Cited by 111interferon and immune responsesCytokine Signaling Pathways and InteractionsT-cell and B-cell Immunology

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Expression of IFN regulatory factor family proteins in lymphocytes. Induction of Stat-1 and IFN consensus sequence binding protein expression by T cell activation

Nelson, N, Kanno, Y, Hong, C, Contursi, C, Fujita, T, Fowlkes, B J, O’Connell, E, Hu-Li, J, Paul, W E, Jankovic, D, Sher, A F, Coligan, J E, Thornton, A, Appella, E, Yang, Y, Ozato, K·1996·The Journal of Immunology

DOI 10.4049/jimmunol.156.10.3711

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Abstract

Interferon consensus sequence binding protein (ICSBP) is a transcription factor of the IFN regulatory factor (IRF) family. Evidence indicates that this family has a function in the immune system. Unlike other members of the family, ICSBP is expressed exclusively in the immune system. In this work, immunoblot analysis was performed to study expression of ICSBP and other members of the family in various murine lymphocytes. The results show that all IRF family members are expressed constitutively in B cells throughout development, and in resting and activated cells. In contrast, ICSBP expression was undetectable in thymocytes and resting T cells, while all other IRF proteins tested (IRF-1, IRF-2, and ISGF3-γ) were detected in these cells. Induction of ICSBP (and weakly IRF-1, but not other members) was observed upon activation of T cells following anti-CD3 Ab binding or Con A stimulation. Once T cells were activated, ICSBP was expressed stably in both Th1 and Th2 cells. We show that Stat-1, which binds to the IFN-γ-responsive element of the ICSBP promoter, was induced following anti-CD3 Ab and Con A stimulation. Stat-1 induction was found in T cells of IFN-γ+/+, but not of IFN-γ-/- mice, indicating that T cell activation stimulates the Stat pathway of transcription that is mediated through IFN-γ. IFN-γ-activated Stat-1 partly accounted for ICSBP induction in activated T cells, as levels of induction were lower in IFN-γ-/- than in IFN+/+ T cells. Taken together, these results show that activation of ICSBP is coupled with T cell activation that is partly due to IFN-γ-induced Stat-1.

