In vivo complex formation of PU.1 with HDAC1 associated with PU.1-mediated transcriptional repression

Kihara-Negishi, Fumiko; Yamamoto, Hitomi; Suzuki, Mitsuhiro; Yamada, Toshiyuki; Sakurai, Takuya; Tamura, Takaaki; Oikawa, Tsuneyuki

doi:10.1038/sj.onc.1204756

Cited by 65Genomics and Chromatin DynamicsHistone Deacetylase Inhibitors ResearchEpigenetics and DNA Methylation

In vivo complex formation of PU.1 with HDAC1 associated with PU.1-mediated transcriptional repression

Kihara-Negishi, Fumiko, Yamamoto, Hitomi, Suzuki, Mitsuhiro, Yamada, Toshiyuki, Sakurai, Takuya, Tamura, Takaaki, Oikawa, Tsuneyuki·2001·Oncogene

DOI 10.1038/sj.onc.1204756

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Abstract

We previously reported that overexpression of PU.1, a member of the Ets family of transcription factors, induces differentiation inhibition and apoptosis associated with c-Myc down-regulation in murine erythroleukemia (MEL) cells. To understand the molecular mechanism by which c-Myc is down-regulated due to overexpression of PU.1, we performed luciferase reporter assays using the mouse c-myc promoter. PU.1 repressed the activities of not only the c-myc promoter but also several other promoters. Experiments with deletion mutants of PU.1 revealed that the C-terminal region spanning amino acids (aa) 123-272 including the PEST and ETS domains but not the activation domain was sufficient for this transcriptional repression. It was unlikely that the repression was due to sequestration of a limited amount of CBP/p300 nor pCAF, because overexpression of these co-activators did not relieve PU.1-mediated transcriptional repression. Instead, it was found that the C-terminal aa 101-272 of PU.1 formed a complex with mSin3A and HDAC1 in vivo, which was speculated to be associated with the repression. The C-terminal region of PU.1 also formed a complex with the basic transcription factor TBP in vitro and in vivo. Our results suggest that overexpression of PU.1 induces transcriptional repression in several gene promoters including the c-myc promoter which may be mediated by its complex formation with HDACs.

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PU.1 can interact with coactivators or corepressors to function as either a transcriptional activator or a transcriptional repressor.
“PU.1 can interact with coactivators or corepressors to function as either a transcriptional activator or a transcriptional repressor.17–19”
From RUNX1 regulates corepressor interactions of PU.1 (2011) · cites this paper as [19]
There is limited understanding of the mechanisms that determine coactivator versus corepressor recruitment by RUNX1 and PU.1.
“There is limited understanding of the mechanisms that determine coactivator versus corepressor recruitment by RUNX1 and PU.1.17–20”
From RUNX1 regulates corepressor interactions of PU.1 (2011) · cites this paper as [19]
The mechanisms that regulate corepressor versus coactivator interactions of RUNX1 and PU.1 are incompletely understood.
“However, the mechanisms that regulate corepressor versus coactivator interactions of RUNX1 and PU.1 are incompletely understood.17–20”
From RUNX1 regulates corepressor interactions of PU.1 (2011) · cites this paper as [19]
Prior studies indicate that PU.1 can be recruited to the Myc promoter in complex with histone deacetylase proteins.
“in line with prior studies indicating that PU.1 can be recruited to the Myc promoter in complex with histone deacetylase proteins (Kihara-Negishi et al., 2001).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Kihara-Negishi et al., 2001

