Role of PU.1 in MHC class II expression through transcriptional regulation of class II transactivator pI in dendritic cells

Kitamura, Nao; Yokoyama, Hokuto; Yashiro, Takuya; Nakano, Nobuhiro; Nishiyama, Makoto; Kanada, Shunsuke; Fukai, Tatsuo; Hara, Mutsuko; Ikeda, Shigaku; Ogawa, Hideoki; Okumura, Ko; Nishiyama, Chiharu

doi:10.1016/j.jaci.2011.10.019

Cited by 56Immunotherapy and Immune ResponsesGenomics and Chromatin DynamicsT-cell and B-cell Immunology

Role of PU.1 in MHC class II expression through transcriptional regulation of class II transactivator pI in dendritic cells

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Kitamura, Nao, Yokoyama, Hokuto, Yashiro, Takuya, Nakano, Nobuhiro, Nishiyama, Makoto, Kanada, Shunsuke, Fukai, Tatsuo, Hara, Mutsuko +4 more·2012·Journal of Allergy and Clinical Immunology

DOI 10.1016/j.jaci.2011.10.019

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Abstract

Background PU.1 is a hematopoietic cell-specific transcription factor belonging to the Ets family. We hypothesized that PU.1 is involved in MHC class II expression in dendritic cells (DCs). Objective The role of PU.1 in MHC class II expression in DCs was analyzed. Methods Transcriptional regulation of the DC-specific pI promoter of the class II transactivator (CIITA) gene and subsequent MHC class II expression was investigated by using PU.1 small interfering RNA (siRNA) and reporter, chromatin immunoprecipitation, and electrophoretic mobility shift assays. Results PU.1 siRNA introduction suppressed MHC class II expression, allogeneic and syngeneic T-cell activation activities of bone marrow-derived DCs (BMDCs) with reduction of CIITA mRNA driven by the DC-specific promoter pI, and MHC class II mRNA. The chromatin immunoprecipitation assay showed constitutive binding of PU.1 to the pI region in BMDCs, whereas acetylation of histone H3 on pI was suppressed by LPS stimulation in parallel with shutdown of CIITA transcription. PU.1 transactivated the pI promoter through cis-elements at -47/-44 and -30/-27 in a reporter assay and to which PU.1 directly bound in an electrophoretic mobility shift assay. Acetylation of histones H3 and H4 on pI was reduced in PU.1 siRNA-introduced BMDCs. Knockdown of interferon regulatory factor 4 or 8, which is a heterodimer partner of PU.1, by siRNA did not affect pI-driven CIITA transcription or MHC class II expression. Conclusion PU.1 basally transactivates the CIITA pI promoter in DCs by functioning as a monomeric transcription factor and by affecting histone modification, resulting in the subsequent expression and function of MHC class II.

