The Hox cofactors Meis1 and Pbx act upstream of gata1 to regulate primitive hematopoiesis

Developmental Biology

Volumn 340, Issue 2, 2010, Pages 306-317

  Pillay, Laura M ^a   Forrester, A Michael ^b   Erickson, Timothy ^a   Berman, Jason N ^b   Waskiewicz, Andrew Jan ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cdx; Erythroid; Erythropoiesis; Gata1; Hematopoiesis; Hemoglobin; Hox; Hoxb7a; Lmo2; Meis; Meis1; Myeloid; Myelopoiesis; Pbx; Pu.1; Scl; Spi1; Zebrafish

Indexed keywords

HEMOGLOBIN; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR MEIS1; TRANSCRIPTION FACTOR PBX; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ERYTHROID CELL; ERYTHROPOIESIS; HEMATOPOIESIS; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

EID: 77951204547     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.01.033     Document Type: Article

References (98)

1. Abramovich C., Humphries R.K. Hox regulation of normal and leukemic hematopoietic stem cells. Curr. Opin. Hematol. 2005, 12:210-216.
2. Abu-Shaar M., Ryoo H.D., Mann R.S. Control of the nuclear localization of Extradenticle by competing nuclear import and export signals. Genes Dev. 1999, 13:935-945.
3. Anderson K.L., Smith K.A., Conners K., McKercher S.R., Maki R.A., Torbett B.E. Myeloid development is selectively disrupted in PU.1 null mice. Blood 1998, 91:3702-3710.
4. Azcoitia V., Aracil M., Martinez A.C., Torres M. The homeodomain protein Meis1 is essential for definitive hematopoiesis and vascular patterning in the mouse embryo. Dev. Biol. 2005, 280:307-320.
5. Baumann R., Dragon S. Erythropoiesis and red cell function in vertebrate embryos. Eur. J. Clin. Invest. 2005, 35(Suppl 3):2-12.
6. Berthelsen J., Zappavigna V., Ferretti E., Mavilio F., Blasi F. The novel homeoprotein Prep1 modulates Pbx-Hox protein cooperativity. EMBO J. 1998, 17:1434-1445.
7. Berthelsen J., Zappavigna V., Mavilio F., Blasi F. Prep1, a novel functional partner of Pbx proteins. EMBO J. 1998, 17:1423-1433.
8. Berthelsen J., Kilstrup-Nielsen C., Blasi F., Mavilio F., Zappavigna V. The subcellular localization of PBX1 and EXD proteins depends on nuclear import and export signals and is modulated by association with PREP1 and HTH. Genes Dev. 1999, 13:946-953.
9. Bjornsson J.M., Larsson N., Brun A.C., Magnusson M., Andersson E., Lundstrom P., Larsson J., Repetowska E., Ehinger M., Humphries R.K., Karlsson S. Reduced proliferative capacity of hematopoietic stem cells deficient in Hoxb3 and Hoxb4. Mol. Cell. Biol. 2003, 23:3872-3883.
10. Brun A.C., Bjornsson J.M., Magnusson M., Larsson N., Leveen P., Ehinger M., Nilsson E., Karlsson S. Hoxb4-deficient mice undergo normal hematopoietic development but exhibit a mild proliferation defect in hematopoietic stem cells. Blood 2004, 103:4126-4133.
11. Chan S.K., Mann R.S. A structural model for a homeotic protein-extradenticle-DNA complex accounts for the choice of HOX protein in the heterodimer. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:5223-5228.
12. Chan S.K., Popperl H., Krumlauf R., Mann R.S. An extradenticle-induced conformational change in a HOX protein overcomes an inhibitory function of the conserved hexapeptide motif. EMBO J. 1996, 15:2476-2487.
13. Chang C.P., Shen W.F., Rozenfeld S., Lawrence H.J., Largman C., Cleary M.L. Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev. 1995, 9:663-674.
14. Chang C.P., Brocchieri L., Shen W.F., Largman C., Cleary M.L. Pbx modulation of Hox homeodomain amino-terminal arms establishes different DNA-binding specificities across the Hox locus. Mol. Cell. Biol. 1996, 16:1734-1745.
