PU.1 (Spi-1) and C/EBPα Regulate Expression of the Granulocyte-Macrophage Colony-Stimulating Factor Receptor α Gene
Open accessAbstract
Growth factor receptors play an important role in hematopoiesis. In order to further understand the mechanisms directing the expression of these key regulators of hematopoiesis, we initiated a study investigating the transcription factors activating the expression of the granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor alpha gene. Here, we demonstrate that the human GM-CSF receptor alpha promoter directs reporter gene activity in a tissue-specific fashion in myelomonocytic cells, which correlates with its expression pattern as analyzed by reverse transcription PCR. The GM-CSF receptor alpha promoter contains an important functional site between positions -53 and -41 as identified by deletion analysis of reporter constructs. We show that the myeloid and B cell transcription factor PU.1 binds specifically to this site. Furthermore, we demonstrate that a CCAAT site located upstream of the PU.1 site between positions -70 and -54 is involved in positive-negative regulation of the GM-CSF receptor alpha promoter activity. C/EBP alpha is the major CCAAT/enhancer-binding protein (C/EBP) form binding to this site in nuclear extracts of U937 cells. Point mutations of either the PU.1 site or the C/EBP site that abolish the binding of the respective factors result in a significant decrease of GM-CSF receptor alpha promoter activity in myelomonocytic cells only. Furthermore, we demonstrate that in myeloid and B cell extracts, PU.1 forms a novel, specific, more slowly migrating complex (PU-SF) when binding the GM-CSF receptor alpha promoter PU.1 site. This is the first demonstration of a specific interaction with PU.1 on a myeloid PU.1 binding site. The novel complex is distinct from that described previously as binding to B cell enhancer sites and can be formed by addition of PU.1 to extracts from certain nonmyeloid cell types which do not express PU.1, including T cells and epithelial cells, but not from erythroid cells. Furthermore, we demonstrate that the PU-SF complex binds to PU.1 sites found on a number of myeloid promoters, and its formation requires an intact PU.1 site adjacent to a single-stranded region. Expression of PU.1 in nonmyeloid cells can activate the GM-CSF receptor alpha promoter. Deletion of the amino-terminal region of PU.1 results in a failure to form the PU-SF complex and in a concomitant loss of transactivation, suggesting that formation of the PU-SF complex is of functional importance for the activity of the GM-CSF receptor alpha promoter. Finally, we demonstrate that C/EBP alpha can also active the GM-CSF receptor alpha promoter in nonmyeloid cells. These results suggest that PU.1 and C/EBP alpha direct the cell-type-specific expression of GM-CSF receptor alpha, further establish the role of PU.1 as a key regulator of hematopoiesis, and point to C/EBP alpha as an additional important factor in this process.
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PU.1 regulates vast number of myeloid gene promoters including GM-CSF receptor α, M-CSF receptor, CD163, and CD11b.
“PU.1 imparts its key functions by regulating vast number of myeloid gene promoters that include GM-CSF receptor a, M-CSF receptor (M-CSFR), scavenger receptor CD163, and CD11b, etc (6,7).”
From FBW7 Inhibits Myeloid Differentiation in Acute Myeloid Leukemia via GSK3-Dependent Ubiquitination of PU.1 (2021) · cites this paper as [6]
The Discussion (page not supplied) says that most myeloid cell-specific promoters contain functional PU.1 sites, including the M-CSF receptor promoter, and identifies a functional PU.1 site in the GM-CSF receptor α promoter. The paper also names CD11b as a previously described myeloid PU.1 target. Our copy does not identify CD163 as a PU.1-regulated promoter, so the full list is not supported. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn cotransfection experiments, RUNX1, PU.1, and CEBPA play essential roles in activation of the hematopoietic differentiation genes MCSFR and GMCSFR.
“In cotransfection experiments, RUNX1, PU.1, and CEBPA play essential roles in activation of the hematopoietic differentiation genes MCSFR and GMCSFR.7,8,31”
From RUNX1 regulates corepressor interactions of PU.1 (2011) · cites this paper as [31]
The Results report that cotransfected PU.1 and C/EBPα each increased GM-CSF receptor α promoter activity, supporting that part of the sentence. This paper does not report cotransfection evidence for RUNX1 or activation of the M-CSF receptor gene; it mentions the latter as another PU.1-regulated promoter. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn myeloid lineages, putative PU.1 target genes include G-SCF receptor, GM-CSF receptor and M-CSF receptor.