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Method
Safeguard function of PU.1 shapes the inflammatory epigenome of neutrophils
Fischer, J., Walter, C., Tönges, A., Aleth, H., Jordão, M. J. C., Leddin, M., Gröning, V., Erdmann, T., Lenz, G., Roth, J., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0343-z · Cited by 56 · see citing works
Dynamic Protein Associations Define Two Phases of IL-1β Transcriptional Activation
Zhang, Y., Saccani, S., Shin, H., & Nikolajczyk, B. S. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.1.503 · Cited by 57 · see citing works
Up regulation of GW112 Gene by NFκB promotes an antiapoptotic property in gastric cancer cells
Kim, K. K., Park, K., Song, S., & Kim, K. (2010) · Molecular Carcinogenesis · doi:10.1002/mc.20596 · Cited by 53 · see citing works
Epigenetic control of hematopoiesis: the PU.1 chromatin connection
van Riel, B., & Rosenbauer, F. (2014) · Biological Chemistry · doi:10.1515/hsz-2014-0195 · Cited by 47 · see citing works
Transcriptional Activators, Repressors, and Epigenetic Modifiers Controlling Hematopoietic Stem Cell Development
Teitell, M. A., & Mikkola, H. K. A. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000205155.26315.c7 · Cited by 47 · see citing works
“1 also can participate in a co-repressor complex with histone deacetylase (HDAC) activity and directly binds DNMTs 3a and 3b to direct DNA methylation (58,59).”
Background
BCR-ABL1 mediated miR-150 downregulation through MYC contributed to myeloid differentiation block and drug resistance in chronic myeloid leukemia
Šrůtová, K., Čuřík, N., Burda, P., et al. (2018) · Haematologica · doi:10.3324/haematol.2018.193086 · Cited by 46 · see citing works
“By the dashed lines we outlined regulations that we assumed based on published observations.(15,17,18,24,25,27) A B”
BackgroundMethod
Transcriptional Regulation of Mouse μ Opioid Receptor Gene by PU.1
Hwang, C. K., Kim, C. S., Choi, H. S., McKercher, S. R., & Loh, H. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400755200 · Cited by 46 · see citing works
Regulating the Regulators: The Role of Histone Deacetylase 1 (HDAC1) in Erythropoiesis
Kim, M. Y., Yan, B., Huang, S., & Qiu, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228460 · Cited by 44 · see citing works
PU.1 Suppresses Th2 Cytokine Expression via Silencing of GATA3 Transcription in Dendritic Cells
Yashiro, T., Kubo, M., Ogawa, H., Okumura, K., & Nishiyama, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137699 · Cited by 41 · see citing works
Cooperative interaction between ETS1 and GFI1 transcription factors in the repression of Bax gene expression
Nakazawa, Y., Suzuki, M., Manabe, N., Yamada, T., Kihara‐Negishi, F., Sakurai, T., Tenen, D. G., Iwama, A., Mochizuki, M., & Oikawa, T. (2007) · Oncogene · doi:10.1038/sj.onc.1210140 · Cited by 39 · see citing works
“1, another member of the ETS family, also forms a complex with mSin3A/HDAC1 and MeCP2 under certain conditions (Kihara-Negishi et al., 2001; Suzuki et al., 2003; Hwang et al., 2004).”
BackgroundSelf-citation
Overlapping CRE and E Box Motifs in the Enhancer Sequences of the Bovine Leukemia Virus 5′ Long Terminal Repeat Are Critical for Basal and Acetylation-Dependent Transcriptional Activity of the Viral Promoter: Implications for Viral Latency
Calomme, C., Dekoninck, A., Nizet, S., Adam, E., Nguyên, T. L.-A., den Broeke, A. V., Willems, L., Kettmann, R., Burny, A., & Lint, C. M. V. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13848-13864.2004 · Cited by 39 · see citing works
“1 (43) and glucocorticoid receptor (35), have been shown to interact with deacetylases.”
Background
Going ballistic: Leishmania nuclear subversion of host cell plasticity