15. Chang C.P., Jacobs Y., Nakamura T., Jenkins N.A., Copeland N.G., Cleary M.L. Meis proteins are major in vivo DNA binding partners for wild-type but not chimeric Pbx proteins. Mol. Cell. Biol. 1997, 17:5679-5687.
16. Cooper K.L., Leisenring W.M., Moens C.B. Autonomous and nonautonomous functions for Hox/Pbx in branchiomotor neuron development. Dev. Biol. 2003, 253:200-213.
17. Davidson A.J., Zon L.I. The caudal-related homeobox genes cdx1a and cdx4 act redundantly to regulate hox gene expression and the formation of putative hematopoietic stem cells during zebrafish embryogenesis. Dev. Biol. 2006, 292:506-518.
18. Davidson A.J., Ernst P., Wang Y., Dekens M.P., Kingsley P.D., Palis J., Korsmeyer S.J., Daley G.Q., Zon L.I. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 2003, 425:300-306.
19. Di Rosa P., Villaescusa J.C., Longobardi E., Iotti G., Ferretti E., Diaz V.M., Miccio A., Ferrari G., Blasi F. The homeodomain transcription factor Prep1 (pKnox1) is required for hematopoietic stem and progenitor cell activity. Dev. Biol. 2007, 311:324-334.
20. DiMartino J.F., Selleri L., Traver D., Firpo M.T., Rhee J., Warnke R., O'Gorman S., Weissman I.L., Cleary M.L. The Hox cofactor and proto-oncogene Pbx1 is required for maintenance of definitive hematopoiesis in the fetal liver. Blood 2001, 98:618-626.
21. Dooley K.A., Davidson A.J., Zon L.I. Zebrafish scl functions independently in hematopoietic and endothelial development. Dev. Biol. 2005, 277:522-536.
22. Ebner A., Cabernard C., Affolter M., Merabet S. Recognition of distinct target sites by a unique Labial/Extradenticle/Homothorax complex. Development 2005, 132:1591-1600.
23. Erickson T., Scholpp S., Brand M., Moens C.B., Waskiewicz A.J. Pbx proteins cooperate with Engrailed to pattern the midbrain-hindbrain and diencephalic-mesencephalic boundaries. Dev. Biol. 2007, 301:504-517.
24. Ferretti E., Marshall H., Popperl H., Maconochie M., Krumlauf R., Blasi F. Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 2000, 127:155-166.
25. Ferretti E., Villaescusa J.C., Di Rosa P., Fernandez-Diaz L.C., Longobardi E., Mazzieri R., Miccio A., Micali N., Selleri L., Ferrari G., Blasi F. Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol. Cell. Biol. 2006, 26:5650-5662.
26. French C.R., Erickson T., Callander D., Berry K.M., Koss R., Hagey D.W., Stout J., Wuennenberg-Stapleton K., Ngai J., Moens C.B., Waskiewicz A.J. Pbx homeodomain proteins pattern both the zebrafish retina and tectum. BMC Dev. Biol. 2007, 7:85.
27. French C.R., Erickson T., French D.V., Pilgrim D.B., Waskiewicz A.J. Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development. Dev. Biol. 2009, 333:37-47.
28. Galloway J.L., Wingert R.A., Thisse C., Thisse B., Zon L.I. Loss of gata1 but not gata2 converts erythropoiesis to myelopoiesis in zebrafish embryos. Dev. Cell 2005, 8:109-116.
29. Gering M., Rodaway A.R., Gottgens B., Patient R.K., Green A.R. The SCL gene specifies haemangioblast development from early mesoderm. EMBO J. 1998, 17:4029-4045.
30. Gering M., Yamada Y., Rabbitts T.H., Patient R.K. Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development 2003, 130:6187-6199.
31. Gongal P.A., Waskiewicz A.J. Zebrafish model of holoprosencephaly demonstrates a key role for TGIF in regulating retinoic acid metabolism. Hum. Mol. Genet. 2008, 17:525-538.
32. Gottgens B., Nastos A., Kinston S., Piltz S., Delabesse E.C., Stanley M., Sanchez M.J., Ciau-Uitz A., Patient R., Green A.R. Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J. 2002, 21:3039-3050.
33. Hall C., Flores M.V., Storm T., Crosier K., Crosier P. The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish. BMC Dev. Biol. 2007, 7:42.
