Acetylation of EKLF is essential for epigenetic modification and transcriptional activation of the β-globin locus

Molecular and Cellular Biology

Volumn 28, Issue 20, 2008, Pages 6160-6170

  Sengupta, Tanushri ^a   Chen, Ken ^a   Milot, Eric ^b   Bieker, James J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; ERYTHROID KRUPPEL LIKE FACTOR; HISTONE H3; LYSINE;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA MODIFICATION; GENE LOCUS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; RETROVIRUS INFECTION; ZINC FINGER MOTIF;

ACETYLATION; ANIMALS; CELL LINE; CELL MEMBRANE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; EPIGENESIS, GENETIC; ERYTHROID CELLS; GLOBINS; HISTONES; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LYSINE; MICE; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; TRANS-ACTIVATION (GENETICS); ZINC FINGERS;

EID: 53549113643     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00919-08     Document Type: Article

References (77)

1. Ahmad, K., and S. Henikoff. 2002. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9:1191-1200.
2. min globin gene expression. Genomics 63:417-424.
3. Alevizopoulos, A., Y. Dusserre, M. Tsai-Pflugfelder, T. von der Weid, W. Wahli, and N. Mermod. 1995. Aproline-rich TGF-beta-responsive transcriptional activator interacts with histone H3. Genes Dev. 9:3051-3066.
4. Armstrong, J. A., J. J. Bieker, and B. M. Emerson. 1998. A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLF in vitro. Cell 95:93-104.
5. Blobel, G. A. 2002. CBP and p300: versatile coregulators with important roles in hematopoietic gene expression. J. Leukoc. Biol. 71:545-556.
6. Bottardi, S., A. Aumont, F. Grosveld, and E. Milot. 2003. Developmental stage-specific epigenetic control of human beta-globin gene expression is potentiated in hematopoietic progenitor cells prior to their transcriptional activation. Blood 102:3989-3997.
7. Bottardi, S., J. Ross, N. Pierre-Charles, V. Blank, and E. Milot. 2006. Lineage-specific activators affect beta-globin locus chromatin in multipotent hematopoietic progenitors. EMBO J. 25:3586-3595.
8. Bouilloux, F., G. Juban, N. Cohet, D. Buet, B. Guyot, W. Vainchenker, F. Louache, and F. Morle. 2008. EKLF restricts megakaryocytic differentiation at the benefit of erythrocytic differentiation. Blood 112:576-584.
9. Bresnick, E. H., K. D. Johnson, S. I. Kim, and H. Im. 2006. Establishment and regulation of chromatin domains: mechanistic insights from studies of hemoglobin synthesis. Prog. Nucleic Acid Res. Mol. Biol. 81:435-471.
10. Brown, R. C., S. Pattison, J. van Ree, E. Coghill, A. Perkins, S. M. Jane, and J. M. Cunningham. 2002. Distinct domains of erythroid Kruppel-like factor modulate chromatin remodeling and transactivation at the endogenous β-globin gene promoter. Mol. Cell. Biol. 22:161-170.
11. Bultman, S. J., T. C. Gebuhr, and T. Magnuson. 2005. A Brgl mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SWI/SNF-related complexes in beta-globin expression and erythroid development. Genes Dev. 19:2849-2861.
12. Chen, X., and J. J. Bieker. 2004. Stage-specific repression by the EKLF transcriptional activator. Mol. Cell. Biol. 24:10416-10424.
13. Chow, C. M., A. Georgiou, H. Szutorisz, A. Maia e Silva, A. Pombo, I. Barahona, E. Dargelos, C. Canzonetta, and N. Dillon. 2005. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep. 6:354-360.
14. Coghill, E., S. Eccleston, V. Fox, L. Cerruti, C. Brown, J. Cunningham, S. Jane, and A. Perkins. 2001. Erythroid Kruppel-like factor (EKLF) coordinates erythroid cell proliferation and hemoglobinization in cell lines derived from EKLF null mice. Blood 97:1861-1868.
15. Cosma, M. P. 2002. Ordered recruitment: gene-specific mechanism of transcription activation. Mol. Cell 10:227-236.
