Dissecting molecular steps in chromatin domain activation during hematopoietic differentiation

Molecular and Cellular Biology

Volumn 27, Issue 12, 2007, Pages 4551-4565

  Kim, Shin Il ^a   Bultman, Scott J ^b   Jing, Huie ^c   Blobel, Gerd A ^c   Bresnick, Emery H ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; CELL PROTEIN; PROTEIN BRG1; RNA POLYMERASE II; SERINE; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE CONTROL; GENETIC TRANSCRIPTION; HEMATOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN BINDING; REGULATOR GENE; TRANSCRIPTION INITIATION;

ALLELES; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA HELICASES; ERYTHROID CELLS; GATA1 TRANSCRIPTION FACTOR; GENE DELETION; GENE EXPRESSION REGULATION; GLOBINS; HEMATOPOIETIC SYSTEM; LOCUS CONTROL REGION; MICE; MICE, KNOCKOUT; MODELS, GENETIC; NUCLEAR PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; TEMPERATURE; TRANSCRIPTION FACTORS;

MUS;

EID: 34250183131     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00235-07     Document Type: Article

References (87)

1. Agalioti, T., G. Chen, and D. Thanos. 2002. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111:381-392.
2. Agalioti, T., S. Lomvardas, B. Parekh, J. Yie, T. Maniatis, and D. Thanos. 2000. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103:667-678.
3. Andrews, N. C., H. Erdjument-Bromage, M. B. Davidson, P. Tempst, and S. H. Orkin. 1993. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 362:722-728.
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. Bender, M. A., M. Bulger, J. Close, and M. Groudine. 2000. Beta-globin gene switching and DNaseI sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol. Cell 5:387-393.
6. Bender, M. A., J. N. Roach, J. Halow, J. Close, R. Aland, E. E. Bouhassira, M. Groudine, and S. N. Fiering. 2001. Targeted deletion of 5′HSI and 5′HS4 of the beta-globin locus control region reveals additive activity of the DNaseI hypersensitive sites. Blood 98:2022-2027.
7. Blobel, G. A., T. Nakajima, R. Eckner, M. Montminy, and S. H. Orkin. 1998. CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc. Natl. Acad. Sci. USA 95:2061-2066.
8. 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 Acids Res. Mol. Biol. 81:435-471.
9. Bultman, S. J., T. C. Gebuhr, and T. Magnuson. 2005. A Brg1 mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SW1/SNF complexes in beta-globin expression and erythroid development. Genes Dev. 19:2849-2861.
10. Cantor, A. B., and S. H. Orkin. 2002. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21:3368-3376.
11. Cantor, A. B., and S. H. Orkin. 2005. Coregulation of GATA factors by the Friend of GATA (FOG) family of multitype zinc finger proteins. Semin. Cell Dev. Biol. 16:117-128.
12. Charles, M. A., T. L. Saunders, W. M. Wood, K. Owens, A. F. Parlow, S. A. Camper, E. C. Ridgway, and D. F. Gordon. 2006. Pituitary-specific Gata2 knockout: effects on gonadotrope and thyrotrope function. Mol. Endocrinol. 20:1366-1377.
13. Cosma, M. P. 2002. Ordered recruitment: gene-specific mechanism of transcription activation. Mol. Cell 10:227-236.
14. Cosma, M. P., T. Tanaka, and K. Nasmyth. 1999. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 97:299-311.
15. Craven, S. E., K. C. Lim, W. Ye, J. D. Engel, F. de Sauvage, and A. Rosenthal. 2004. Gata2 specifics serotonergic neurons downstream of sonic hedgehog. Development 131:1165-1173.
16. Crispino, J. D., M. B. Lodish, J. P. MacKay, and S. H. Orkin. 1999. Use of altered specificity mutants to probe a specific protein-protein interaction in differentiation: the GATA-1:FOG complex. Mol. Cell 3:219-228.
17. Dean, A. 2006. On a chromosome far, far away: LCRs and gene expression. Trends Genet. 22:38-45.
18. 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.
19. Epner, E., A. Reik, D. Cimbora, A. Telling, M. A. Bender, S. Fiering, T. Enver, D. I. Martin, M. Kennedy, G. Keller, and M. Groudine. 1998. The beta-globin LCR is not necessary for an open chromatin structure or developmentally regulated transcription of the native mouse beta-globin locus. Mol. Cell 2:447-455.
