Derepression of the DNA Methylation Machinery of the Gata1 Gene Triggers the Differentiation Cue for Erythropoiesis

REFERENCES

• Takahashi S, Onodera K, Motohashi H, Suwabe N, Hayashi N, Yanai N, Nabesima Y, Yamamoto M. 1997. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem 272:12611–12615. https://doi.org/10.1074/jbc.272.19.12611.
   PubMed Web of Science ®Google Scholar
• Takahashi S, Komeno T, Suwabe N, Yoh K, Nakajima O, Nishimura S, Kuroha T, Nagasawa T, Yamamoto M. 1998. Role of GATA-1 in proliferation and differentiation of definitive erythroid and megakaryocytic cells in vivo. Blood 92:434–442.
   PubMed Web of Science ®Google Scholar
• Zon LI, Yamaguchi Y, Yee K, Albee EA, Kimura A, Bennett JC, Orkin SH, Ackerman SJ. 1993. Expression of mRNA for the GATA-binding proteins in human eosinophils and basophils: potential role in gene transcription. Blood 81:3234–3241.
   PubMedGoogle Scholar
• Martin DI, Zon LI, Mutter G, Orkin SH. 1990. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature 344:444–447. https://doi.org/10.1038/344444a0.
   PubMed Web of Science ®Google Scholar
• Shimizu R, Engel JD, Yamamoto M. 2008. GATA1-related leukaemias. Nat Rev Cancer 8:279–287. https://doi.org/10.1038/nrc2348.
   PubMedGoogle Scholar
• Shimizu R, Yamamoto M. 2012. Contribution of GATA1 dysfunction to multi-step leukemogenesis. Cancer Sci 103:2039–2044. https://doi.org/10.1111/cas.12007.
   PubMed Web of Science ®Google Scholar
• Hasegawa A, Kaneko H, Ishihara D, Nakamura M, Watanabe A, Yamamoto M, Trainor CD, Shimizu R. 2016. GATA1 binding kinetics on conformation-specific binding sites elicit differential transcriptional regulation. Mol Cell Biol 36:2151–2167. https://doi.org/10.1128/MCB.00017-16.
   PubMedGoogle Scholar
• Toki T, Kanezaki R, Kobayashi E, Kaneko H, Suzuki M, Wang R, Terui K, Kanegane H, Maeda M, Endo M, Mizuochi T, Adachi S, Hayashi Y, Yamamoto M, Shimizu R, Ito E. 2013. Naturally occurring oncogenic GATA1 mutants with internal deletions in transient abnormal myelopoiesis in Down syndrome. Blood 121:3181–3184. https://doi.org/10.1182/blood-2012-01-405746.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Suwabe N, Ohneda O, Obara N, Imagawa S, Pan X, Motohashi H, Yamamoto M. 2003. Identification and characterization of 2 types of erythroid progenitors that express GATA-1 at distinct levels. Blood 102:3575–3583. https://doi.org/10.1182/blood-2003-04-1154.
   PubMed Web of Science ®Google Scholar
• Suzuki M, Moriguchi T, Ohneda K, Yamamoto M. 2009. Differential contribution of the Gata1 gene hematopoietic enhancer to erythroid differentiation. Mol Cell Biol 29:1163–1175. https://doi.org/10.1128/MCB.01572-08.
   PubMedGoogle Scholar
• Tsai SF, Strauss E, Orkin SH. 1991. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev 5:919–931. https://doi.org/10.1101/gad.5.6.919.
   PubMed Web of Science ®Google Scholar
• Onodera K, Takahashi S, Nishimura S, Ohta J, Motohashi H, Yomogida K, Hayashi N, Engel JD, Yamamoto M. 1997. GATA-1 transcription is controlled by distinct regulatory mechanisms during primitive and definitive erythropoiesis. Proc Natl Acad Sci U S A 94:4487–4492. https://doi.org/10.1073/pnas.94.9.4487.
   PubMedGoogle Scholar
• Nishimura S, Takahashi S, Kuroha T, Suwabe N, Nagasawa T, Trainor C, Yamamoto M. 2000. A GATA box in the GATA-1 gene hematopoietic enhancer is a critical element in the network of GATA factors and sites that regulate this gene. Mol Cell Biol 20:713–723. https://doi.org/10.1128/MCB.20.2.713-723.2000.
   PubMedGoogle Scholar
• Ohneda K, Shimizu R, Nishimura S, Muraosa Y, Takahashi S, Engel JD, Yamamoto M. 2002. A minigene containing four discrete cis elements recapitulates GATA-1 gene expression in vivo. Genes Cells 7:1243–1254. https://doi.org/10.1046/j.1365-2443.2002.00595.x.