“In myeloid lineages, the putative PU.1 target genes include G-SCF receptor [23], GM-CSF receptor [24] and M-CSF receptor [25].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
C/EBP-α expression is prominent in immature myeloid cells.
“C/EBP-α expression is prominent in immature myeloid cells [24, 101].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
Each factor (PU.1 and C/EBP-α) has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase (NE) promoter.
“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase (NE) promoter [24, 63].”
From PU.1 and partners: regulation of haematopoietic stem cell fate in normal and malignant haematopoiesis (2009) · cites this paper as [24]
C/EBP-α weakly activates several myeloid cell-specific promoters, including those for cytokine receptors and granule proteins.
“C/EBP-␣ minimally activates several myeloid cell-specific promoters, including those for cytokine receptors (e.g., GM-CSF, G-CSF, and M-CSF receptors) (26,65,78,79) and granule proteins (e.g., NE) (50).”
From The t(8;21) Fusion Product, AML-1–ETO, Associates with C/EBP-α, Inhibits C/EBP-α-Dependent Transcription, and Blocks Granulocytic Differentiation (1998) · cites this paper as [26]
C/EBP-α cooperates with other myeloid transcription factors, including AML-1B and PU.1, to synergistically upregulate several myeloid cell-specific promoters.
“Moreover, C/EBP-␣ cooperates with other myeloid transcription factors, including AML-1B and PU.1, to synergistically upregulate the expression of several myeloid cellspecific promoters (26,50,78).”
From The t(8;21) Fusion Product, AML-1–ETO, Associates with C/EBP-α, Inhibits C/EBP-α-Dependent Transcription, and Blocks Granulocytic Differentiation (1998) · cites this paper as [26]
C/EBPα and PU.1 synergize on various promoters, including the M-CSF receptor promoter and the neutrophil elastase promoter.
“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase promoter.15,35”
From Granulocyte inducer C/EBPα inactivates the myeloid master regulator PU.1: possible role in lineage commitment decisions (2002) · cites this paper as [15]
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Lekstrom-Himes, J., & Xanthopoulos, K. G. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.28545 · Cited by 801 · see citing works
Transcription Factors, Normal Myeloid Development, and Leukemia
Tenen, D. G., Hromas, R., Licht, J. D., & Zhang, D.-E. (1997) · Blood · doi:10.1182/blood.v90.2.489 · Cited by 735 · see citing works
Cowland, J. B., & Borregaard, N. (1997) · Genomics · doi:10.1006/geno.1997.4896 · Cited by 619 · see citing works
Disruption of differentiation in human cancer: AML shows the way
Tenen, D. G. (2003) · Nature Reviews Cancer · doi:10.1038/nrc989 · Cited by 612 · see citing works
Shi, Y., Liu, C. H., Roberts, A. I., Das, J., Xu, G., Ren, G., Zhang, Y., Zhang, L., Yuan, Z., Tan, H. S., et al. (2006) · Cell Research · doi:10.1038/sj.cr.7310017 · Cited by 550 · see citing works
Fröhling, S., Schlenk, R. F., Stolze, I., Bihlmayr, J., Benner, A., Kreitmeier, S., Tobis, K., Döhner, H., & Döhner, K. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.06.060 · Cited by 458 · see citing works
“regulates the promoters of a number of granulocyte-specific genes [18-22].”