20. Evans, T., and G. Felsenfeld. 1989. The erythroid-specitic transcription factor Eryf1: a new linger protein. Cell 58:877-885.
21. Forrester, W. C., S. Takegawa, T. Papayannopoulou, G. Stamatoyannopoulos, and M. Groudine. 1987. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res. 15:10159-10177.
22. Forsberg, E. C., K. Johnson, T. N. Zaboikina, E. A. Mosser, and E. H. Bresnick. 1999. Requirement of an E1A-scnsitive coactivator for long-range transactivation by the beta-globin locus control region. J. Biol. Chem. 274: 26850-26859.
23. 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. USA 100:8811-8816.
24. Grass, J. A., H. Jing, S.-I. Kim, M. L. Martowicz, S. Pal, G. A. Blobel, and E. H. Bresnick. 2006. Distinct functions of dispersed GATA factor complexes at an endogenous gene locus. Mol. Cell. Biol. 26:7056-7067.
25. Gregory, T., C. Yu, A. Ma, S. H. Orkin, G. A. Blobel, and M. J. Weiss. 1999. GATA-1 and erythropoietin cooperate to promoter erythroid cell survival by regulating bcl-xl expression. Blood 94:87-96.
26. Grosveld, F., G. B. van Assendelft, D. R. Greaves, and G. Kollias. 1987. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell 51:975-985.
27. Hatzis, P., and I. Talianidis. 2002. Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol. Cell 10:1467-1477.
28. Ho, I. C., P. Vorhees, N. Marin, B. K. Oakley, S. F. Tsai, S. H. Orkin, and J. M. Leiden. 1991. Human GATA-3: a lineage-restricted transcription factor that regulates the expression of the T cell receptor alpha gene. EMBO J. 10:1187-1192.
29. Hong, W., M. Nakazawa, Y. Y. Chen, R. Kori, C. R. Vakoc, C. Rakowski, and G. A. Blobel. 2005. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 24:67-78.
30. 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.
31. Im, H., J. A. Grass, K. D. Johnson, M. E. Boyer, J. Wu, and E. H. Bresnick. 2004. Measurement of protein-DNA interactions in vivo by chromatin immunoprecipitation. Methods Mol. Biol. 284:129-146.
32. 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.
33. Johnson, K. D., M. E. Boyer, S.-I. Kim, S. Y. Kang, A. Wickrema, A. B. Cantor, and E. H. Bresnick. 5 March 2007. Friend of GATA-1-independent transcriptional repression: a novel mode of GATA-1 function. Blood. doi: 10.1182/blood-2007-02-072983.
34. Johnson, K. D., H. M. Christensen, B. Zhao, and E. H. Bresnick. 2001. Distinct mechanisms control RNA polymerase II recruitment to a tissue-specific locus control region and a downstream promoter. Mol. Cell 8:465-471.
35. Johnson, K. D., J. A. Grass, H. Im, C. Park, K. Choi, and E. H. Bresnick. 2003. Highly restricted localization of RNA polymerase 11 to the hypersensitive site cores of a tissue-specific locus control region. Mol. Cell. Biol. 23:6468-6493.
36. Johnson, K. D., J. D. Grass, M. E. Boyer, C. M. Kiekhaefer, G. A. Blobel, M. J. Weiss, and E. H. Bresnick. 2002. Cooperative activities of hematopoietic regulators recruit RNA polymerase II to a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 99:11760-11765.
37. Johnson, K. D., S.-I. Kim, and E. H. Bresnick. 2006. Differential sensitivities of transcription factor target genes underlie cell type-specific gene expression patterns. Proc. Natl. Acad. Sci. USA 103:15939-15944.
38. Kadam, S., G. S. McAlpine, M. L. Phelan, R. E. Kingston, K. A. Jone, and B. M. Emerson. 2000. Functional selectivity of recombinant mammalian SW1/SNF subunits. Genes Dev. 14:2441-2451.
39. Kingsley, P. D., J. Malik, R. L. Emerson, T. P. Bushnell, K. E. McGrath, L. A. Bloedorn, M. Bulger, and J. Palis. 2006. " Maturational" globin switching in primary primitive erythroid cells. Blood 107:1665-1672.
40. Kotkow, K. J., and S. H. Orkin. 1995. Dependence of globin gene expression in mouse erythroleukemia cells on the NF-E2 heterodimer. Mol. Cell. Biol. 15:4640-4647.
41. Lee, M. E., D. H. Temizer, J. A. Clifford, and T. Quertermous. 1991. Cloning of the GATA binding protein that regulates endothelin-1 gene expression in endothelial cells. J. Biol. Chem. 266:16188-16192.
42. Letting, D. L., Y. Y. Chen, C. Rakowski, S. Reedy, and G. A. Blobel. 2004. Context-dependent regulation of GATA-1 by friend of GATA-1. Proc. Natl. Acad. Sci. USA 101:476-481.