   PubMedGoogle Scholar
• Moriguchi T, Suzuki M, Yu L, Takai J, Ohneda K, Yamamoto M. 2015. Progenitor stage-specific activity of a cis-acting double GATA motif for Gata1 gene expression. Mol Cell Biol 35:805–815. https://doi.org/10.1128/MCB.01011-14.
   PubMedGoogle Scholar
• Suzuki N, Ohneda O, Minegishi N, Nishikawa M, Ohta T, Takahashi S, Engel JD, Yamamoto M. 2006. Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci U S A 103:2202–2207. https://doi.org/10.1073/pnas.0508928103.
   PubMedGoogle Scholar
• Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH, Engel JD. 1990. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 4:1650–1662. https://doi.org/10.1101/gad.4.10.1650.
   PubMed Web of Science ®Google Scholar
• Tsai FY, Orkin SH. 1997. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 89:3636–3643.
   PubMed Web of Science ®Google Scholar
• Minegishi N, Suzuki N, Yokomizo T, Pan X, Fujimoto T, Takahashi S, Hara T, Miyajima A, Nishikawa S, Yamamoto M. 2003. Expression and domain-specific function of GATA-2 during differentiation of the hematopoietic precursor cells in midgestation mouse embryos. Blood 102:896–905. https://doi.org/10.1182/blood-2002-12-3809.
   PubMed Web of Science ®Google Scholar
• Lim KC, Hosoya T, Brandt W, Ku CJ, Hosoya-Ohmura S, Camper SA, Yamamoto M, Engel JD. 2012. Conditional Gata2 inactivation results in HSC loss and lymphatic mispatterning. J Clin Invest 122:3705–3717. https://doi.org/10.1172/JCI61619.
   PubMed Web of Science ®Google Scholar
• de Pater E, Kaimakis P, Vink CS, Yokomizo T, Yamada-Inagawa T, van der Linden R, Kartalaei PS, Camper SA, Speck N, Dzierzak E. 2013. Gata2 is required for HSC generation and survival. J Exp Med 210:2843–2850. https://doi.org/10.1084/jem.20130751.
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Suzuki M, Otsuki A, Shimizu R, Bresnick EH, Engel JD, Yamamoto M. 2014. A remote GATA2 hematopoietic enhancer drives leukemogenesis in inv(3)(q21;q26) by activating EVI1 expression. Cancer Cell 25:415–427. https://doi.org/10.1016/j.ccr.2014.02.008.
   PubMed Web of Science ®Google Scholar
• Ohneda K, Yamamoto M. 2002. Roles of hematopoietic transcription factors GATA-1 and GATA-2 in the development of red blood cell lineage. Acta Haematol 108:237–245. https://doi.org/10.1159/000065660.
   PubMed Web of Science ®Google Scholar
• Kaneko H, Shimizu R, Yamamoto M. 2010. GATA factor switching during erythroid differentiation. Curr Opin Hematol 17:163–168. https://doi.org/10.1097/MOH.0b013e32833800b8.
   PubMed Web of Science ®Google Scholar
• Bresnick EH, Lee HY, Fujiwara T, Johnson KD, Keles S. 2010. GATA switches as developmental drivers. J Biol Chem 285:31087–31093. https://doi.org/10.1074/jbc.R110.159079.
   PubMed Web of Science ®Google Scholar
• Suzuki M, Shimizu R, Yamamoto M. 2011. Transcriptional regulation by GATA1 and GATA2 during erythropoiesis. Int J Hematol 93:150–155. https://doi.org/10.1007/s12185-011-0770-6.
   PubMedGoogle Scholar
• Suzuki M, Kobayashi-Osaki M, Tsutsumi S, Pan X, Ohmori S, Takai J, Moriguchi T, Ohneda O, Ohneda K, Shimizu R, Kanki Y, Kodama T, Aburatani H, Yamamoto M. 2013. GATA factor switching from GATA2 to GATA1 contributes to erythroid differentiation. Genes Cells 18:921–933. https://doi.org/10.1111/gtc.12086.
   PubMedGoogle Scholar
• Shimizu R, Yamamoto M. 2016. GATA-related hematologic disorders. Exp Hematol 44:696–705. https://doi.org/10.1016/j.exphem.2016.05.010.
   PubMed Web of Science ®Google Scholar
• Takai J, Moriguchi T, Suzuki M, Yu L, Ohneda K, Yamamoto M. 2013. The Gata1 5′ region harbors distinct cis-regulatory modules that direct gene activation in erythroid cells and gene inactivation in HSCs. Blood 122:3450–3460. https://doi.org/10.1182/blood-2013-01-476911.