BackgroundZhang, D.-E., Hetherington, C. J., Meyers, S., Rhoades, K. L., Larson, C. J., Chen, H.-M., Hiebert, S. W., & Tenen, D. G. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.3.1231 · Cited by 396 · see citing works
Self-citationEts target genes: past, present and future
Sementchenko, V. I., & Watson, D. K. (2000) · Oncogene · doi:10.1038/sj.onc.1204034 · Cited by 371 · see citing works
“…Reddy et al., 1994; Ross et al., 1998; cells, RAW 264, Repression Zhang et al., 1994, 1996) NIH3T3, Cos by TEL GM-CSF-R U937 PU.1 TGAGGAAGCA d,m (Hohaus et al., 1995) gc chain (subunit of IL R) Raji, Jurkat EBS ACCGGAAGCT d,m (Markiewicz et al., 1996) AGAGGAAACG TCR a Jurkat Ets1 CACATCCTCT f,t…”
BackgroundTranscriptional regulation of granulocyte and monocyte development
Friedman, A. D. (2002) · Oncogene · doi:10.1038/sj.onc.1205324 · Cited by 325 · see citing works
“The widespread role of C/EBPs and PU.1 in regulating myeloid genes combined with the defects evident in C/ EBPa (7/7) and PU.1 (7/7) mice make these transcription factors leading candidates for roles in determining the myeloid lineages.”
BackgroundInfluentialDeKoter, R. P., Walsh, J. C., & Singh, H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.15.4456 · Cited by 296 · see citing works
“…the promoters of genes encoding the myeloidspecific cytokine receptor subunits, granulocyte–macrophage colony-stimulating factor receptor α (GM-CSFRα) (Hohaus et al., 1995), c-Fms (Reddy et al., 1994; Zhang et al., 1994) and granulocyte colony-stimulating factor receptor (G-CSFR) (Smith et al.,…”
BackgroundGombart, A. F., Hofmann, W., Kawano, S., Takeuchi, S., Krug, U. O., Kwok, S. H., Larsen, R. J., Asou, H., Miller, C. W., Hoelzer, D. F., et al. (2002) · Blood · doi:10.1182/blood.v99.4.1332 · Cited by 288 · see citing works
“Lodie et al 56 reported that the PML/RARaprotein product resulting from the acute promyelocytic leukemia translocation t(15;17) physically interacts with C/EBP a.”
Carotta, S., Dakic, A., D'Amico, A., Pang, S. H. M., Greig, K. T., Nutt, S. L., & Wu, L. (2010) · Immunity · doi:10.1016/j.immuni.2010.05.005 · Cited by 279 · see citing works
“As the gene encoding the GM-CSFRa chain (Csf2ra) is a known PU.1 target gene (Hohaus et al., 1995), these findings suggest that PU.1 is required for the complementary functions of GM-CSFR and Flt3 in supporting (E) The number of DCs of each phenotype generated in fetal liver or LSK cell cultur per…”
BackgroundWestendorf, J. J., Yamamoto, C. M., Lenny, N., Downing, J. R., Selsted, M. E., & Hiebert, S. W. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.1.322 · Cited by 270 · see citing works
“The AML-1B(1-290) mutant and its variants lack three of these residues but retain the major phosphorylation site, S276.”
BackgroundInfluentialVangala, R. K., Heiss-Neumann, M. S., Rangatia, J. S., Singh, S. M., Schoch, C., Tenen, D. G., Hiddemann, W., & Behre, G. (2003) · Blood · doi:10.1182/blood-2002-04-1288 · Cited by 245 · see citing works
Self-citationHeterozygous PU.1 mutations are associated with acute myeloid leukemia
Mueller, B. U., Pabst, T., Osato, M., Asou, N., Johansen, L. M., Minden, M. D., Behre, G., Hiddemann, W., Ito, Y., & Tenen, D. G. (2002) · Blood · doi:10.1182/blood.v100.3.998 · Cited by 243 · see citing works
C/EBP, c-Myb, and PU.1 Cooperate To Regulate the Neutrophil Elastase Promoter
Oelgeschläger, M., Nuchprayoon, I., Lüscher, B., & Friedman, A. D. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.4717 · Cited by 229 · see citing works
“C/EBPais present in immature myeloid cells and cell lines, including 32D cl3 cells, as demonstrated by Western blot and EMSAstudies( 19 ,39),whereasexpressionofC/EBPbismore prominentandpredominatesinmaturemyeloidcells(39).The functional C/EBP site in the NE promoter was identified in induced 32D cl3 cells (30); howeve…”
BackgroundMethodInfluentialKim, W., Sieweke, M., Ogawa, E., Wee, H., Englmeier, U., Graf, T., & Ito, Y. (1999) · The EMBO Journal · doi:10.1093/emboj/18.6.1609 · Cited by 230 · see citing works
“…the bZip transcription factor C/EBPα and the Ets family member PU.1 in transactivation of the macrophage colony stimulating factor receptor promoter (Hohaus et al., 1995; Zhang et al., 1996; Kanno et al., 1998) but does not display mutual cooperative DNA binding with these proteins (T.Kanno and…”
BackgroundNF-IL6 and NF-kappa B in cytokine gene regulation.