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Background
Differential Requirement of IFN Consensus Sequence Binding Protein for the Production of IL-12 and Induction of Th1-Type Cells in Response to IFN-γ
Wu, C.-Y., Maeda, H., Contursi, C., Ozato, K., & Seder, R. A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.2.807 · Cited by 31
Self-citation
USP 4 interacts and positively regulates IRF 8 function via K48‐linked deubiquitination in regulatory T cells
Lin, R., Nie, J., Ren, J., Liang, R., Li, D., Wang, P., Gao, C., Zhuo, C., Yang, C., & Li, B. (2017) · FEBS Letters · doi:10.1002/1873-3468.12668 · Cited by 31
Interferon Consensus Sequence-binding Protein Is Constitutively Expressed and Differentially Regulated in the Ocular Lens
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Expression patterns of transcription factors in progressively transformed germinal centers and Hodgkin lymphoma
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Dual Function of the IRF8 Transcription Factor in Autoimmune Uveitis: Loss of IRF8 in T Cells Exacerbates Uveitis, Whereas Irf8 Deletion in the Retina Confers Protection
Kim, S.-H., Burton, J. H., Yu, C., Sun, L., He, C., Wang, H., Morse, H. C., & Egwuagu, C. E. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500653 · Cited by 28
“In contrast, IRF8 is not expressed in naive T cells, but is rapidly induced in response to antigenic stimulation or TCR activation (5), suggesting that it may be required for regulating genes involved in T cell differentiation and/or effector functions.”
BackgroundResult
Two Genetic Variations in the IRF8 region are associated with Behçet’s disease in Han Chinese
Jiang, Y., Wang, H., Yu, H., Li, L., Xu, D., Hou, S., Kijlstra, A., & Yang, P. (2016) · Scientific Reports · doi:10.1038/srep19651 · Cited by 27
Stimulation strength controls the rate of initiation but not the molecular organisation of TCR-induced signalling
Ma, C. Y., Marioni, J. C., Griffiths, G. M., & Richard, A. C. (2020) · eLife · doi:10.7554/elife.53948 · Cited by 22
“Nr4a1 (Nur77) and Irf8 encode transcription factors that are rapidly expressed upon T cell activation (Moran et al., 2011; Nelson et al., 1996), and we previously found that their transcripts are upregulated at 1 and 3 hr, respectively, after strong N4 stimulation (Richard et al., 2018; Figure…”
Background
Retinoic Acid and Polyriboinosinic Acid Act Synergistically to Enhance the Antibody Response to Tetanus Toxoid during Vitamin A Deficiency: Possible Involvement of Interleukin‐2 Receptor‐β, Signal Transducer and Activator of Transcription‐1, and Interferon Regulatory Factor‐1
DeCicco-Skinner, K. L., Zolfaghari, R., Li, N., & Ross, A. C. (2000) · The Journal of Infectious Diseases · doi:10.1086/315908 · Cited by 22
“Two of these factors, IRF-1 and IRF-2, induce numerous antiviral genes, play roles in humoral and cell-mediated immunity [19-21], and often act as regulatory opposites, with IRF-1 activating and IRF-2 repressing the transcription of genes regulated by type I IFNs [19].”
Background
Interferon in chronic myeloid leukaemia: past and future
Guilhot, F., Roy, L., Saulnier, P., & Guilhot, J. (2009) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2009.10.005 · Cited by 23
“ICSBP is expressed mainly in haematopoietic cells [13,14].”
Background
Inhibition of interferon-γ-induced nitric oxide production by 10-hydroxy-trans-2-decenoic acid through inhibition of interferon regulatory factor-8 induction
Takahashi, K., Sugiyama, T., Tokoro, S., Neri, P., & Mori, H. (2011) · Cellular Immunology · doi:10.1016/j.cellimm.2011.11.004 · Cited by 21
IRF-8 regulates expansion of myeloid-derived suppressor cells and Foxp3+ regulatory T cells and modulates Th2 immune responses to gastrointestinal nematode infection
Valanparambil, R. M., Tam, M., Gros, P.-P., Auger, J.-P., Segura, M., Gros, P., Jardim, A., Geary, T. G., Ozato, K., & Stevenson, M. M. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006647 · Cited by 19
“IRF-8 is essential for the development of various myeloid-derived cells including macrophages, dendritic cells (DC), eosinophils, and basophils, but negatively regulates neutrophil differentiation [2, 3].”
BackgroundSelf-citation
Berberine inhibits IFN-γ signaling pathway in DSS-induced ulcerative colitis
Yang, T., Ma, X., Wang, R., et al. (2022) · Saudi Pharmaceutical Journal · doi:10.1016/j.jsps.2022.03.015 · Cited by 19
“In addition, IFN-c activator factor (GAF), as a dimer of interferon, can bind to the IFN-c activation site (GAS) and then up-regulate interferon regulatory factor 8 (IRF8) (Nelson et al., 1996).”
The development of immune-modulating compounds to disrupt HIV latency
Remoli, A. L., Marsili, G., Battistini, A., & Sgarbanti, M. (2012) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2012.05.003 · Cited by 18
“IRF-1 expression, which is high in activated but not in resting CD4+ T cells [57] is further enhanced by HIV-1 infection and prior to Tat expression [58].”
Background
Interferon Regulator Factor 8 (IRF8) Limits Ocular Pathology during HSV-1 Infection by Restraining the Activation and Expansion of CD8+ T Cells
Sun, L., Leger, A. J. S., Yu, C., He, C., Mahdi, R. M., Chan, C., Wang, H., Morse, H. C., & Egwuagu, C. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155420 · Cited by 19
“While expression of IRF8 is rapidly induced in T cells in response to TCR activation and/or cytokine stimulation, the role of IRF8 in the development or effector functions of T cells is less well understood [6].”
Background
HIV and Interferon Regulatory Factor 1: A Story of Manipulation and Control
Sivro, A., Su, R., Plummer, F. A., & Ball, T. B. (2013) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2013.0098 · Cited by 16
“This is supported by observations that latent proviruses can be reactivated by stimulating the host T cells with mitogens and anti-CD3-CD28 antibodies,(4,32,33) where both IRF1 and NF-jB are present at higher levels in activated T cells compared to resting cells.(10,34,35) Consistent with this, proinflammatory cytokin…”
Lack of Interferon Consensus Sequence Binding Protein (ICSBP) Transcripts in Human Myeloid Leukemias
Schmidt, M., Nagel, S., Proba, J., et al. (1998) · Blood · doi:10.1182/blood.v91.1.22.22_22_29 · Cited by 13
Inhibition of Monocytic Differentiation by Phosphorylation‐deficient Stat1 is Associated with Impaired Expression of Stat2, ICSBP/IRF8 and C/EBPɛ
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Ocular Behcet’s disease is associated with aberrant methylation of interferon regulatory factor 8 (IRF8) in monocyte-derived dendritic cells
Qiu, Y., Zhu, Y., Yu, H., Yi, S., Su, W., Cao, Q., Yuan, G., Kijlstra, A., & Yang, P. (2017) · Oncotarget · doi:10.18632/oncotarget.17235 · Cited by 11
“A previous study shows that IRF8 is not expressed in naïve T cells until they are stimulated by antigens or following TCR activation, suggesting that IRF8 may be required in the process of regulating genes that are involved in T cell differentiation and/or effector functions [23].”
Influential
Cinnamaldehyde inhibits cytokine storms induced by the ORF3a protein of SARS‐CoV ‐2 via ROS ‐elimination in activated T cells
Ma, J., Chen, X., Xue, R., Wang, F., Dong, J., Tao, N., & Qin, Z. (2023) · Phytotherapy Research · doi:10.1002/ptr.8016 · Cited by 9
“Stat-1 (Nelson et al., 1996) and AP-1 (Yukawa et al., 2020)”
Immunotherapy in Chronic Myelogenous Leukemia
Guilhot, F., Roy, L., Martineau, G., Guilhot, J., & Millot, F. (2007) · Clinical Lymphoma & Myeloma · doi:10.3816/clm.2007.s.004 · Cited by 9
Differential Requirements for IRF-2 in Generation of CD1d-Independent T Cells Bearing NK Cell Receptors
Notake, T., Horisawa, S., Sanjo, H., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200210 · Cited by 8
“Ly49 gene expression, as IRF-2 was expressed comparably in IL2–expanded Ly49 and Ly49 T cells and in lymph node T cells (33), which contained many fewer Ly49 T cells than those in the”
Method
STEM CELLS IN CHRONIC MYELOGENOUS LEUKEMIA
Verfaillie, C. M. (1997) · Hematology/Oncology Clinics of North America · doi:10.1016/s0889-8588(05)70484-6 · Cited by 8
Interferon‐regulatory factors during development of CD4 and CD8 thymocytes
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Evasion of interferon-mediated immune response by arteriviruses
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HIV-1 Targeting of IFN Regulatory Factors
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Interferon regulatory factor 8 regulates expression of acid ceramidase and infection susceptibility in cystic fibrosis
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“(2021) 296 100650 The Jak/Stat pathway, which is activated by interferons, has been previously shown to stimulate expression of IRF proteins (32).”
Background
Identification and characterization of interferon regulatory factor 8 (IRF8) in Nile tilapia (Oreochromis niloticus)
Sun, H., Li, C. L., Lei, Y., Wang, Y., Li, B., & Ye, J. (2025) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2025.110426 · Cited by 4
Natural Resistance to HIV Infection: Role of Immune Activation
Naranjo‐Covo, M. M., Rincón, D. S., Flórez‐Álvarez, L., Hernández, J. C., & Zapata, W. (2025) · Immunity Inflammation and Disease · doi:10.1002/iid3.70138 · Cited by 4
“This could be mediated by low activation, as IRF1 seems to be highly expressed in activated cells [86].”
Gene expression studies
Schramm, K. (2016) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.20703 · Cited by 4
Androgen Influence on Lymphocyte Gene Expression
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Interferon regulatory factor 8 induces intrinsic functional changes in mature neutrophils
Polmann, L., Grimm, J. C., Roth, J., & Barczyk‐Kahlert, K. (2025) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiaf078 · Cited by 2

