Genetic analysis of hierarchical regulation for Gata1 and NF-E2 p45 gene expression in megakaryopoiesis

Molecular and Cellular Biology

Volumn 30, Issue 11, 2010, Pages 2668-2680

  Takayama, Mariko ^a   Fujita, Rie ^a   Suzuki, Mikiko ^a   Okuyama, Ryuhei ^a   Aiba, Setsuya ^a   Motohashi, Hozumi ^a   Yamamoto, Masayuki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR NF E2 P45 SUBUNIT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLEEDING; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC COMPLEMENTATION; IN VIVO STUDY; MALE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; THROMBOCYTE COUNT; TRANSACTIVATION; TRANSGENE;

ANIMALS; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; MEGAKARYOCYTES; MICE; MICE, TRANSGENIC; NF-E2 TRANSCRIPTION FACTOR, P45 SUBUNIT; PROMOTER REGIONS, GENETIC; SPLEEN; THROMBOPOIESIS;

MUS; MUS MUSCULUS;

EID: 77952607108     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01304-09     Document Type: Article

References (54)

1. Amrolia, P. J., L. Ramamurthy, D. Saluja, N. Tanese, S. M. Jane, and J. M. Cunningham. 1997. The activation domain of the enhancer binding protein p45NF-E2 interacts with TAFII130 and mediates long-range activation of the α- and β-globin gene loci in an erythroid cell line. Proc. Natl. Acad. Sci. U. S. A. 94:10051-10056.
2. Bartůneǩ, P., J. Králová, G. Blendinger, M. Dvorák, and M. Zenke. 2003. GATA-1 and c-myb crosstalk during red blood cell differentiation through GATA-1 binding sites in the c-myb promoter. Oncogene 22:1927-1935.
3. Bean, T. L., and P. A. Ney. 1997. Multiple regions of p45 NF-E2 are required for β-globin gene expression in erythroid cells. Nucleic Acids Res. 25:2509-2515.
4. Chang, A. N., A. B. Cantor, Y. Fujiwara, M. B. Lodish, S. Droho, J. D. Crispino, and S. H. Orkin. 2002. GATA-factor dependence of the multitype zinc-finger protein FOG-1 for its essential role in megakaryopoiesis. Proc. Natl. Acad. Sci. U. S. A. 99:9237-9242.
5. Chen, Z., M. Hu, and R. A. Shivdasani. 2007. Expression analysis of primary mouse megakaryocyte differentiation and its application in identifying stage-specific molecular markers and a novel transcriptional target of NF-E2. Blood 109:1451-1459. (Pubitemid 46239576)
6. Chou, S. T., E. Khandros, L. C. Bailey, K. E. Nichols, C. R. Vakoc, Y. Yao, Z. Huang, J. D. Crispino, R. C. Hardison, G. A. Blobel, and M. J. Weiss. 2009. Graded repression of PU.1/Sfpi1 gene transcription by GATA factors regulates hematopoietic cell fate. Blood 114:983-994.
7. Deveaux, S., S. Cohen-Kaminsky, R. A. Shivdasani, N. C. Andrews, A. Filipe, I. Kuzniak, S. H. Orkin, P. H. Roméo, and V. Mignotte. 1997. p45 NF-E2 regulates expression of thromboxane synthase in megakaryocytes. EMBO J. 16:5654-5661. (Pubitemid 27399857)
8. FANTOM Consortium, H. Suzuki, A. R. R. Forrest, E. van Nimwegen, C. O. Daub, P. J. Balwierz, K. M. Irvine, T. Lassmann, T. Ravasi, Y. Hasegawa, M. J. L. de Hoon, S. Katayama, K. Schroder, P. Carninci, Y. Tomaru, M. Kanamori-Katayama, A. Kubosaki, A. Akalin, Y. Ando, E. Arner, M. Asada, H. Asahara, T. Bailey, V. B. Bajic, D. Bauer, A. G. Beckhouse, N. Bertin, J. Björkegren, F. Brombacher, E. Bulger, A. M. Chalk, J. Chiba, N. Cloonan, A. Dawe, J. Dostie, P. G. Engström, M. Essack, G. J. Faulkner, J. L. Fink, D. Fredman, K. Fujimori, M. Furuno, T. Gojobori, J. Gough, S. M. Gimmond, M. Gustafsson, M. Hashimoto, T. Hashimoto, M. Hatakeyama, S. Heinzel, W. Hide, O. Hofmann, M. Hörnquist, L. Huminiecki, K. Ikeo, N. Imamoto, S. Inoue, Y. Inoue, R. Ishihara, T. Iwayanagi, A. Jacobsen, M. Kaur, H. Kawaji, M. C. Kerr, R. Kimura, S. Kimura, Y. Kimura, H. Kitano, H. Koga, T. Kojima, S. Kondo, T. Konno, A. Krogh, A. Kruger, A. Kumar, B. Lenhard, A. Lennartsson, M. Lindow, M. Lizio, C. MacPherson, N. Maeda, C. A. Maher, M. Maqungo, J. Mar, N. A. Matigian, H. Matsuda, J. S. Mattick, S. Meier, S. Miyamoto, E. Miyamoto-Sato, K. Nakabayashi, Y. Nakachi, M. Nakano, S. Nygaard, T. Okayama, Y. Okazaki, H. Okuda-Yabukami, V. Orlando, J. Otomo, M. Pachkow, et al. 2009. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat. Genet. 41:553-562.
9. Fock, E.-L., F. Yan, S. Pan, and B. H. Chong. 2008. NF-E2-mediated enhancement of megakaryocytic differentiation and platelet production in vitro and in vivo. Exp. Hematol. 36:78-92.
10. Fujiwara, T., H. O'heen, S. Keles, K. Blahnik, A. K. Linnemann, Y.-A. Kang, K. Choi, P. J. Farnham, and E. H. Bresnick. 2009. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol. Cell. 36:667-681.
11. Fujiwara, Y., C. P. Browne, K. Cunniff, S. C. Goff, and S. H. Orkin. 1996. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc. Natl. Acad. Sci. U. S. A. 93:12355-12358.
12. Grass, J. A., M. E. Boyer, S. Pal, J. Wu, M. J. Weiss, and E. H. Bresnick. 2003. GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc. Natl. Acad. Sci. U. S. A. 100:8811-8816.
13. Hung, H.-L., A. Y. Kim, W. Hong, C. Rakowski, and G. A. Blobel. 2001. Stimulation of NF-E2 DNA binding by CREB-binding protein (CBP)-mediated acetylation. J. Biol. Chem. 276:10715-10721.
14. Igarashi, K., K. Kataoka, K. Itoh, N. Hayashi, M. Nishizawa, and M. Yamamoto. 1994. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature 367:568-572. (Pubitemid 24055517)
15. Kacena, M. A., C. M. Gundberg, T. Nelson, and M. C. Horowitz. 2005. Loss of the transcription factor p45 NF-E2 results in a developmental arrest of megakaryocyte differentiation and the onset of a high bone mass phenotype. Bone 36:215-223.
16. Kiekhaefer, C. M., M. E. Boyer, K. D. Johnson, and E. H. Bresnick. 2004. A WW domain-binding motif within the activation domain of the hematopoietic transcription factor NF-E2 is essential for establishment of a tissue-specific histone modification pattern. J. Biol. Chem. 279:7456-7461.
17. Lecine, P., J.-L. Villeval, P. Vyas, B. Swencki, Y. Xu, and R. A. Shivdasani. 1998. Mice lacking transcription factor NF-E2 provide in vivo validation of the proplatelet model of thrombocytopoiesis and show a platelet production defect that is intrinsic to megakaryocytes. Blood 92:1608-1616. (Pubitemid 28406864)
18. Levin, J., J.-P. Peng, G. R. Baker, J.-L. Villeval, P. Lecine, S. A. Burstein, and R. A. Shivdasani. 1999. Pathophysiology of thrombocytopenia and anemia in mice lacking transcription factor NF-E2. Blood 94:3037-3047. (Pubitemid 29512708)
19. Lohmann, F., and J. J. Bieker. 2008. Activation of Eklf expression during hematopoiesis by Gata2 and Smad5 prior to erythroid commitment. Development 135:2071-2082. (Pubitemid 352022521)
20. McCormack, M. P., M. A. Hall, S. M. Schoenwaelder, Q. Zhao, S. Ellis, J. A. Prentice, A. J. Clarke, N. J. Slater, J. M. Salmon, S. P. Jackson, S. M. Jane, and D. J. Curtis. 2006. A critical role for the transcription factor Scl in platelet production during stress thrombopoiesis. Blood 108:2248-2256.
21. McDevitt, M. A., R. A. Shivdasani, Y. Fujiwara, H. Yang, and S. H. Orkin. 1997. A "knockdown" mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc. Natl. Acad. Sci. U. S. A. 94:6781-6785.