Akira, S., & Kishimoto, T. (1997) · PubMed · Cited by 231 · see citing works
Thyroid-specific gene expression
Damante, G., & Lauro, R. D. (1994) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/0167-4781(94)90176-7 · Cited by 214 · see citing works
Multiple Functional Domains of AML1: PU.1 and C/EBPα Synergize with Different Regions of AML1
Petrovick, M. S., Hiebert, S. W., Friedman, A. D., Hetherington, C. J., Tenen, D. G., & Zhang, D.-E. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.3915 · Cited by 223 · see citing works
“mAML1A(1-288) is terminated at amino acid 288 of AML1A.”
BackgroundMethodInfluentialTranscription factors that regulate monocyte/macrophage differentiation
Valledor, A. F., Borràs, F. E., Cullell-Young, M., & Celada, A. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.63.4.405 · Cited by 211 · see citing works
Role of the transcription factor AML-1 in acute leukemia and hematopoietic differentiation
Lutterbach, B. A., & Hiebert, S. W. (2000) · Gene · doi:10.1016/s0378-1119(00)00014-7 · Cited by 209 · see citing works
Interrogation of human hematopoiesis at single-cell and single-variant resolution
Ulirsch, J. C., Lareau, C. A., Bao, E. L., Ludwig, L. S., Guo, M. H., Benner, C., Satpathy, A. T., Kartha, V. K., Salem, R. M., Hirschhorn, J. N., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0362-6 · Cited by 208 · see citing works
NF-IL6 and NF-κB in Cytokine Gene Regulation
Akira, S., & Kishimoto, T. (1997) · Advances in immunology · doi:10.1016/s0065-2776(08)60740-3 · Cited by 201 · see citing works
Park, D. J., Chumakov, A. M., Vuong, P. T., Chih, D. Y., Gombart, A. F., Miller, W. H., & Koeffler, H. P. (1999) · Journal of Clinical Investigation · doi:10.1172/jci2887 · Cited by 187 · see citing works
Roberta Morosetti, A., Park, D. J., Chumakov, A. M., Grillier‐Vuissoz, I., Shiohara, M., Gombart, A. F., Nakamaki, T., Weinberg, K. I., & Koeffler, H. P. (1997) · Blood · doi:10.1182/blood.v90.7.2591 · Cited by 188 · see citing works
Olson, M. C., Scott, E. W., Hack, A. A., Su, G. H., Tenen, D. G., Singh, H., & Simon, M. C. (1995) · Immunity · doi:10.1016/1074-7613(95)90060-8 · Cited by 191 · see citing works
Self-citationMyeloid Development Is Selectively Disrupted in PU.1 Null Mice
Anderson, K. L., Smith, K. A., Conners, K., McKercher, S. R., Maki, R. A., & Torbett, B. E. (1998) · Blood · doi:10.1182/blood.v91.10.3702 · Cited by 193 · see citing works
Anderson, M. K., Weiss, A. H., Hernandez-Hoyos, G., Dionne, C. J., & Rothenberg, E. V. (2002) · Immunity · doi:10.1016/s1074-7613(02)00277-7 · Cited by 182 · see citing works
Distinct transcription factor networks control neutrophil-driven inflammation
Khoyratty, T. E., Ai, Z.-C., Ballesteros, I., Eames, H. L., Mathie, S., Martín-Salamanca, S., Wang, L., Hemmings, A., Willemsen, N., von Werz, V., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-00968-4 · Cited by 167 · see citing works
Potential Autoregulation of Transcription Factor PU.1 by an Upstream Regulatory Element
Okuno, Y., Huang, G., Rosenbauer, F., Evans, E. K., Radomska, H. S., Iwasaki, H., Akashi, K., Moreau-Gachelin, F., Li, Y., Zhang, P., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.7.2832-2845.2005 · Cited by 174 · see citing works
Wang, X., Scott, E., Sawyers, C. L., & Friedman, A. D. (1999) · Blood · doi:10.1182/blood.v94.2.560 · Cited by 166 · see citing works
Lécuyer, É. (2002) · Blood · doi:10.1182/blood-2002-02-0568 · Cited by 165 · see citing works
Neuronal death and survival in two models of hypoxic-ischemic brain damage
Walton, M. R., Connor, B. J., Lawlor, P. A., Young, D., Sirimanne, E. S., Gluckman, P. D., Cole, G. M., & Dragunow, M. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00053-8 · Cited by 164 · see citing works
ETS transcription factors and regulation of immunity
Gallant, S., & Gilkeson, G. S. (2006) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-006-0017-z · Cited by 163 · see citing works
“1-binding sites within the G-CSF receptor α-subunit promoter are suspected regulators of its expression [70, 166].”