16. Daury, L., C. Chailleux, J. Bonvallet, and D. Trouche. 2006. Histone H3.3 deposition at E2F-regulated genes is linked to transcription. EMBO Rep. 7:66-71.
17. Dean, A. 2006. On a chromosome far, far away: LCRs and gene expression. Trends Genet. 22:38-45.
18. de Laat, W., P. Klous, J. Kooren, D. Noordermeer, R. J. Palstra, M. Simonis, E. Splinter, and F. Grosveld. 2008. Three-dimensional organization of gene expression in erythroid cells. Curr. Top. Dev. Biol. 82:117-139.
19. Drissen, R., R. J. Palstra, N. Gillemans, E. Splinter, F. Grosveld, S. Philipsen, and W. de Laat. 2004. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev. 18:2485-2490.
20. Drissen, R., M. von Lindern, A. Kolbus, S. Driegen, P. Steinlein, H. Beug, F. Grosveld, and S. Philipsen. 2005. The erythroid phenotype of EKLF-null mice: defects in hemoglobin metabolism and membrane stability. Mol. Cell. Biol. 25:5205-5214.
21. Fabian, I., and Z. Williams. 1988. The effect of deoxycoformycin on bone marrow cells treated with adenosine and deoxyadenosine and hemopoietic growth factors. Hum. Immunol. 21:81-87.
22. Frontelo, P., D. Manwani, M. Galdass, H. Karsunky, F. Lohmann, P. G. Gallagher, and J. J. Bieker. 2007. Novel role for EKLF in megakaryocyte lineage commitment. Blood 110:3871-3880.
23. Fu, X. H., D. P. Liu, and C. C. Liang. 2002. Chromatin structure and transcriptional regulation of the beta-globin locus. Exp. Cell Res. 278:1-11.
24. Funnell, A. P., C. A. Maloney, L. J. Thompson, J. Keys, M. Tallack, A. C. Perkins, and M. Crossley. 2007. Erythroid Kruppel-like factor directly activates the basic Kruppel-like factor gene in erythroid cells. Mol. Cell. Biol. 27:2777-2790.
25. Griffin, C. T., J. Brennan, and T. Magnuson. 2008. The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development. Development 135:493-500.
26. Gurbuxani, S., Y. Xu, G. Keerthivasan, A. Wickrema, and J. D. Crispino. 2005. Differential requirements for survivin in hematopoietic cell development. Proc. Natl. Acad. Sci. USA 102:11480-11485.
27. Hodge, D., E. Coghill, J. Keys, T. Maguire, B. Hartmann, A. McDowall, M. Weiss, S. Grimmond, and A. Perkins. 2006. A global role for EKLF in definitive and primitive erythropoiesis. Blood 107:3359-3370.
28. Im, H., J. A. Grass, K. D. Johnson, S. I. Kim, M. E. Boyer, A. N. Imbalzano, J. J. Bieker, and E. H. Bresnick. 2005. Chromatin domain activation via GATA-1 utilization of a small subset of dispersed GATA motifs within a broad chromosomal region. Proc. Natl. Acad. Sci. USA 102:17065-17070.
29. Jimenez, G., S. D. Griffiths, A. M. Ford, M. F. Greaves, and T. Enver. 1992. Activation of the beta-globin locus control region precedes commitment to the eiythroid lineage. Proc. Natl. Acad. Sci. USA 89:10618-10622.
30. Jin, C., and G. Felsenfeld. 2006. Distribution of histone H3.3 in hematopoietic cell lineages. Proc. Natl. Acad. Sci. USA 103:574-579.
31. Jin, C., and G. Felsenfeld. 2007. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 21:1519-1529.
32. Johnson, K. D., M. E. Boyer, J. A. Kang, A. Wickrema, A. B. Cantor, and E. H. Bresnick. 2007. Friend of GATA-1-independent transcriptional repression: a novel mode of GATA-1 function. Blood 109:5230-5233.
33. Kadam, S., and B. M. Emerson. 2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11:377-389.
34. Kadam, S., G. S. McAlpine, M. L. Phelan, R. E. Kingston, K. A. Jones, and B. M. Emerson. 2000. Functional selectivity of recombinant mammalian SWI/SNF subunits. Genes Dev. 14:2441-2451.
35. Kadonaga, J. T. 1998. Eukaryotic transcription: an interlaced network of transcription factors and chromatin-modifying machines. Cell 92:307-313.
