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Article ; Online: Regulation of Early Lymphocyte Development

Akiyama, Taishin / Yamamoto, Tadashi

2021 Volume 12, Page(s) 715675

Abstract: Development of lymphocytes is precisely regulated by various mechanisms. In addition to transcriptional rates, post-transcriptional regulation of mRNA abundance contributes to differentiation of lymphocytes. mRNA decay is a post-transcriptional mechanism ...

Abstract	Development of lymphocytes is precisely regulated by various mechanisms. In addition to transcriptional rates, post-transcriptional regulation of mRNA abundance contributes to differentiation of lymphocytes. mRNA decay is a post-transcriptional mechanism controlling mRNA abundance. The carbon catabolite repression 4 (CCR4)-negative on TATA-less (NOT) complex controls mRNA longevity by catalyzing mRNA deadenylation, which is the rate-limiting step in the mRNA decay pathway. mRNA decay, regulated by the CCR4-NOT complex, is required for differentiation of pro-B to pre-B cells and V(D)J recombination in pro-B cells. In this process, it is likely that the RNA-binding proteins, ZFP36 ring finger protein like 1 and 2, recruit the CCR4-NOT complex to specific target mRNAs, thereby inducing cell quiescence of pro-B cells. A recent study showed that the CCR4-NOT complex participates in positive selection of thymocytes. Mechanistically, the CCR4-NOT deadenylase complex inhibits abnormal apoptosis by reducing the expression level of mRNAs encoding pro-apoptotic proteins, which are otherwise up-regulated during positive selection. We discuss mechanisms regulating CCR4-NOT complex-dependent mRNA decay in lymphocyte development and selection.
MeSH term(s)	Animals ; Cell Differentiation/genetics ; Gene Expression Regulation, Developmental ; Humans ; Lymphocytes/cytology ; Lymphocytes/metabolism ; Lymphopoiesis/genetics ; Nuclear Receptor Subfamily 4, Group A, Member 2/metabolism ; RNA Processing, Post-Transcriptional ; RNA Stability ; RNA, Messenger/genetics ; Receptors, CCR4/metabolism ; Transcription Factors/metabolism
Chemical Substances	NR4A2 protein, human ; Nuclear Receptor Subfamily 4, Group A, Member 2 ; RNA, Messenger ; Receptors, CCR4 ; Transcription Factors
Language	English
Publishing date	2021-07-19
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2021.715675
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Article ; Online: Sample Preparation and Integrative Data Analysis of a Droplet-based Single-Cell ATAC-sequencing Using Murine Thymic Epithelial Cells.

Ishikawa, Tatsuya / Ishii, Hiroto / Miyao, Takahisa / Horie, Kenta / Miyauchi, Maki / Akiyama, Nobuko / Akiyama, Taishin

Bio-protocol

2023 Volume 13, Issue 1, Page(s) e4588

Abstract: Accessible chromatin regions modulate gene expression by acting as cis-regulatory elements. Understanding the epigenetic landscape by mapping accessible regions of DNA is therefore imperative to decipher mechanisms of gene regulation under specific ... ...

Abstract	Accessible chromatin regions modulate gene expression by acting as cis-regulatory elements. Understanding the epigenetic landscape by mapping accessible regions of DNA is therefore imperative to decipher mechanisms of gene regulation under specific biological contexts of interest. The assay for transposase-accessible chromatin sequencing (ATAC-seq) has been widely used to detect accessible chromatin and the recent introduction of single-cell technology has increased resolution to the single-cell level. In a recent study, we used droplet-based, single-cell ATAC-seq technology (scATAC-seq) to reveal the epigenetic profile of the transit-amplifying subset of thymic epithelial cells (TECs), which was identified previously using single-cell RNA-sequencing technology (scRNA-seq). This protocol allows the preparation of nuclei from TECs in order to perform droplet-based scATAC-seq and its integrative analysis with scRNA-seq data obtained from the same cell population. Integrative analysis has the advantage of identifying cell types in scATAC-seq data based on cell cluster annotations in scRNA-seq analysis.
Language	English
Publishing date	2023-01-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	2833269-6
ISSN	2331-8325 ; 2331-8325
ISSN (online)	2331-8325
ISSN	2331-8325
DOI	10.21769/BioProtoc.4588
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Article ; Online: In Pursuit of Adult Progenitors of Thymic Epithelial Cells.

Ishikawa, Tatsuya / Akiyama, Nobuko / Akiyama, Taishin

Frontiers in immunology

2021 Volume 12, Page(s) 621824

Abstract: Peripheral T cells capable of discriminating between self and non-self antigens are major components of a robust adaptive immune system. The development of self-tolerant T cells is orchestrated by thymic epithelial cells (TECs), which are localized in ... ...

Abstract	Peripheral T cells capable of discriminating between self and non-self antigens are major components of a robust adaptive immune system. The development of self-tolerant T cells is orchestrated by thymic epithelial cells (TECs), which are localized in the thymic cortex (cortical TECs, cTECs) and medulla (medullary TECs, mTECs). cTECs and mTECs are essential for differentiation, proliferation, and positive and negative selection of thymocytes. Recent advances in single-cell RNA-sequencing technology have revealed a previously unknown degree of TEC heterogeneity, but we still lack a clear picture of the identity of TEC progenitors in the adult thymus. In this review, we describe both earlier and recent findings that shed light on features of these elusive adult progenitors in the context of tissue homeostasis, as well as recovery from stress-induced thymic atrophy.
MeSH term(s)	Adult Stem Cells/physiology ; Animals ; Autoantigens/immunology ; Cell Differentiation ; Clonal Selection, Antigen-Mediated ; Epithelial Cells/physiology ; Humans ; Immune Tolerance ; Immunity, Cellular ; Immunologic Deficiency Syndromes/immunology ; T-Lymphocytes/immunology ; Thymus Gland/cytology
Chemical Substances	Autoantigens
Language	English
Publishing date	2021-02-25
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2021.621824
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Article ; Online: Machine Learning Approaches to TCR Repertoire Analysis.