BackgroundAnderson, K. L., Perkin, H. B., Surh, C. D., Venturini, S., Maki, R. A., & Torbett, B. E. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.4.1855 · Cited by 159 · see citing works
Fisher, R. C., & Scott, E. W. (1998) · STEM CELLS · doi:10.1002/stem.160025 · Cited by 158 · see citing works
Reddy, V. A., Iwama, A., Iotzova, G., Schulz, M., Elsasser, A., Vangala, R. K., Tenen, D. G., Hiddemann, W., & Behre, G. (2002) · Blood · doi:10.1182/blood.v100.2.483 · Cited by 152 · see citing works
Self-citationGombart, A. F., Kwok, S. H., Anderson, K. L., Yamaguchi, Y., Torbett, B. E., & Koeffler, H. P. (2003) · Blood · doi:10.1182/blood-2002-04-1039 · Cited by 151 · see citing works
The key role of PU.1/SPI-1 in B cells, myeloid cells and macrophages
Lloberas, J., Soler, C., & Celada, A. (1999) · Immunology Today · doi:10.1016/s0167-5699(99)01442-5 · Cited by 142 · see citing works
Rosmarin, A. G., Yang, Z., & Resendes, K. K. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2004.08.015 · Cited by 142 · see citing works
Neutrophils Deficient in PU.1 Do Not Terminally Differentiate or Become Functionally Competent
Anderson, K. L., Smith, K. A., Pio, F., Torbett, B. E., & Maki, R. A. (1998) · Blood · doi:10.1182/blood.v92.5.1576 · Cited by 142 · see citing works
Dichotomy of AML1-ETO Functions: Growth Arrest versus Block of Differentiation
Burel, S. A., Harakawa, N., Zhou, L., Pabst, T., Tenen, D. G., & Zhang, D. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.16.5577-5590.2001 · Cited by 140 · see citing works
The Role of C/EBPε in the Terminal Stages of Granulocyte Differentiation
Lekstrom‐Himes, J. A. (2001) · STEM CELLS · doi:10.1634/stemcells.19-2-125 · Cited by 127 · see citing works
Regulation of granulopoiesis by transcription factors and cytokine signals
Ward, A. C., Loeb, D., Soede-Bobok, A. A., Touw, I., & Friedman, A. (2000) · Leukemia · doi:10.1038/sj.leu.2401808 · Cited by 131 · see citing works
Calvo, K. R., Sykes, D. B., Pasillas, M. P., & Kamps, M. P. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.9.3274-3285.2000 · Cited by 126 · see citing works
PU.1 determines the self-renewal capacity of erythroid progenitor cells
Back, J., Dierich, A., Bronn, C., Kastner, P., & Chan, S. (2004) · Blood · doi:10.1182/blood-2003-11-4089 · Cited by 123 · see citing works
Du, J., Stankiewicz, M. J., Liu, Y., Xi, Q., Schmitz, J. E., Lekstrom-Himes, J. A., & Ackerman, S. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204777200 · Cited by 120 · see citing works
Rehli, M., Lichanska, A., Cassady, A. I., Ostrowski, M. C., & Hume, D. A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.3.1559 · Cited by 116 · see citing works
Gu, X., Ebrahem, Q., Mahfouz, R. Z., Hasipek, M., Enane, F. O., Radivoyevitch, T., Rapin, N., Przychodzen, B. P., Hu, Z., Balusu, R., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci97117 · Cited by 114 · see citing works
Regulation of eosinophil‐specific gene expression by a C/EBP–Ets complex and GATA‐1
McNagny, K. M., Sieweke, M. H., Döderlein, G., Graf, T., & Nerlov, C. (1998) · The EMBO Journal · doi:10.1093/emboj/17.13.3669 · Cited by 108 · see citing works
“…the genes encoding the receptors for the myeloid growth factors granulocyte (G)-, macrophage (M)- and GMcolony-stimulating factor (CSF) all contain binding sites for C/EBP and PU.1 (and, in the case of M-CSF, a receptor for AML-1 also) (Hohaus et al., 1995; Smith et al., 1996; Zhang et al., 1996).”