34. Hisa T., Spence S.E., Rachel R.A., Fujita M., Nakamura T., Ward J.M., Devor-Henneman D.E., Saiki Y., Kutsuna H., Tessarollo L., Jenkins N.A., Copeland N.G. Hematopoietic, angiogenic and eye defects in Meis1 mutant animals. EMBO J. 2004, 23:450-459.
35. Hove J.R., Koster R.W., Forouhar A.S., Acevedo-Bolton G., Fraser S.E., Gharib M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 2003, 421:172-177.
36. Iwasaki H., Mizuno S., Wells R.A., Cantor A.B., Watanabe S., Akashi K. GATA-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/erythrocyte lineages. Immunity 2003, 19:451-462.
37. Izon D.J., Rozenfeld S., Fong S.T., Komuves L., Largman C., Lawrence H.J. Loss of function of the homeobox gene Hoxa-9 perturbs early T-cell development and induces apoptosis in primitive thymocytes. Blood 1998, 92:383-393.
38. Jacobs Y., Schnabel C.A., Cleary M.L. Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol. Cell. Biol. 1999, 19:5134-5142.
39. Jaw T.J., You L.R., Knoepfler P.S., Yao L.C., Pai C.Y., Tang C.Y., Chang L.P., Berthelsen J., Blasi F., Kamps M.P., Sun Y.H. Direct interaction of two homeoproteins, homothorax and extradenticle, is essential for EXD nuclear localization and function. Mech. Dev. 2000, 91:279-291.
40. Kappen C. Disruption of the homeobox gene Hoxb-6 in mice results in increased numbers of early erythrocyte progenitors. Am. J. Hematol. 2000, 65:111-118.
41. Kilstrup-Nielsen C., Alessio M., Zappavigna V. PBX1 nuclear export is regulated independently of PBX-MEINOX interaction by PKA phosphorylation of the PBC-B domain. EMBO J. 2003, 22:89-99.
42. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
43. Knoepfler P.S., Lu Q., Kamps M.P. Pbx-1 Hox heterodimers bind DNA on inseparable half-sites that permit intrinsic DNA binding specificity of the Hox partner at nucleotides 3′ to a TAAT motif. Nucleic Acids Res. 1996, 24:2288-2294.
44. Knoepfler P.S., Calvo K.R., Chen H., Antonarakis S.E., Kamps M.P. Meis1 and pKnox1 bind DNA cooperatively with Pbx1 utilizing an interaction surface disrupted in oncoprotein E2a-Pbx1. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14553-14558.
45. Ko K.H., Lam Q.L., Zhang M., Wong C.K., Lo C.K., Kahmeyer-Gabbe M., Tsang W.H., Tsang S.L., Chan L.C., Sham M.H., Lu L. Hoxb3 deficiency impairs B lymphopoiesis in mouse bone marrow. Exp. Hematol. 2007, 35:465-475.
46. Kroon E., Thorsteinsdottir U., Mayotte N., Nakamura T., Sauvageau G. NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 2001, 20:350-361.
47. LaRonde-LeBlanc N.A., Wolberger C. Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev. 2003, 17:2060-2072.
48. Lawrence H.J., Helgason C.D., Sauvageau G., Fong S., Izon D.J., Humphries R.K., Largman C. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 1997, 89:1922-1930.
49. Le Guyader D., Redd M.J., Colucci-Guyon E., Murayama E., Kissa K., Briolat V., Mordelet E., Zapata A., Shinomiya H., Herbomel P. Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 2008, 111:132-141.
50. Lieschke G.J., Oates A.C., Crowhurst M.O., Ward A.C., Layton J.E. Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 2001, 98:3087-3096.
51. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
52. Longobardi E., Blasi F. Overexpression of PREP-1 in F9 teratocarcinoma cells leads to a functionally relevant increase of PBX-2 by preventing its degradation. J. Biol. Chem. 2003, 278:39235-39241.
53. Lyons S.E., Lawson N.D., Lei L., Bennett P.E., Weinstein B.M., Liu P.P. A nonsense mutation in zebrafish gata1 causes the bloodless phenotype in vlad tepes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5454-5459.
54. Magnusson M., Brun A.C., Lawrence H.J., Karlsson S. Hoxa9/hoxb3/hoxb4 compound null mice display severe hematopoietic defects. Exp. Hematol. 2007, 35:1421-1428.