   PubMedGoogle Scholar
• Moriguchi T, Yamamoto M. 2014. A regulatory network governing Gata1 and Gata2 gene transcription orchestrates erythroid lineage differentiation. Int J Hematol 100:417–424. https://doi.org/10.1007/s12185-014-1568-0.
   PubMed Web of Science ®Google Scholar
• Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109–1121. https://doi.org/10.1016/j.cell.2005.05.026.
   PubMed Web of Science ®Google Scholar
• Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, Dausman J, Lee P, Wilson C, Lander E, Jaenisch R. 2001. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 27:31–39. https://doi.org/10.1038/83730.
   PubMed Web of Science ®Google Scholar
• Socolovsky M, Nam H, Fleming MD, Haase VH, Brugnara C, Lodish HF. 2001. Ineffective erythropoiesis in Stat5a(−/−)5b(−/−) mice due to decreased survival of early erythroblasts. Blood 98:3261–3273. https://doi.org/10.1182/blood.V98.12.3261.
   PubMed Web of Science ®Google Scholar
• Richmond TD, Chohan M, Barber DL. 2005. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol 15:146–155. https://doi.org/10.1016/j.tcb.2005.01.007.
   PubMed Web of Science ®Google Scholar
• Munugalavadla V, Dore LC, Tan BL, Hong L, Vishnu M, Weiss MJ, Kapur R. 2005. Repression of c-kit and its downstream substrates by GATA-1 inhibits cell proliferation during erythroid maturation. Mol Cell Biol 25:6747–6759. https://doi.org/10.1128/MCB.25.15.6747-6759.2005.
   PubMed Web of Science ®Google Scholar
• Broudy VC. 1997. Stem cell factor and hematopoiesis. Blood 90:1345–1364.
   PubMed Web of Science ®Google Scholar
• Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 25:338–342. https://doi.org/10.1038/77124.
   PubMed Web of Science ®Google Scholar
• Li J. 2013. Myelodysplastic syndrome hematopoietic stem cell. Int J Cancer 133:525–533. https://doi.org/10.1002/ijc.27896.
   PubMed Web of Science ®Google Scholar
• Kerbauy DB, Deeg HJ. 2007. Apoptosis and antiapoptotic mechanisms in the progression of myelodysplastic syndrome. Exp Hematol 35:1739–1746. https://doi.org/10.1016/j.exphem.2007.09.007.
   PubMed Web of Science ®Google Scholar
• Maratheftis CI, Bolaraki PE, Voulgarelis M. 2007. GATA-1 transcription factor is up-regulated in bone marrow hematopoietic progenitor CD34(+) and erythroid CD71(+) cells in myelodysplastic syndromes. Am J Hematol 82:887–892. https://doi.org/10.1002/ajh.20993.
   PubMedGoogle Scholar
• Yu L, Moriguchi T, Souma T, Takai J, Satoh H, Morito N, Engel JD, Yamamoto M. 2014. GATA2 regulates body water homeostasis through maintaining aquaporin 2 expression in renal collecting ducts. Mol Cell Biol 34:1929–1941. https://doi.org/10.1128/MCB.01659-13.
   PubMedGoogle Scholar
• Katsuoka F, Yokozawa J, Tsuda K, Ito S, Pan X, Nagasaki M, Yasuda J, Yamamoto M. 2014. An efficient quantitation method of next-generation sequencing libraries by using MiSeq sequencer. Anal Biochem 466:27–29. https://doi.org/10.1016/j.ab.2014.08.015.
   PubMed Web of Science ®Google Scholar
• Yi Z, Cohen-Barak O, Hagiwara N, Kingsley PD, Fuchs DA, Erickson DT, Epner EM, Palis J, Brilliant MH. 2006. Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet 2:e14. https://doi.org/10.1371/journal.pgen.0020014.
   PubMed Web of Science ®Google Scholar
• Wu LC, Sun CW, Ryan TM, Pawlik KM, Ren J, Townes TM. 2006. Correction of sickle cell disease by homologous recombination in embryonic stem cells. Blood 108:1183–1188. https://doi.org/10.1182/blood-2006-02-004812.
   PubMed Web of Science ®Google Scholar
• Gregory RC, Taxman DJ, Seshasayee D, Kensinger MH, Bieker JJ, Wojchowski DM. 1996. Functional interaction of GATA1 with erythroid Kruppel-like factor and Sp1 at defined erythroid promoters. Blood 87:1793–1801.
   PubMedGoogle Scholar