22. Moroni, E., T. Mastrangelo, R. Razzini, L. Cairns, P. Moi, S. Ottolenghi, and B. Giglioni. 2000. Regulation of mouse p45 NF-E2 transcription by an erythroid-specific GATA-dependent intronic alternative promoter. J. Biol. Chem. 275:10567-10576.
23. Mosser, E. A., J. D. Kasanov, E. C. Forsberg, B. K. Kay, P. A. Ney, and E. H. Bresnick. 1998. Physical and functional interactions between the transactivation domain of the hematopoietic transcription factor NF-E2 and WW domains. Biochemistry 37:13686-13695.
24. Motohashi, H., K. Igarashi, K. Onodera, S. Takahashi, H. Ohtani, M. Nakafuku, M. Nishizawa, J. D. Engel, and M. Yamamoto. 1996. Mesodermal- vs. neuronal-specific expression of MafK is elicited by different promoters. Genes Cells 1:223-238.
25. Motohashi, H., F. Katsuoka, J. A. Shavit, J. D. Engel, and M. Yamamoto. 2000. Positive or negative MARE-dependent transcriptional regulation is determined by the abundance of small Maf proteins. Cell 103:865-875.
26. Motohashi, H., F. Katsuoka, C. Miyoshi, Y. Uchimura, H. Saitoh, C. Francastel, J. D. Engel, and M. Yamamoto. 2006. MafG sumoylation is required for active transcriptional repression. Mol. Cell. Biol. 26:4652-4663.
27. Motohashi, H., M. Kimura, R. Fujita, A. Inoue, X. Pan, M. Takayama, F. Katsuoka, H. Aburatani, E. H. Bresnick, and M. Yamamoto. 2010. NF-E2 domination over Nrf2 promotes ROS accumulation and megakaryocytic maturation. Blood 115:677-686.
28. Mukai, H. Y., H. Motohashi, O. Ohneda, N. Suzuki, M. Nagano, and M. Yamamoto. 2006. Transgene insertion in proximity to the c-myb gene disrupts erythroid-megakaryocytic lineage bifurcation. Mol. Cell. Biol. 26:7953-7965.
29. Murate, T., T. Hotta, K. Tsushita, M. Suzuki, T. Yoshida, S. Saga, H. Saito, and S. Yoshida. 1991. Aphidicolin, an inhibitor of DNA replication, blocks the TPA-induced differentiation of a human megakaryoblastic cell line, MEG01. Blood 12:3168-3177.
30. Nagai, T., K. Igarashi, J. Akasaka, K. Furuyama, H. Fujita, N. Hayashi, M. Yamamoto, and S. Sassa. 1998. Regulation of NF-E2 activity in erythroleukemia cell differentiation. J. Biol. Chem. 273:5358-5365.
31. Onodera, K., S. Takahashi, S. Nishimura, J. Ohta, H. Motohashi, K. Yomogida, N. Hayashi, J. D. Engel, and M. Yamamoto. 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.
32. Onodera, K., J. A. Shavit, H. Motohashi, M. Yamamoto, and J. D. Engel. 2000. Perinatal synthetic lethality and hematopoietic defects in compound mafG::mafK mutant mice. EMBO J. 19:1335-1345.
33. Pang, L., M. J. Weiss, and M. Poncz. 2005. Megakaryocyte biology and related disorders. J. Clin. Invest. 115:3332-3338.
34. Pischedda, C., S. Cocco, A. Melis, M. G. Marini, Y. W. Kan, A. Cao, and P. Moi. 1995. Isolation of a differentially regulated splicing isoform of human NF-E2. Proc. Natl. Acad. Sci. U. S. A. 92:3511-3515.
35. Shavit, J. A., H. Motohashi, K. Onodera, J. Akasaka, M. Yamamoto, and J. D. Engel. 1998. Impaired megakaryopoiesis and behavioral defects in mafG-null mutant mice. Genes Dev. 12:2164-2174.
36. Shimizu, R., K. Ohneda, J. D. Engel, C. D. Trainor, and M. Yamamoto. 2004. Transgenic rescue of GATA-1-deficient mice with GATA-1 lacking a FOG-1 association site phenocopies patients with X-linked thrombocytopenia. Blood 103:2560-2567. (Pubitemid 38393007)
37. Shivdasani, R. A., M. F. Rosenblatt, D. Zucker-Franklin, C. W. Jackson, P. Hunt, C. J. M. Saris, and S. H. Orkin. 1995. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/ MGDF in megakaryocyte development. Cell 81:695-704.
38. Shivdasani, R. A., Y. Fujiwara, M. A. McDevitt, and S. H. Orkin. 1997. A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in megakaryocyte growth and platelet development. EMBO J. 16:3965-3973.