43. Letting, D. L., C. Rakowski, M. J. Weiss, and G. A. Blobel. 2003. Formation of a tissue-specific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol. Cell. Biol. 23:1334-1340.
44. Lu, S. J., S. Rowan, M. R. Bani, and Y. Ben-David. 1994. Retroviral integration within the Fli-2 locus results in inactivation of the erythroid transcription factor NF-E2 in Friend crythroleukemias: evidence that NF-E2 is essential for globin expression. Proc. Natl. Acad. Sci. USA 91:8398-8402.
45. Martowicz, M. L., J. A. Grass, M. E. Boyer, H. Guend, and E. H. Bresnick. 2005. Dynamic GATA factor interplay at a multi-component regulatory region of the GATA-2 locus. J. Biol. Chem. 280:1724-1732.
46. Merika, M., and S. H. Orkin. 1995. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Kruppel family proteins Sp1 and EKLF. Mol. Cell. Biol. 15:2437-2447.
47. Metivier, R., G. Penot, M. R. Hubner, G. Reid, H. Brand, M. Kos, and F. Gannon. 2003. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763.
48. Migliaccio, A. R., R. A. Rana, M. Sanchez, R. Lorenzini, L. Centurione, L. Bianchi, A. M. Vannucchi, G. Migliaccio, and S. H. Orkin. 2003. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J. Exp. Med. 197:281-296.
49. 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.
50. Muntean, A. G., and J. D. Crispino. 2005. Differential requirements for the activation domain and FOG-interaction surface of GATA-1 in megakaryocyte gene expression and development. Blood 106:1223-1231.
51. Nardelli, J., D. Thiesson, Y. Fujiwara, F.-Y. Tsai, and S. H. Orkin. 1999. Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 210:305-321.
52. Nerlov, C., E. Querfurth, H. Kulessa, and T. Graf. 2000. GATA-1 interacts with the myeloid PU. 1 transcription factor and represses PU.1-dependent transcription. Blood 95:2543-2551.
53. Ney, P. A., N. C. Andrews, S. M. Jane, B. Safer, M. E. Purucker, S. Weremowicz, C. C. Morton, S. C. Goff, S. H. Orkin, and A. W. Nienhuis. 1993. Purification of the human NF-E2 complex: cDNA cloning of the hematopoietic cell-specific subunit and evidence for an associated partner. Mol. Cell. Biol. 13:5604-5612.
54. Omichinski, J. G., G. M. Clore, O. Schaad, G. Felsenfeld, C. Trainor, E. Appella, S. J. Stahl, and A. M. Gronenhorn. 1993. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 261:438-446.
55. Orphanides, G., and D. Reinberg. 2002. A unified theory of gene expression. Cell 108:439-451.
56. Pai, S. Y., M. L. Truitt, C. N. Ting, J. M. Leiden, L. H. Glimcher, and I. C. Ho. 2003. Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 19:863-875.
57. Pal, S., A. B. Cantor, K. D. Johnson, T. Moran, M. E. Boyer, S. H. Orkin, and E. H. Bresnick. 2004. Coregulator-dependent facilitation of chromatin occupancy by GATA-1. Proc. Natl. Acad. Sci. USA 101:980-985.
58. Pevny, L., C. S. Lin, V. D'Agati, M. C. Simon, S. H. Orkin, and F. Costantini. 1995. Development of hematopoietic cells lacking transcription factor GATA-1. Development 121:163-172.
59. Pevny, L., M. C. Simon, E. Robertson, W. H. Klein, S. F. Tsai, V. D'Agati, S. H. Orkin, and F. Costantini. 1991. Erythroid differentiation in chimacric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349:257-260.
60. Phatnani, H. P., and A. L. Greenleaf. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:2922-2936.
61. Ragoczy, T., M. A. Bender, A. Telling, R. Byron, and M. Groudine. 2006. The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. Genes Dev. 20:1447-1457.
62. Rekhtman, N., F. Radparvar, T. Evans, and A. I. Skoultchi. 1999. Direct interaction of hematopoietic transcription factors PU. 1 and GATA-1: functional antagonism in erythroid cells. Genes Dev. 13:1398-1411.
63. Rodriguez, P., E. Bonte, J. Krijgsveld, K. E. Kolodziej, B. Guyot, A. J. Heck, P. Vyas, E. de Boer, F. Grosveld, and J. Strouboulis. 2005. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24:2354-2366.
64. Salma, N., H. Xiao, E. Mueller, and A. N. Imbalzano. 2004. Temporal recruitment of transcription factors and SWI/SNF chromatin remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated gamma nuclear hormone receptor. Mol. Cell. Biol. 24:4651-4663.
