. Proc. Natl. Acad. Sci. U. S. A. 106:13353–13358.
   PubMedGoogle Scholar
• Xu, J., et al. 2010. Transcriptional silencing of γ-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev. 24:783–798.
   PubMed Web of Science ®Google Scholar
• Yang, X. J., and E. Seto. 2008. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell. Biol. 9:206–218.
   PubMed Web of Science ®Google Scholar
• Yi, Z., et al. 2006. Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet. 2:e14.
   PubMed Web of Science ®Google Scholar
• Yin, W., et al. 2007. Histone acetylation at the human β-globin locus changes with developmental age. Blood 110:4101–4107.
   PubMedGoogle Scholar
• Yokoyama, A., S. Takezawa, R. Schule, H. Kitagawa, and S. Kato. 2008. Transrepressive function of TLX requires the histone demethylase LSD1. Mol. Cell. Biol. 28:3995–4003.
   PubMed Web of Science ®Google Scholar
• Zeng, P. Y., C. R. Vakoc, Z. C. Chen, G. A. Blobel, and S. L. Berger. 2006. In vivo dual cross-linking for identification of indirect DNA-associated proteins by chromatin immunoprecipitation. Biotechniques 41:694–698.
   PubMed Web of Science ®Google Scholar
• Zhang, L. J., X. Liu, P. R. Gafken, C. Kioussi, and M. Leid. 2009. A chicken ovalbumin upstream promoter transcription factor I (COUP-TFI) complex represses expression of the gene encoding tumor necrosis factor α-induced protein 8 (TNFAIP8). J. Biol. Chem. 284:6156–6168.
   PubMedGoogle Scholar
• Zhang, Q., et al. 2005. STAT3- and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 102:6948–6953.
   PubMedGoogle Scholar
• Zhou, D., K. Liu, C. W. Sun, K. M. Pawlik, and T. M. Townes. 2010. KLF1 regulates BCL11A expression and γ- to β-globin gene switching. Nat. Genet. 42:742–744.
   PubMed Web of Science ®Google Scholar
• Zhou, X. E., et al. 2010. The orphan nuclear receptor TR4 is a vitamin A-activated nuclear receptor. J. Biol. Chem. 286:2877–2885.
   PubMedGoogle Scholar