BackgroundRegulation of the PU.1 gene by distal elements
Li, Y., Okuno, Y., Zhang, P., Radomska, H. S., Chen, H.-M., Iwasaki, H., Akashi, K., Klemsz, M. J., McKercher, S. R., Maki, R. A., et al. (2001) · Blood · doi:10.1182/blood.v98.10.2958 · Cited by 110 · see citing works
The Role of Ets Transcription Factors in the Development and Function of the Mammalian Immune System
Bassuk, A. G., & Leiden, J. M. (1997) · Advances in immunology · doi:10.1016/s0065-2776(08)60887-1 · Cited by 110 · see citing works
Rı́us, C., Smith, J. D., Almendro, N., Langa, C., Botella, L. M., Marchuk, D. A., Vary, C., & Bernabéu, C. (1998) · Blood · doi:10.1182/blood.v92.12.4677 · Cited by 111 · see citing works
Oikawa, T., Yamada, T., Kihara-Negishi, F., Yamamoto, H., Kondoh, N., Hitomi, Y., & Hashimoto, Y. (1999) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4400534 · Cited by 109 · see citing works
Mutations of CEBPA in acute myeloid leukemia FAB types M1 and M2
Snaddon, J., Smith, M. L., Neat, M. J., Cambal‐Parrales, M., Dixon‐McIver, A., Arch, R., Amess, J. A. L., Rohatiner, A. Z. S., Lister, T. A., & Fitzgibbon, J. (2003) · Genes Chromosomes and Cancer · doi:10.1002/gcc.10185 · Cited by 108 · see citing works
“C/EBP is important in the regulation of myeloid differentiation, being expressed particularly in early myeloid cells, in addition to regulating a number of granulocyte-specific genes (Hohaus et al., 1995; Oelgeschlager et al., 1996; Smith et al., 1996; Petrovick et al., 1998).”
BackgroundThe RUNX1–PU.1 axis in the control of hematopoiesis
Imperato, M. R., Cauchy, P., Obier, N., & Bonifer, C. (2015) · International Journal of Hematology · doi:10.1007/s12185-015-1762-8 · Cited by 94 · see citing works
“1 is a master regulator of later hematopoiesis and is required for commitment to the myeloid lineage since together with C/EBPα it controls the expression of the receptors for GM-CSF [46], and of CSF-1 which are critical cytokines for myelopoiesis [47, 48].”
BackgroundA tumor suppressor role for C/EBPα in solid tumors: more than fat and blood
Lourenço, A. R., & Coffer, P. J. (2017) · Oncogene · doi:10.1038/onc.2017.151 · Cited by 101 · see citing works
The Transcription Factor PU.1 is a Critical Regulator of Cellular Communication in the Immune System
Turkistany, S. A., & DeKoter, R. P. (2011) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-011-0147-9 · Cited by 96 · see citing works
Visualizing PU.1 activity during hematopoiesis
Back, J., Allman, D., Chan, S., & Kastner, P. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2004.12.010 · Cited by 97 · see citing works
Suh, H. C., Gooya, J., Renn, K., Friedman, A. D., Johnson, P. F., & Keller, J. R. (2006) · Blood · doi:10.1182/blood-2005-06-2216 · Cited by 95 · see citing works
Obesity-Induced Changes in Bone Marrow Homeostasis
Beňová, A., & Tencerová, M. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00294 · Cited by 95 · see citing works
“1/Spi-1 is involved in myeloid lineage determination via regulation of target genes, including granulocyte colony-stimulating factor receptor (31), granulocyte-macrophage colony-stimulating factor receptor (32) and macrophage colony-stimulating factor receptor (33).”