36. Kouzarides, T. 2000. Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 19:1176-1179.
37. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
38. Lamonica, J. M., C. R. Vakoc, and G. A. Blobel. 2006. Acetylation of GATA-1 is required for chromatin occupancy. Blood 108:3736-3738.
39. Lemon, B., and R. Tjian. 2000. Orchestrated response: a symphony of transcription factors for gene control. Genes Dev. 14:2551-2569.
40. Lohmann, F., and J. J. Bieker. 2008. Activation of Eklf expression during hematopoiesis by Gata2 and Smad5 prior to eiythroid commitment. Development 135:2071-2082.
41. Loyola, A., and G. Almouzni. 2007. Marking histone H3 variants: how, when and why? Trends Biochem. Sci. 32:425-4-33.
42. Luo, J., M. Li, Y. Tang, M. Laszkowska, R. G. Roeder, and W. Gu. 2004. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc. Natl. Acad. Sci. USA 101:2259-2264.
43. Ma, K, J. K. Chan, G. Zhu, and Z. Wu. 2005. Myocyte enhancer factor 2 acetylation by p300 enhances its DNA binding activity, transcriptional activity, and myogenic differentiation. Mol. Cell. Biol. 25:3575-3582.
44. Mahajan, M. C., S. Karmakar, and S. M. Weissman. 2007. Control of beta globin genes. J. Cell. Biochem. 102:801-810.
45. Mahajan, M. C., and S. M. Weissman. 2006. Multi-protein complexes at the beta-globin locus. Brief. Funct. Genomic. Proteomic. 5:62-65.
46. McArthur, M., S. Gerum, and G. Stamatoyannopoulos. 2001. Quantification of DNaseI-sensitivity by real-time PCR: quantitative analysis of DNaseI-hypersensitivity of the mouse beta-globin LCR. J. Mol. Biol. 313:27-34.
47. McKittrick, E., P. R. Gafken, K. Ahmad, and S. Henikoff. 2004. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101:1525-1530.
48. Mellor, J. 2005. The dynamics of chromatin remodeling at promoters. Mol. Cell 19:147-157.
49. Miller, I. J., and J. J. Bieker. 1993. A novel, eiythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Kruppel family of nuclear proteins. Mol. Cell. Biol. 13:2776-2786.
50. Mo, X., E. Kowenz-Leutz, Y. Laumonnier, H. Xu, and A. Leutz. 2005. Histone H3 tail positioning and acetylation by the c-Myb but not the v-Myb DNA-binding SANT domain. Genes Dev. 19:2447-2457.
51. Montes de Oca, R., K. K Lee, and K. L. Wilson. 2005. Binding of barrier to autointegration factor (BAF) to histone H3 and selected linker histones including H1.1. J. Biol. Chem. 280:42252-42262.
52. Naar, A. M., P. A. Beaurang, K. M. Robinson, J. D. Oliner, D. Avizonis, S. Scheek, J. Zwicker, J. T. Kadonaga, and R. Tjian. 1998. Chromatin, TAFs, and a novel multiprotein coactivator are required for synergistic activation by Sp1 and SREBP-1a in vitro. Genes Dev. 12:3020-3031.
53. Naviaux, R. K., E. Costanzi, M. Haas, and I. M. Verma. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701-5705.
54. Nuez, B., D. Michalovich, A. Bygrave, R. Ploemacher, and F. Grosveld. 1995. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375:316-318.
55. Oike, Y., N. Takakura, A. Hata, T. Kaname, M. Akizuki, Y. Yamaguchi, H. Yasue, K. Araki, K. Yamamura, and T. Suda. 1999. Mice homozygous for a truncated form of CREB-binding protein exhibit defects in hematopoiesis and vasculo-angiogenesis. Blood 93:2771-2779.
56. Ouyang, L., X. Chen, and J. J. Bieker. 1998. Regulation of eiythroid Kruppel-like factor (EKLF) transcriptional activity by phosphorylation of a protein kinase casein kinase II site within its interaction domain. J. Biol. Chem. 273:23019-23025.
57. Owen-Hughes, T., R. T. Utley, D. J. Steger, J. M. West, S. John, J. Cote, K. M. Havas, and J. L. Workman. 1999. Analysis of nucleosome disruption by ATP-driven chromatin remodeling complexes. Methods Mol. Biol. 119: 319-331.