Lecoeur, H., Prina, E., Gutiérrez-Sanchez, M., & Späth, G. F. (2021) · Trends in Parasitology · doi:10.1016/j.pt.2021.09.009 · Cited by 36 · see citing works
“1 further forms a complex with the corepressor mSin3A and HDAC1 to reduce the expression of C-MYC, which is a key regulator of M2-like polarization [30].”
Background
Identification and characterization of a PU.1/Spi-B binding site in the bovine leukemia virus long terminal repeat
Dekoninck, A., Calomme, C., Nizet, S., de Launoit, Y., Burny, A., Ghysdael, J., & Lint, C. M. V. (2003) · Oncogene · doi:10.1038/sj.onc.1206392 · Cited by 34 · see citing works
“…to interact with chromatin-modifying enzymes: the histone acetyltransferase CREB binding protein (CBP) (Yamamoto et al., 1999) (which also interacts with Spi-B, Yamamoto et al., 2002) and the histone deacetylase HDAC1 (Kihara-Negishi et al., 2001), further implicating PU.1 in chromatin remodeling.”
Background
Open Chromatin Profiling in Adipose Tissue Marks Genomic Regions with Functional Roles in Cardiometabolic Traits
Cannon, M. E., Currin, K. W., Young, K. L., Perrin, H. J., Vadlamudi, S., Safi, A., Song, L., Wu, Y., Wabitsch, M., Laakso, M., et al. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400294 · Cited by 32 · see citing works
Role of hypoxia in the regulation of periovulatory EDN2 expression in the mouseThis article is one of a selection of papers published in the special issue (part 1 of 2) on Forefronts in Endothelin.
Na, G., Bridges, P. J., Koo, Y., et al. (2008) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y08-025 · Cited by 31 · see citing works
“2006) and the c-myc gene by forming a complex with mSin3A and HDAC1 in vivo (Kihara-Negishi et al. 2001).”
Background
HDAC1 and PRC2 mediate combinatorial control in SPI1/PU.1-dependent gene repression in murine erythroleukaemia
Gregoricchio, S., Polit, L., Esposito, M., Berthelet, J., Delestré, L., Evanno, E., Diop, M., Gallais, I., Aleth, H., Poplineau, M., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac613 · Cited by 27 · see citing works
“SPI1, SIN3A and HDAC1 seem to belong to the same complex as deduced from their co-immunoprecipitations with SIN3A and HDAC1 (Figure 2A).”
BackgroundInfluential
Epigenetic Mechanisms in the Dopamine D2 Receptor-Dependent Inhibition of the Prolactin Gene
Liu, J., Baker, R. E., Chow, W., Sun, C. K., & Elsholtz, H. P. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0111 · Cited by 30 · see citing works
NGF activation of TrkA decreases N-myc expression via MAPK path leading to a decrease in neuroblastoma cell number
Woo, C., Lucarelli, E., & Thiele, C. J. (2003) · Oncogene · doi:10.1038/sj.onc.1207267 · Cited by 30 · see citing works
Metallothionein-1 Isoforms and Vimentin Are Direct PU.1 Downstream Target Genes in Leukemia Cells
Imoto, A., Okada, M., Okazaki, T., Kitasato, H., Harigae, H., & Takahashi, S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.095810 · Cited by 28 · see citing works
The Ewing Sarcoma Protein (EWS) Binds Directly to the Proximal Elements of the Macrophage-Specific Promoter of the CSF-1 Receptor ( csf1r ) Gene
Hume, D. A., Sasmono, R. T., Himes, S. R., Sharma, S. M., Bronisz, A., Constantin, M., Ostrowski, M. C., & Ross, I. L. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.10.6733 · Cited by 28 · see citing works
Epstein-Barr Virus EBNA-3C Is Targeted to and Regulates Expression from the Bidirectional LMP-1/2B Promoter
Jiménez-Ramírez, C., Brooks, A. J., Forshell, L. P., Yakimchuk, K., Zhao, B., Fulgham, T. Z., & Sample, C. E. (2006) · Journal of Virology · doi:10.1128/jvi.00897-06 · Cited by 25 · see citing works
“1 associates with HDAC1, which leads to a repression of transcription (34).”
Background