BackgroundUse of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU.1 and C/EBP
Iwama, A., Zhang, P., Darlington, G. J., McKercher, S. R., Maki, R., & Tenen, D. G. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.12.3034 · Cited by 91 · see citing works
Wang, Q., & Friedman, A. D. (2002) · Blood · doi:10.1182/blood.v99.8.2776 · Cited by 88 · see citing works
Yamada, T., Kondoh, N., Matsumoto, M., Yoshida, M., Maekawa, A., & Oikawa, T. (1997) · Blood · doi:10.1182/blood.v89.4.1383 · Cited by 91 · see citing works
Behre, G., Singh, S. M., Liu, H., Bortolin, L. T., Christopeit, M., Radomska, H. S., Rangatia, J., Hiddemann, W., Friedman, A. D., & Tenen, D. G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202301200 · Cited by 81 · see citing works
Surprising new roles for PU.1 in the adaptive immune response
Carotta, S., Wu, L., & Nutt, S. L. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00955.x · Cited by 93 · see citing works
“1 is Csf2ra, the gene coding for the GM-CSFRa chain (26).”
BackgroundPan, Z., Hetherington, C. J., & Zhang, D. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.33.23242 · Cited by 80 · see citing works
PU.1 but not ets-2 is essential for macrophage development from embryonic stem cells
Henkel, G., McKercher, Sr., Yamamoto, H., Anderson, K., Oshima, R., & Maki, R. (1996) · Blood · doi:10.1182/blood.v88.8.2917.bloodjournal8882917 · Cited by 76 · see citing works
Ross, I. L., Xie, Y., Ostrowski, M. C., & Hume, D. A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.6662 · Cited by 78 · see citing works
Gupta, P., Gurudutta, G. U., Saluja, D., & Tripathi, R. P. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00757.x · Cited by 74 · see citing works
“Each factor has been shown to synergize on various promoters, including M-CSF receptor promoter and neutrophil elastase (NE) promoter [24, 63].”
BackgroundA Two-Step Mechanism for Recruitment of Pip by PU.1
Perkel, J. M., & Atchison, M. L. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.1.241 · Cited by 77 · see citing works
PU.1 and Haematopoietic Cell Fate: Dosage Matters
Mak, K. S., Funnell, A. P. W., Pearson, R. C. M., & Crossley, M. (2011) · International Journal of Cell Biology · doi:10.1155/2011/808524 · Cited by 77 · see citing works
Transcriptional control of B cell development and function
Bartholdy, B., & Matthias, P. (2003) · Gene · doi:10.1016/j.gene.2003.11.008 · Cited by 75 · see citing works
GABP Cooperates With c-Myb and C/EBP to Activate the Neutrophil Elastase Promoter
Nuchprayoon, I., Simkevich, C. P., Luo, M., Friedman, A. D., & Rosmarin, A. G. (1997) · Blood · doi:10.1182/blood.v89.12.4546 · Cited by 73 · see citing works
Myeloid-specific gene expression
Clarke, S., & Gordon, S. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.63.2.153 · Cited by 72 · see citing works
“Cloned Myeloid-Restricted Genes Gene Binding sites and response regions References Genes primarily expressed in macrophages M-CSF receptor (c-fms) PU.1,* PEBP2/CBF,* C/EBPa* (h) PU.1, PEBP2/CBF (m) [17, 56, 57, 91, 92] Macrophage scavenger receptor (MSR) TPA response region of AP-1/Ets-2,* PU.1* (h) [94, 97] Lipopolys…”
BackgroundInfluentialWalton, M. R., Gibbons, H., MacGibbon, G. A., Sirimanne, E., Saura, J., Gluckman, P. D., & Dragunow, M. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00262-3 · Cited by 73 · see citing works
Epigenetic regulator genes direct lineage switching in MLL/AF4 leukemia
Tirtakusuma, R., Szoltysek, K., Milne, P., Grinev, V. V., Ptasinska, A., Chin, P. S., Meyer, C., Nakjang, S., Hehir‐Kwa, J. Y., Williamson, D., et al. (2022) · Blood · doi:10.1182/blood.2021015036 · Cited by 73 · see citing works
Role of Transcription Factors C/EBPa and PU.1 in Normal Hematopoiesis and Leukemia
Koschmieder, S., Rosenbauer, F., Steidl, U., Owens, B. M., & Tenen, D. G. (2005) · International Journal of Hematology · doi:10.1532/ijh97.05051 · Cited by 72 · see citing works