58. Pandya, K, and T. M. Townes. 2002. Basic residues within the Kruppel zinc finger DNA binding domains are the critical nuclear localization determinants of EKLF/KLF-1. J. Biol. Chem. 277:16304-16312.
59. Perkins, A. C., A. H. Sharpe, and S. H. Orkin. 1995. Lethal beta-thalas-saemia in mice lacking the eiythroid CACCC-transcription factor EKLF. Nature 375:318-322.
60. Pilon, A. M., D. G. Nilson, D. Zhou, J. Sangerman, T. M. Townes, D. M. Bodine, and P. G. Gallagher. 2006. Alterations in expression and chromatin configuration of the alpha hemoglobin-stabilizing protein gene in eiythroid Kruppel-like factor-deficient mice. Mol. Cell. Biol. 26:4368-4377.
61. Quadrini, K. J., and J. J. Bieker. 2006. EKLF/KLF1 is ubiquitinated in vivo and its stability is regulated by activation domain sequences through the 26S proteasome. FEBS Lett. 580:2285-2293.
62. Quadrini, K. J., and J. J. Bieker. 2002. Kruppel-like zinc fingers bind to nuclear import proteins and are required for efficient nuclear localization of eiythroid Kruppel-like factor. J. Biol. Chem. 277:32243-32252.
63. Sarma, K, and D. Reinberg. 2005. Histone variants meet their match. Nat. Rev. Mol. Cell Biol. 6:139-149.
64. Schwartz, B. E., and K Ahmad. 2005. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 19:804-814.
65. Shahbazian, M. D., and M. Grunstein. 2007. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76:75-100.
66. Siatecka, M., L. Xue, and J. J. Bieker. 2007. Sumoylation of EKLF promotes transcriptional repression and is involved in inhibition of megakaryopoiesis. Mol. Cell. Biol. 27:8547-8560.
67. Southwood, C. M., K. M. Downs, and J. J. Bieker. 1996. Eiythroid Kruppel-like factor exhibits an early and sequentially localized pattern of expression during mammalian eiythroid ontogeny. Dev. Dyn. 206:248-259.
68. Stamatoyannopoulos, G. 2005. Control of globin gene expression during development and eiythroid differentiation. Exp. Hematol. 33:259-271.
69. Tagami, H., D. Ray-Gallet, G. Almouzni, and Y. Nakatani. 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51-61.
70. Tewari, R., N. Gillemans, A. Harper, M. Wijgerde, G. Zafarana, D. Drabek, F. Grosveld, and S. Philipsen. 1996. The human beta-globin locus control region confers an early embryonic eiythroid-specific expression pattern to a basic promoter driving the bacterial lacZ gene. Development 122:3991-3999.
71. Tewari, R., N. Gillemans, M. Wijgerde, B. Nuez, M. von Lindern, F. Grosveld, and S. Philipsen. 1998. Eiythroid Kruppel-like factor (EKLF) is active in primitive and definitive eiythroid cells and is required for the function of 5'HS3 of the beta-globin locus control region. EMBO J. 17:2334-2341.
72. Van Parijs, L., Y. Refaeli, A. K Abbas, and D. Baltimore. 1999. Autoimmunity as a consequence of retrovirus-mediated expression of C-FLIP in lymphocytes. Immunity 11:763-770.
73. Vermeulen, M., K. W. Mulder, S. Denissov, W. W. Pijnappel, F. M. van Schaik, R. A. Varier, M. P. Baltissen, H. G. Stunnenberg, M. Mann, and H. T. Timmers. 2007. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58-69.
74. Wijgerde, M., J. Gribnau, T. Trimborn, B. Nuez, S. Philipsen, F. Grosveld, and P. Fraser. 1996. The role of EKLF in human beta-globin gene competition. Genes Dev. 10:2894-2902.
75. Wozniak, R. J., and E. H. Bresnick. 2008. Epigenetic control of complex loci during erythropoiesis. Curr. Top. Dev. Biol. 82:55-83.
76. Zhang, W., and J. J. Bieker. 1998. Acetylation and modulation of eiythroid Kruppel-like factor (EKLF) activity by interaction with histone acetyltrans-ferases. Proc. Natl. Acad. Sci. USA 95:9855-9860.
77. Zhang, W., S. Kadam, B. M. Emerson, and J. J. Bieker. 2001. Site-specific acetylation by p300 or CREB binding protein regulates eiythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol. Cell. Biol. 21:2413-2422.