55. Magnusson M., Brun A.C., Miyake N., Larsson J., Ehinger M., Bjornsson J.M., Wutz A., Sigvardsson M., Karlsson S. HOXA10 is a critical regulator for hematopoietic stem cells and erythroid/megakaryocyte development. Blood 2007, 109:3687-3696.
56. Mann R.S. The specificity of homeotic gene function. Bioessays 1995, 17:855-863.
57. Mann R.S., Affolter M. Hox proteins meet more partners. Curr. Opin. Genet. Dev. 1998, 8:423-429.
58. Mann R.S., Chan S.K. Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet. 1996, 12:258-262.
59. Maves L., Waskiewicz A.J., Paul B., Cao Y., Tyler A., Moens C.B., Tapscott S.J. Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation. Development 2007, 134:3371-3382.
60. McKercher S.R., Torbett B.E., Anderson K.L., Henkel G.W., Vestal D.J., Baribault H., Klemsz M., Feeney A.J., Wu G.E., Paige C.J., Maki R.A. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 1996, 15:5647-5658.
61. McNulty C.L., Peres J.N., Bardine N., van den Akker W.M., Durston A.J. Knockdown of the complete Hox paralogous group 1 leads to dramatic hindbrain and neural crest defects. Development 2005, 132:2861-2871.
62. Mercader N., Leonardo E., Azpiazu N., Serrano A., Morata G., Martinez C., Torres M. Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 1999, 402:425-429.
63. Minehata K., Kawahara A., Suzuki T. meis1 regulates the development of endothelial cells in zebrafish. Biochem. Biophys. Res. Commun. 2008, 374:647-652.
64. Moens C.B., Selleri L. Hox cofactors in vertebrate development. Dev. Biol. 2006, 291:193-206.
65. Nakamura T., Largaespada D.A., Shaughnessy J.D., Jenkins N.A., Copeland N.G. Cooperative activation of Hoxa and Pbx1-related genes in murine myeloid leukaemias. Nat. Genet. 1996, 12:149-153.
66. Nerlov C., Querfurth E., Kulessa H., Graf T. GATA-1 interacts with the myeloid PU.1 transcription factor and represses PU.1-dependent transcription. Blood 2000, 95:2543-2551.
67. Orkin S.H. GATA-binding transcription factors in hematopoietic cells. Blood 1992, 80:575-581.
68. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
69. Patterson L.J., Gering M., Eckfeldt C.E., Green A.R., Verfaillie C.M., Ekker S.C., Patient R. The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish. Blood 2007, 109:2389-2398.
70. Penkov D., Di Rosa P., Fernandez Diaz L., Basso V., Ferretti E., Grassi F., Mondino A., Blasi F. Involvement of Prep1 in the alphabeta T-cell receptor T-lymphocytic potential of hematopoietic precursors. Mol. Cell. Biol. 2005, 25:10768-10781.
71. Pevny L., Simon M.C., Robertson E., Klein W.H., Tsai S.F., D'Agati V., Orkin S.H., Costantini F. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 1991, 349:257-260.
72. Pineault N., Buske C., Feuring-Buske M., Abramovich C., Rosten P., Hogge D.E., Aplan P.D., Humphries R.K. Induction of acute myeloid leukemia in mice by the human leukemia-specific fusion gene NUP98-HOXD13 in concert with Meis1. Blood 2003, 101:4529-4538.
73. Popperl H., Rikhof H., Chang H., Haffter P., Kimmel C.B., Moens C.B. lazarus is a novel pbx gene that globally mediates hox gene function in zebrafish. Mol. Cell 2000, 6:255-267.
74. Rekhtman N., Radparvar F., Evans T., Skoultchi A.I. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev. 1999, 13:1398-1411.
75. Rhodes J., Hagen A., Hsu K., Deng M., Liu T.X., Look A.T., Kanki J.P. Interplay of pu.1 and gata1 determines myelo-erythroid progenitor cell fate in zebrafish. Dev. Cell 2005, 8:97-108.
76. Rieckhof G.E., Casares F., Ryoo H.D., Abu-Shaar M., Mann R.S. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 1997, 91:171-183.
77. Ryoo H.D., Marty T., Casares F., Affolter M., Mann R.S. Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 1999, 126:5137-5148.