Authors: Nelson, N., Kanno, Y., Hong, C., Contursi, C., Fujita, T., Fowlkes, B. J., O’Connell, E., Hu-Li, J., Paul, W. E., Jankovic, D., Sher, A. F., Coligan, J. E., Thornton, A., Appella, E., Yang, Y., & Ozato, K.
Affiliations: National Institutes of Health (US)
Laboratory of Molecular Growth Regulation, National Institute of Child Health and Human Development , Bethesda, MD 20892,
ORCID: Kanno, Y
Fujita, T
Jankovic, D
Sher, A F
Thornton, A
Appella, E
Yang, Y
Ozato, K
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 1996-05
Volume: 156
Issue: 10
Pages: 3711-3720
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.156.10.3711
OpenAlex: W1541863220
Cited by: 110
References: 0
Citations by year: 2026: 1 · 2025: 6 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 3 · 2017: 4 · 2016: 3 · 2015: 1 · 2014: 2 · 2013: 4 · 2012: 4
FWCI: 3.29
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: STAT1, T cell activation, interferon-gamma signaling, IRF1, IRF2, B cells, thymocytes, Th1/Th2 cells, transcriptional regulation, anti-CD3 stimulation, concanavalin A
MeSH terms: Interferon Regulatory Factor-8, Amino Acid Sequence, Animals, Antibodies, Monoclonal, B-Lymphocytes, Base Sequence, Carrier Proteins, Cell Differentiation, Cell Line, DNA-Binding Proteins, Hybridomas, Interferon-gamma, Interphase, Lipopolysaccharides, Lymphocyte Activation, Molecular Sequence Data, Phosphoproteins, Receptors, Antigen, T-Cell, Repressor Proteins, T-Lymphocytes, Trans-Activators, CD3 Complex, Th1 Cells, Th2 Cells, STAT1 Transcription Factor, Interferon Regulatory Factors, Interferon Regulatory Factor-1, Mice

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Expression of IFN regulatory factor family proteins in lymphocytes. Induction of Stat-1 and IFN consensus sequence binding protein expression by T cell activation

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