65. Sawado, T., J. Halow, M. A. Bender, and M. Groudine. 2003. The beta-globin locus control region (LCR) functions primarily by enhancing the transition from transcription initiation to elongation. Genes Dev. 17:1009-1118.
66. Shang, Y., X. Hu, J. DiRenzo, M. A. Zazar, and M. Brown. 2000. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852.
67. 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 mekagaryocyte growth and platelet development. EMBO J. 16:3965-3973.
68. Simon, M. C., L. Pevny, M. V. Wiles, G. Keller, F. Costantini, and S. H. Orkin. 1992. Rescue of erythroid development in gene targeted GATA-1-mouse embryonic stem cells. Nat. Genet. 1:92-98.
69. Takahashi, S., K. Onodera, H. Motohashi, N. Suwabe, N. Hayashi, N. Yanai, Y. Nabesima, and M. Yamamoto. 1997. Arrest in primitive erythroid cell development by promoter-specific disruption of the GATA-1 gene. J. Biol. Chem. 272:12611-12615.
70. Ting, C. N., M. C. Olson, K. P. Barton, and J. M. Leiden. 1996. Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 384:474-478.
71. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 10:1453-1475.
72. Tsai, F.-Y., and S. H. Orkin. 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.
73. Tsai, F. Y., G. Keller, F. C. Kuo, M. Weiss, J. Chen, M. Rosenblatt, F. W. Alt, and S. H. Orkin. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221-226.
74. Tsai, S. F., D. I. Martin, L. I. Zon, A. D. D'Andrea, G. G. Wong, and S. H. Orkin. 1989. Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature 339:446-451.
75. Tsang, A. P., Y. Fujiwara, D. B. Hom, and S. H. Orkin. 1998. Failure of megakaryopoiesis and arrested crythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev. 12:1176-1188.
76. Tsang, A. P., J. E. Visvader, C. A. Turner, Y. Fujuwara, C. Yu, M. J. Weiss, M. Crossley, and S. H. Orkin. 1997. FOG. a multitype zinc finger protein as a cofactor for transcription factor GATA-1 in erythroid and megakaryocyte differentiation. Cell 90:109-119.
77. Vakoc, C. R., D. L. Letting, N. Gheldof, T. Sawado, M. A. Bender, M. Groudine, M. J. Weiss, J. Dekker, and G. A. Blobel. 2005. Proximity among distant regulatory elements at the beta globin locus requires GATA-1 and FOG-1. Mol. Cell 17:453-462.
78. Vieira, K. F., P. P. Levings, M. A. Hill, V. J. Cruselle, S. H. Kang, J. D. Engel, and J. Bungert. 2004. Recruitment of transcription complexes to the beta-globin gene locus in vivo and in vitro. J. Biol. Chem. 279:50350-50357.
79. Weiss, M. J., G. Keller, and S. H. Orkin. 1994. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 8:1184-1197.
80. 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.
81. Yamamoto, M., L. J. Ko, M. W. Leonard, H. Beug, S. H. Orkin, and J. D. Engel. 1990. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 4:1650-1662.
82. Yu, C., A. B. Cantor, H. Yang, C. Browne, R. A. Wells, Y. Fukiwara, and S. H. Orkin. 2002. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med. 195:1387-1395.
83. Zhang, P. J., X. Zhang, A. Iwaina. C. Yu, K. A. Smith, B. U. Mueller, S. Narravula, B. E. Torbett, S. H. Orkin, and D. G. Tenen. 2000. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96:2641-2648.
84. Zhang, W., S. Kadam, B. M. Emerson, and J. J. Bieker. 2001. Site-specific acetylation by p300 or CREB binding protein regulates erythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol. Cell. Biol. 21:2413-2422.
85. Zhou, D., K. M. Pawlik, J. Ren, C. W. Sun, and T. M. Townes. 2006. Differential binding of erythroid Krupple-like factor to embryonic/fetal globin gene promoters during development. J. Biol. Chem. 281:16052-16057.
86. Zhou, Y., K. C. Lim, K. Onodera, S. Takahashi, J. Ohta, N. Minegishi, F. Y. Tsai, S. H. Orkin, M. Yamamoto, and J. D. Engel. 1998. Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA-2 in urogenital development. EMBO J. 17:6689-6700.
87. Zon, L. I., C. Mather, S. Burgess, M. E. Bolce, R. M. Harland, and S. H. Orkin. 1991. Expression of GATA-binding proteins during embryonic development in Xcnopus laevis. Proc. Natl. Acad. Sci. USA 88:10642-10646.