Modeling the Hematopoietic Landscape
Brown, G., & Ceredig, R. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00104 · Cited by 25 · see citing works
Inverse correlation between Flt3 and PU.1 expression in acute myeloblastic leukemias
Inomata, M., Takahashi, S., Harigae, H., Kameoka, J., Kaku, M., & Sasaki, T. (2005) · Leukemia Research · doi:10.1016/j.leukres.2005.07.015 · Cited by 22 · see citing works
Molecular basis of Stat1 and PU.1 cooperation in cytokine-induced Fc receptor I promoter activation
Aittomäki, S. (2004) · International Immunology · doi:10.1093/intimm/dxh037 · Cited by 18 · see citing works
PU.1/Spi-1 Binds to the Human TAL-1 Silencer to Mediate its Activity
Clech, M. L., Chalhoub, E., Dohet, C., Roure, V., Fichelson, S., Moreau-Gachelin, F., & Mathieu-Mahul, D. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.10.055 · Cited by 18 · see citing works
Identification of annexin 1 as a PU.1 target gene in leukemia cells
Iseki, Y., Imoto, A., Okazaki, T., Harigae, H., & Takahashi, S. (2009) · Leukemia Research · doi:10.1016/j.leukres.2009.04.010 · Cited by 17 · see citing works
Deacetylase Inhibitors and the Viral Transactivator TaxBLV Synergistically Activate Bovine Leukemia Virus Gene Expression via a cAMP-responsive Element- and cAMP-responsive Element-binding Protein-dependent Mechanism
Nguyên, T. L.-A., Calomme, C., Wijmeersch, G., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404081200 · Cited by 16 · see citing works
Impaired repressor activity and biological functions of PU.1 in MEL cells induced by mutations in the acetylation motifs within the ETS domain
Kihara-Negishi, F., Suzuki, M., Yamada, T., Sakurai, T., & Oikawa, T. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.07.098 · Cited by 13 · see citing works
Self-citation
The differentiating and apoptotic effects of 2-aza-5′-deoxycytidine are dependent on the PU.1 expression level in PU.1-transgenic K562 cells
Aoyama, S., Nakano, H., Danbara, M., Higashihara, M., Harigae, H., & Takahashi, S. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.03.071 · Cited by 13 · see citing works
Strategies to generate functionally normal neutrophils to reduce infection and infection-related mortality in cancer chemotherapy
Abdel‐Azim, H., Sun, W., & Wu, L. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107403 · Cited by 13 · see citing works
Subsurface Interactions of Actinide Species with Microorganisms
Reed, D. T., Deo, R. P., & Rittmann, B. E. (2010) · Springer eBooks · doi:10.1007/978-94-007-0211-0_33 · Cited by 12 · see citing works
Interaction between the homeodomain protein HOXC13 and ETS family transcription factor PU.1 and its implication in the differentiation of murine erythroleukemia cells
Yamada, T., Shimizu, T., Suzuki, M., Kihara‐Negishi, F., Nanashima, N., Sakurai, T., Yang, F., Akita, M., Oikawa, T., & Tsuchida, S. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.11.005 · Cited by 11 · see citing works
Self-citation
Epigenetic regulation of the metallothionein-1A promoter by PU.1 during differentiation of THP-1 cells
Suzuki, S., Nakano, H., & Takahashi, S. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.03.007 · Cited by 10 · see citing works
Extensive remodeling of DC function by rapid maturation-induced transcriptional silencing
Seguín-Estévez, Q., Dunand-Sauthier, I., Lemeille, S., Iseli, C., Ibberson, M. R., Ioannidis, V., Schmid, C. D., Rousseau, P., Barras, E., Geinoz, A., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku674 · Cited by 11 · see citing works
“1 has been attributed to its ability to recruit HDACs (40,41), a mechanism consistent with the finding that histone-deacetylation is the primary event associated with the silencing process we have unveiled.”