39. Shivdasani, R. A. 2001. Molecular and transcriptional regulation of megakaryocyte differentiation. Stem Cells 19:397-407. (Pubitemid 32900082)
40. Suzuki, M., T. Moriguchi, K. Ohneda, and M. Yamamoto. 2009. Differential contribution of the Gata1 gene hematopoietic enhancer to erythroid differentiation. Mol. Cell. Biol. 29:1163-1175.
41. Suzuki, N., N. Suwabe, O. Ohneda, N. Obara, S. Imagawa, X. Pan, H. Motohashi, and M. Yamamoto. 2003. Identification and characterization of 2 types of erythroid progenitors that express GATA-1 at distinct levels. Blood 102:3575-3583. (Pubitemid 37409373)
42. Szalai, G., A. C. LaRue, and D. K. Watson. 2006. Molecular mechanisms of megakaryopoiesis. Cell. Mol. Life Sci. 63:2460-2476.
43. Takahashi, S., K. Onodera, H. Motohashi, N. Suwabe, N. Hayashi, N. Yanai, Y. Nabesima, and M. Yamamoto. 1997. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J. Biol. Chem. 272:12611-12615.
44. Takahashi, S., R. Shimizu, N. Suwabe, T. Kuroha, K. Yoh, J. Ohta, S. Nishimura, K. C. Lim, J. D. Engel, and M. Yamamoto. 2000. GATA factor transgenes under GATA-1 locus control rescue germline GATA-1 mutant deficiencies. Blood 96:910-916.
45. Tanabe, O., D. Macphee, S. Kobayashi, Y. Shen, W. Brandt, X. Jiang, A. D. Campbell, Y.-T. Chen, C.-S. Chang, M. Yamamoto, K. Tanimoto, and J. D. Engel. 2007. Embryonic and fetal β-globin gene repression by the orphan nuclear receptors, TR2 and TR4. EMBO J. 26:2295-2306. (Pubitemid 46685858)
46. Toki, T., K. Arai, K. Terui, N. Komatsu, M. Yokoyama, F. Katsuoka, M. Yamamoto, and E. Ito. 2000. Functional characterization of the two alternative promoters of human p45 NF-E2 gene. Exp. Hematol. 28:1113-1119.
47. Toki, T., F. Katsuoka, R. Kanezaki, G. Xu, H. Kurotaki, J. Sun, T. Kamio, S. Watanabe, S. Tandai, K. Terui, S. Yagihashi, N. Komatsu, K. Igarashi, M. Yamamoto, and E. Ito. 2005. Transgenic expression of BACH1 transcription factor results in megakaryocytic impairment. Blood 105:3100-3108. (Pubitemid 40504327)
48. Tsang, A. P., Y. Fujiwara, D. B. Hom, and S. H. Orkin. 1998. Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev. 12:1176-1188.
49. low mice). Blood 100:1123-1132.
50. Vyas, P., K. Ault, C. W. Jackson, S. H. Orkin, and R. A. Shivdasani. 1999. Consequences of GATA-1 deficiency in megakaryocytes and platelets. Blood 93:2867-2875. (Pubitemid 29200777)
51. Welch, J. J., J. A. Watts, C. R. Vakoc, Y. Yao, H. Wang, R. C. Hardison, G. A. Blobel, L. A. Chodosh, and M. J. Weiss. 2004. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 104:3136-3147.
52. Wilson, N. K., D. Miranda-Saavedra, S. Kinston, N. Bonadies, S. D. Foster, F. Calero-Nieto, M. A. Dawson, I. J. Donaldson, S. Dumon, J. Frampton, R. Janky, X. H. Sun, S. A. Teichmann, A. J. Bannister, and B. Göttgens. 2009. The transcriptional program controlled by the stem cell leukemia gene Scl/ Tal1 during early embryonic hematopoietic development. Blood 113:5456-5465.
53. Yan, X.-Q., D. Lacey, D. Hill, Y. Chen, F. Fletcher, R. G. Hawley, and I. K. McNiece. 1996. A model of myelofibrosis and osteosclerosis in mice induced by overexpressing thrombopoietin (mpl ligand): reversal of disease by bone marrow transplantation. Blood 88:402-409. (Pubitemid 26240370)
54. Yates, M. S., M. Tauchi, F. Katsuoka, K. C. Flanders, K. T. Liby, T. Honda, G. W. Gribble, D. A. Johnson, J. A. Johnson, N. C. Burton, T. R. Guilarte, M. Yamamoto, M. B. Sporn, and T. W. Kensler. 2007. Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes. Mol. Cancer Ther. 6:154-162.