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PU.1 regulates numerous gene programs associated with host defense and immune function, including expression of MHC and costimulatory genes, as well as immune checkpoints and immune effector genes.
“PU.1 regulates numerous gene programs associated with host defense and immune function, including expression of MHC and costimulatory genes, as well as immune checkpoints and immune effector genes (Fisher et al., 1998; Karpurapu et al., 2011; Kitamura et al., 2012; Keightley et al., 2017).”
From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Kitamura et al., 2012
The paper’s Abstract (page not provided) reports that PU.1 regulates CIITA pI and subsequent MHC class II expression in dendritic cells. It also describes prior work identifying PU.1 as a regulator of the costimulatory genes CD80 and CD86. Our copy does not support attributing regulation of immune checkpoint or immune effector genes to this paper. (LLM, conf=0.88)
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“PU.1 regulates numerous gene programs associated with host defense and immune function, including expression of MHC and costimulatory genes, as well as immune checkpoints and immune effector genes (Fisher et al., 1998; Karpurapu et al., 2011; Kitamura et al., 2012; Keightley et al., 2017).”
Background
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Publications from Juntendo University Graduate School of Medicine, 2012
(2014) · Juntendō Igaku/Juntendo igaku · doi:10.14789/jmj.60.258
Publications from Juntendo University Graduate School of Medicine, 2012 [5/6]
(2015) · Juntendō Igaku/Juntendo igaku · doi:10.14789/jmj.61.84
NR4A3 deficiency ameliorates contact hypersensitivity and exacerbates psoriasis by regulating gene expression in dendritic cellsPreprint
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Role of PU.1 in MHC Class II Expression via CIITA Transcription in Plasmacytoid Dendritic Cells
Miura, R., Kasakura, K., Nakano, N., Hara, M., Maeda, K., Okumura, K., Ogawa, H., Yashiro, T., & Nishiyama, C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154094 · Cited by 14 · see citing works
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Positive Regulatory Domain I (PRDM1) and IRF8/PU.1 Counter-regulate MHC Class II Transactivator (CIITA) Expression during Dendritic Cell Maturation
Smith, M. A., Wright, G. M., Wu, J., Tailor, P. B., Ozato, K., Chen, X., Wei, S., Piskurich, J. F., Ting, J. P. ‐., & Wright, K. L. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.165431 · Cited by 63 · see citing works
The hematopoietic cell-specific transcription factor PU.1 is critical for expression of CD11c
Yashiro, T., Kasakura, K., Oda, Y., Kitamura, N., Inoue, A., Nakamura, S., Yokoyama, H., Fukuyama, K., Hara, M., Ogawa, H., et al. (2017) · International Immunology · doi:10.1093/intimm/dxx009 · Cited by 14 · see citing works
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Critical Role of Transcription Factor PU.1 in the Expression of CD80 and CD86 on Dendritic Cells
Kanada, S., Nishiyama, C., Nakano, N., Suzuki, R., Maeda, K., Hara, M., Kitamura, N., Ogawa, H., & Okumura, K. (2011) · Blood · doi:10.1182/blood-2010-06-291898 · Cited by 73 · see citing works
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Dual Roles of PU.1 in the Expression of PD-L2: Direct Transactivation with IRF4 and Indirect Epigenetic Regulation
Inaba, K., Yashiro, T., Hiroki, I., Watanabe, R., Kasakura, K., & Nishiyama, C. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901008 · Cited by 13 · see citing works
Self-citation

Authors: Kitamura, N., Yokoyama, H., Yashiro, T., Nakano, N., Nishiyama, M., Kanada, S., Fukai, T., Hara, M., Ikeda, S., Ogawa, H., Okumura, K., & Nishiyama, C.
Affiliations: Juntendo University (JP)
The University of Tokyo (JP)
Corresponding author: Nishiyama, Chiharu
ORCID: Yashiro, Takuya
Nakano, Nobuhiro
Nishiyama, Makoto
Fukai, Tatsuo
Hara, Mutsuko
Ikeda, Shigaku
Ogawa, Hideoki
Okumura, Ko
Nishiyama, Chiharu
Venue: Journal of Allergy and Clinical Immunology
Publisher: Elsevier BV
Published: 2012-03
Volume: 129
Issue: 3
Pages: 814-824.e6
ISSN: 0091-6749 (ISSN-L)
DOI: 10.1016/j.jaci.2011.10.019
OpenAlex: W1974505259
Cited by: 55
References: 37
Citations by year: 2026: 3 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 1 · 2021: 4 · 2020: 9 · 2019: 3 · 2018: 3 · 2017: 4 · 2016: 3 · 2015: 7 · 2014: 3 · 2013: 2 · 2012: 2
FWCI: 0.93
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Allergy and Clinical Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: Ministry of Education, Culture, Sports, Science and Technology
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: PU.1, MHC class II expression, dendritic cells, transcriptional regulation, histone acetylation, histone modifications, ETS transcription factors, IRF4, IRF8, T cell activation, bone marrow-derived dendritic cells, promoter cis-acting elements
MeSH terms: Proto-Oncogene Protein Spi-1, Acetylation, Animals, Histocompatibility Antigens Class II, Bone Marrow Cells, Cells, Cultured, Dendritic Cells, Gene Expression Regulation, Histones, Lymphocyte Activation, Mice, Inbred BALB C, Mice, Inbred C57BL, Nuclear Proteins, Promoter Regions, Genetic, Proto-Oncogene Proteins, T-Lymphocytes, Transcriptional Activation, Trans-Activators, RNA, Small Interfering, Mice

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Role of PU.1 in MHC class II expression through transcriptional regulation of class II transactivator pI in dendritic cells

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