78. Sarno J.L., Kliman H.J., Taylor H.S. HOXA10, Pbx2, and Meis1 protein expression in the human endometrium: formation of multimeric complexes on HOXA10 target genes. J. Clin. Endocrinol. Metab. 2005, 90:522-528.
79. Scott E.W., Simon M.C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 1994, 265:1573-1577.
80. Shanmugam K., Green N.C., Rambaldi I., Saragovi H.U., Featherstone M.S. PBX and MEIS as non-DNA-binding partners in trimeric complexes with HOX proteins. Mol. Cell. Biol. 1999, 19:7577-7588.
81. Shen W.F., Montgomery J.C., Rozenfeld S., Moskow J.J., Lawrence H.J., Buchberg A.M., Largman C. AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol. Cell. Biol. 1997, 17:6448-6458.
82. Shen W.F., Rozenfeld S., Lawrence H.J., Largman C. The Abd-B-like Hox homeodomain proteins can be subdivided by the ability to form complexes with Pbx1a on a novel DNA target. J. Biol. Chem. 1997, 272:8198-8206.
83. Shen W.F., Rozenfeld S., Kwong A., Kom ves L.G., Lawrence H.J., Largman C. HOXA9 forms triple complexes with PBX2 and MEIS1 in myeloid cells. Mol. Cell. Biol. 1999, 19:3051-3061.
84. Shimamoto T., Tang Y., Naot Y., Nardi M., Brulet P., Bieberich C.J., Takeshita K. Hematopoietic progenitor cell abnormalities in Hoxc-8 null mutant mice. J. Exp. Zool. 1999, 283:186-193.
85. Shivdasani R.A., Mayer E.L., Orkin S.H. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 1995, 373:432-434.
86. Shivdasani R.A., Fujiwara Y., McDevitt M.A., Orkin S.H. A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in megakaryocyte growth and platelet development. EMBO J. 1997, 16:3965-3973.
87. Slape C., Aplan P.D. The role of NUP98 gene fusions in hematologic malignancy. Leuk. Lymphoma 2004, 45:1341-1350.
88. So C.W., Karsunky H., Wong P., Weissman I.L., Cleary M.L. Leukemic transformation of hematopoietic progenitors by MLL-GAS7 in the absence of Hoxa7 or Hoxa9. Blood 2004, 103:3192-3199.
89. Stevens K.E., Mann R.S. A balance between two nuclear localization sequences and a nuclear export sequence governs extradenticle subcellular localization. Genetics 2007, 175:1625-1636.
90. Stopka T., Amanatullah D.F., Papetti M., Skoultchi A.I. PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J. 2005, 24:3712-3723.
91. Vlachakis N., Choe S.K., Sagerstrom C.G. Meis3 synergizes with Pbx4 and Hoxb1b in promoting hindbrain fates in the zebrafish. Development 2001, 128:1299-1312.
92. Warren A.J., Colledge W.H., Carlton M.B., Evans M.J., Smith A.J., Rabbitts T.H. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell 1994, 78:45-57.
93. Waskiewicz A.J., Rikhof H.A., Hernandez R.E., Moens C.B. Zebrafish Meis functions to stabilize Pbx proteins and regulate hindbrain patterning. Development 2001, 128:4139-4151.
94. Waskiewicz A.J., Rikhof H.A., Moens C.B. Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Dev. Cell 2002, 3:723-733.
95. Williams T.M., Williams M.E., Innis J.W. Range of HOX/TALE superclass associations and protein domain requirements for HOXA13:MEIS interaction. Dev. Biol. 2005, 277:457-471.
96. Zhang D.E., Hohaus S., Voso M.T., Chen H.M., Smith L.T., Hetherington C.J., Tenen D.G. Function of PU.1 (Spi-1), C/EBP, and AML1 in early myelopoiesis: regulation of multiple myeloid CSF receptor promoters. Curr. Top. Microbiol. Immunol. 1996, 211:137-147.
97. Zhang P., Behre G., Pan J., Iwama A., Wara-Aswapati N., Radomska H.S., Auron P.E., Tenen D.G., Sun Z. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8705-8710.
98. Zhang P., Zhang X., Iwama A., Yu C., Smith K.A., Mueller B.U., Narravula S., Torbett B.E., Orkin S.H., Tenen D.G. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 2000, 96:2641-2648.