Transcriptional regulation during myelopoiesis
Lenny, N. T., Westendorf, J. J., & Hiebert, S. W. (1997) · Molecular Biology Reports · doi:10.1023/a:1006859700409 · Cited by 73 · see citing works
Verbeek, W., Gombart, A. F., Chumakov, A. M., Müller‐Tidow, C., Friedman, A. D., & Koeffler, H. P. (1999) · Blood · doi:10.1182/blood.v93.10.3327 · Cited by 72 · see citing works
PU.1 Is Essential for p47 Promoter Activity in Myeloid Cells
Li, S.-L., Valente, A. J., Zhao, S.-J., & Clark, R. A. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.28.17802 · Cited by 71 · see citing works
Ji, M. H., Li, H., Suh, H. C., Klarmann, K. D., Yokota, Y., & Keller, J. R. (2008) · Blood · doi:10.1182/blood-2008-01-133504 · Cited by 71 · see citing works
Transcriptional regulation of neutrophil differentiation and function during inflammation
Ai, Z.-C., & Udalova, I. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.1ru1219-504rr · Cited by 55 · see citing works
Garner, H., Martinovic, M., Liu, N. Q., Bakker, N. A. M., Velilla, I. Q., Hau, C., Vrijland, K., Kaldenbach, D., Kok, M., de Wit, E., et al. (2025) · Cancer Cell · doi:10.1016/j.ccell.2025.04.007 · Cited by 68 · see citing works
Autocrine Induction of the Human Pro-IL-1β Gene Promoter by IL-1β in Monocytes
Toda, Y., Tsukada, J., Misago, M., Kominato, Y., Auron, P. E., & Tanaka, Y. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.4.1984 · Cited by 65 · see citing works
Ritter, M., Buechler, C., Langmann, T., & Schmitz, G. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0866 · Cited by 66 · see citing works
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Is PU.1 a dosage-sensitive regulator of haemopoietic lineage commitment and leukaemogenesis?
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Familial CEBPA-mutated acute myeloid leukemia
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RUNX1 regulates corepressor interactions of PU.1
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c-Jun Homodimers Can Function as a Context-Specific Coactivator
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“1 or C/EBP is enhanced through association with multiple protein partners (26, 53, 60, 61).”
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- Authors
- Hohaus, S., Petrovick, M. S., Voso, M. T., Sun, Z., Zhang, D.-E., & Tenen, D. G.
- Affiliations
- Harvard University (US)
- Corresponding author
- Tenen, Daniel G.
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 1995-10-01
- Volume
- 15
- Issue
- 10
- Pages
- 5830-5845
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC230835
- OpenAlex
- W2161743101
- Cited by
- 284
- References
- 73
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 3 · 2020: 6 · 2019: 6 · 2018: 7 · 2017: 5 · 2016: 5 · 2015: 8 · 2014: 5 · 2013: 7 · 2012: 6
- FWCI
- 5.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Funders
- American Lung Association
- National Cancer Institute (CA 41456, R01CA041456)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK048660, DK48660)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- PU.1, SPI-1, C/EBPα, GM-CSF receptor alpha, transcription factor binding sites, myelomonocytic cells, B cells, promoter regulation, transcriptional activation, hematopoiesis, single-stranded DNA binding, U937 cells
- MeSH terms
- Amino Acid Sequence, B-Lymphocytes, Base Sequence, Cell Line, DNA, DNA-Binding Proteins, DNA, Single-Stranded, Hematopoiesis, Humans, Methylation, Molecular Sequence Data, Monocytes, Mutation, Nuclear Proteins, Promoter Regions, Genetic, T-Lymphocytes, Transcription Factors, Transcriptional Activation, Retroviridae Proteins, Oncogenic, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Genes, Reporter, CCAAT-Enhancer-Binding Proteins
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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