Formation of a Tissue-specific Histone Acetylation Pattern by the Hematopoietic Transcription Factor GATA-1

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2003 Jan 31

PMID 12556492

Citations 70

Authors

Danielle L Letting

Carrie Rakowski

Mitchell J Weiss

Gerd A Blobel

Affiliations

Soon will be listed here.

Abstract

One function of lineage-restricted transcription factors may be to control the formation of tissue-specific chromatin domains. In erythroid cells, the beta-globin gene cluster undergoes developmentally regulated hyperacetylation of histones at the active globin genes and the locus control region (LCR). However, it is unknown which transcription factor(s) governs the establishment of this erythroid-specific chromatin domain. We measured histone acetylation at the beta-globin locus in the erythroid cell line G1E, which is deficient for the essential hematopoietic transcription factor GATA-1. Restoration of GATA-1 activity in G1E cells led to a substantial increase in acetylation of histones H3 and H4 at the beta-globin promoter and the LCR. Time course experiments showed that histone acetylation occurred rapidly after GATA-1 activation and coincided with globin gene expression, indicating that the effects of GATA-1 are direct. Moreover, increases in histone acetylation correlated with occupancy of GATA-1 and the acetyltransferase CBP at the locus in vivo. Together, these results suggest that GATA-1 and its cofactor CBP are essential for the formation of an erythroid-specific acetylation pattern that is permissive for high levels of gene expression.

Citing Articles

HIC2 controls developmental hemoglobin switching by repressing BCL11A transcription.

Huang P, Peslak S, Ren R, Khandros E, Qin K, Keller C Nat Genet. 2022; 54(9):1417-1426.

PMID: 35941187 PMC: 9940634. DOI: 10.1038/s41588-022-01152-6.

Epigenetic and Transcriptional Control of Erythropoiesis.

Wells M, Steiner L Front Genet. 2022; 13:805265.

PMID: 35330735 PMC: 8940284. DOI: 10.3389/fgene.2022.805265.

Hemogen/BRG1 cooperativity modulates promoter and enhancer activation during erythropoiesis.

Guo X, Zhao Y, Kim J, Dean A Blood. 2022; 139(24):3532-3545.

PMID: 35297980 PMC: 9203704. DOI: 10.1182/blood.2021014308.

Molecular Landscapes and Models of Acute Erythroleukemia.

Fagnan A, Pique-Borras M, Tauchmann S, Mercher T, Schwaller J Hemasphere. 2021; 5(5):e558.

PMID: 33898929 PMC: 8061683. DOI: 10.1097/HS9.0000000000000558.

Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi.

Pfannmuller A, Leufken J, Studt L, Michielse C, Sieber C, Guldener U PLoS One. 2017; 12(4):e0176194.

PMID: 28441411 PMC: 5404775. DOI: 10.1371/journal.pone.0176194.

References

Zhang W, Bieker J . Acetylation and modulation of erythroid Krüppel-like factor (EKLF) activity by interaction with histone acetyltransferases. Proc Natl Acad Sci U S A. 1998; 95(17):9855-60. PMC: 21426. DOI: 10.1073/pnas.95.17.9855. View

Cheng X, Reginato M, Andrews N, Lazar M . The transcriptional integrator CREB-binding protein mediates positive cross talk between nuclear hormone receptors and the hematopoietic bZip protein p45/NF-E2. Mol Cell Biol. 1997; 17(3):1407-16. PMC: 231865. DOI: 10.1128/MCB.17.3.1407. View

Tsang A, Visvader J, Turner C, Fujiwara Y, Yu C, Weiss M . FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell. 1997; 90(1):109-19. DOI: 10.1016/s0092-8674(00)80318-9. View

Blobel G, Nakajima T, Eckner R, Montminy M, Orkin S . CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc Natl Acad Sci U S A. 1998; 95(5):2061-6. PMC: 19248. DOI: 10.1073/pnas.95.5.2061. View

Reik A, Telling A, Zitnik G, Cimbora D, Epner E, Groudine M . The locus control region is necessary for gene expression in the human beta-globin locus but not the maintenance of an open chromatin structure in erythroid cells. Mol Cell Biol. 1998; 18(10):5992-6000. PMC: 109185. DOI: 10.1128/MCB.18.10.5992. View

Higgs D . Do LCRs open chromatin domains?. Cell. 1998; 95(3):299-302. DOI: 10.1016/s0092-8674(00)81761-4. View

Gregory T, Yu C, Ma A, Orkin S, Blobel G, Weiss M . GATA-1 and erythropoietin cooperate to promote erythroid cell survival by regulating bcl-xL expression. Blood. 1999; 94(1):87-96. View

Forsberg E, Johnson K, Zaboikina T, Mosser E, Bresnick E . Requirement of an E1A-sensitive coactivator for long-range transactivation by the beta-globin locus control region. J Biol Chem. 1999; 274(38):26850-9. DOI: 10.1074/jbc.274.38.26850. View

Blobel G . CREB-binding protein and p300: molecular integrators of hematopoietic transcription. Blood. 2000; 95(3):745-55. View

10.

Engel J, Tanimoto K . Looping, linking, and chromatin activity: new insights into beta-globin locus regulation. Cell. 2000; 100(5):499-502. DOI: 10.1016/s0092-8674(00)80686-8. View

11.

Schubeler D, Francastel C, Cimbora D, Reik A, Martin D, Groudine M . Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev. 2000; 14(8):940-50. PMC: 316536. View

12.

Bender M, Bulger M, Close J, Groudine M . Beta-globin gene switching and DNase I sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol Cell. 2000; 5(2):387-93. DOI: 10.1016/s1097-2765(00)80433-5. View

13.

Forsberg E, Downs K, Christensen H, Im H, Nuzzi P, Bresnick E . Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc Natl Acad Sci U S A. 2000; 97(26):14494-9. PMC: 18947. DOI: 10.1073/pnas.97.26.14494. View

14.

Shang Y, Hu X, DiRenzo J, Lazar M, Brown M . Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell. 2001; 103(6):843-52. DOI: 10.1016/s0092-8674(00)00188-4. View

15.

Hung H, Kim A, Hong W, Rakowski C, Blobel G . Stimulation of NF-E2 DNA binding by CREB-binding protein (CBP)-mediated acetylation. J Biol Chem. 2001; 276(14):10715-21. DOI: 10.1074/jbc.M007846200. View

16.

Litt M, Simpson M, Recillas-Targa F, Prioleau M, Felsenfeld G . Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 2001; 20(9):2224-35. PMC: 125441. DOI: 10.1093/emboj/20.9.2224. View

17.

Myers F, Evans D, Clayton A, Thorne A, Crane-Robinson C . Targeted and extended acetylation of histones H4 and H3 at active and inactive genes in chicken embryo erythrocytes. J Biol Chem. 2001; 276(23):20197-205. DOI: 10.1074/jbc.M009472200. View

18.

Marmorstein R . Structure of histone acetyltransferases. J Mol Biol. 2001; 311(3):433-44. DOI: 10.1006/jmbi.2001.4859. View

19.

Johnson K, Christensen H, Zhao B, Bresnick E . Distinct mechanisms control RNA polymerase II recruitment to a tissue-specific locus control region and a downstream promoter. Mol Cell. 2001; 8(2):465-71. DOI: 10.1016/s1097-2765(01)00309-4. View

20.

Schubeler D, Groudine M, Bender M . The murine beta-globin locus control region regulates the rate of transcription but not the hyperacetylation of histones at the active genes. Proc Natl Acad Sci U S A. 2001; 98(20):11432-7. PMC: 58747. DOI: 10.1073/pnas.201394698. View