Background
HDAC6 regulates human erythroid differentiation through modulation of JAK2 signalling
Vong, P., Messaoudi, K., Jankovsky, N., Gomilla, C., Demont, Y., Caulier, A., Jedraszak, G., Demagny, J., Djordjevic, S., Boyer, T., et al. (2022) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17559 · Cited by 8 · see citing works
Genetic determination of the role of PU.1 in macrophage gene expression
Joo, M., Kwon, M., Azim, A. C., Sadikot, R. T., Blackwell, T. S., & Christman, J. W. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.04.189 · Cited by 8 · see citing works
Combinatorial Control of DNase I-hypersensitive Site Formation and Erasure by Immunoglobulin Heavy Chain Enhancer-binding Proteins
Ishii, H., Sen, R., & Pazin, M. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m308973200 · Cited by 6 · see citing works
PU.1, a Versatile Transcription Factor and a Suppressor of Myeloid Leukemia
Takahashi, S. (2011) · InTech eBooks · doi:10.5772/25853 · Cited by 2 · see citing works
“1 formed a complex with mSin3A and HDAC1 in vivo (Kihara-Negishi et al., 2001) (Figure 1).”
BackgroundInfluential
Hematopoietic Stem Cell Development and Transcriptional Regulation
Gekas, C. (2008) · Työväentutkimus Vuosikirja
Reduced PU.1 concentrations lead to hematopoietic stem cell defects and lineage-inappropriate gene expression.
Kamath, M. B. (2009) · OhioLink ETD Center (Ohio Library and Information Network)
The Transcription Factor ERG is a Gatekeeper of Endothelial Cell Homeostasis
Dryden, N. H. (2012) · Spiral (Imperial College London) · doi:10.25560/9798
Anomalies moléculaires dans la macroglobulinémie de Waldenström : identification d’une mutation somatique récurrente dans le gène codant pour le facteur de transcription SPI1/PU.1 et description de ses conséquences fonctionnelles
Roos‐Weil, D. (2018) · doi:10.70675/1030cb13z12b8z4f7cz8f8az165206a6209a
Impacts fonctionnels et conséquences sur la différenciation hématopoïétique d’une mutation somatique récurrente du gène PU.1/SPI1 identifiée dans la macroglobulinémie de Waldenström
Decaudin, C. (2020) · doi:10.70675/e84f591cz6a69z4d60z9d03z6267895b1a9e
Rôle de l'histone désacétylase HDAC6 au cours de l'érythropoïèse humaine
Vong, P. (2022) · doi:10.70675/699e8d9bz5404z43f6zabe7zdd0f0b6c8c42

Nuclear receptor corepressors partner with class II histone deacetylases in a Sin3-independent repression pathwayPreprint
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Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression
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Authors: Kihara-Negishi, F., Yamamoto, H., Suzuki, M., Yamada, T., Sakurai, T., Tamura, T., & Oikawa, T.
Affiliations: Sasaki Institute (JP)
Corresponding author: Oikawa, Tsuneyuki
ORCID: Yamada, Toshiyuki
Sakurai, Takuya
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2001-09-20
Volume: 20
Issue: 42
Pages: 6039-6047
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1204756
OpenAlex: W2335217055
Cited by: 65
References: 48
Citations by year: 2022: 4 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 2 · 2015: 2 · 2014: 2 · 2013: 1 · 2012: 2
FWCI: 1.76
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: PU.1, HDAC1, transcriptional repression, ETS transcription factors, mSin3A, histone deacetylase, TATA-binding protein, c-myc promoter
MeSH terms: Proto-Oncogene Protein Spi-1, Cell Line, DNA-Binding Proteins, HeLa Cells, Histone Deacetylases, Humans, Mutation, Promoter Regions, Genetic, Proto-Oncogene Proteins

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In vivo complex formation of PU.1 with HDAC1 associated with PU.1-mediated transcriptional repression

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