Katayama, Yotaro / Yokota, Ryo / Akiyama, Taishin / Kobayashi, Tetsuya J

Frontiers in immunology

2022 Volume 13, Page(s) 858057

Abstract: Sparked by the development of genome sequencing technology, the quantity and quality of data handled in immunological research have been changing dramatically. Various data and database platforms are now driving the rapid progress of machine learning for ...

Abstract	Sparked by the development of genome sequencing technology, the quantity and quality of data handled in immunological research have been changing dramatically. Various data and database platforms are now driving the rapid progress of machine learning for immunological data analysis. Of various topics in immunology, T cell receptor repertoire analysis is one of the most important targets of machine learning for assessing the state and abnormalities of immune systems. In this paper, we review recent repertoire analysis methods based on machine learning and deep learning and discuss their prospects.
MeSH term(s)	Immune System ; Machine Learning ; Receptors, Antigen, T-Cell/genetics
Chemical Substances	Receptors, Antigen, T-Cell
Language	English
Publishing date	2022-07-15
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.858057
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Article ; Online: RNA decay machinery safeguards immune cell development and immunological responses.

Akiyama, Taishin / Suzuki, Toru / Yamamoto, Tadashi

Trends in immunology

2021 Volume 42, Issue 5, Page(s) 447–460

Abstract: mRNA decay systems control mRNA abundance by counterbalancing transcription. Several recent studies show that mRNA decay pathways are crucial to conventional T and B cell development in vertebrates, in addition to suppressing autoimmunity and excessive ... ...

Abstract	mRNA decay systems control mRNA abundance by counterbalancing transcription. Several recent studies show that mRNA decay pathways are crucial to conventional T and B cell development in vertebrates, in addition to suppressing autoimmunity and excessive inflammatory responses. Selective mRNA degradation triggered by the CCR4-NOT deadenylase complex appears to be required in lymphocyte development, cell quiescence, V(D)J (variable-diversity-joining) recombination, and prevention of inappropriate apoptosis in mice. Moreover, a recent study suggests that mRNA decay may be involved in preventing human hyperinflammatory disease. These findings imply that mRNA decay pathways in humans and mice do not simply maintain mRNA homeostatic turnover but can also precisely regulate immune development and immunological responses by selectively targeting mRNAs.
MeSH term(s)	Animals ; Mice ; RNA Stability ; RNA, Messenger
Chemical Substances	RNA, Messenger
Language	English
Publishing date	2021-04-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2036831-8
ISSN	1471-4981 ; 1471-4906
ISSN (online)	1471-4981
ISSN	1471-4906
DOI	10.1016/j.it.2021.03.008
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Article ; Online: TNF receptor-associated factor 6 (TRAF6) plays crucial roles in multiple biological systems through polyubiquitination-mediated NF-κB activation.

Yamamoto, Mizuki / Gohda, Jin / Akiyama, Taishin / Inoue, Jun-Ichiro

Proceedings of the Japan Academy. Series B, Physical and biological sciences

2021 Volume 97, Issue 4, Page(s) 145–160

Abstract: NF-κB was first identified in 1986 as a B cell-specific transcription factor inducing immunoglobulin κ light chain expression. Subsequent studies revealed that NF-κB plays important roles in development, organogenesis, immunity, inflammation, and ... ...

Abstract	NF-κB was first identified in 1986 as a B cell-specific transcription factor inducing immunoglobulin κ light chain expression. Subsequent studies revealed that NF-κB plays important roles in development, organogenesis, immunity, inflammation, and neurological functions by spatiotemporally regulating cell proliferation, differentiation, and apoptosis in several cell types. Furthermore, studies on the signal pathways that activate NF-κB led to the discovery of TRAF family proteins with E3 ubiquitin ligase activity, which function downstream of the receptor. This discovery led to the proposal of an entirely new signaling mechanism concept, wherein K63-ubiquitin chains act as a scaffold for the signaling complex to activate downstream kinases. This concept has revolutionized ubiquitin studies by revealing the importance of the nonproteolytic functions of ubiquitin not only in NF-κB signaling but also in a variety of other biological systems. TRAF6 is the most diverged among the TRAF family proteins, and our studies uncovered its notable physiological and pathological functions.
MeSH term(s)	Animals ; Humans ; NF-kappa B/metabolism ; Signal Transduction ; TNF Receptor-Associated Factor 6/metabolism ; Ubiquitination
Chemical Substances	NF-kappa B ; TNF Receptor-Associated Factor 6
Language	English
Publishing date	2021-03-26
Publishing country	Japan
Document type	Journal Article ; Review
ZDB-ID	161781-3
ISSN	1349-2896 ; 0386-2208
ISSN (online)	1349-2896
ISSN	0386-2208
DOI	10.2183/pjab.97.009
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Article ; Online: T-cell receptor repertoire analysis of CD4-positive T cells from blood and an affected organ in an autoimmune mouse model.

Ishikawa, Tatsuya / Horie, Kenta / Takakura, Yuki / Ohki, Houko / Maruyama, Yuya / Hayama, Mio / Miyauchi, Maki / Miyao, Takahisa / Hagiwara, Naho / Kobayashi, Tetsuya J / Akiyama, Nobuko / Akiyama, Taishin

Genes to cells : devoted to molecular & cellular mechanisms

2023 Volume 28, Issue 12, Page(s) 929–941

Abstract: One hallmark of some autoimmune diseases is the variability of symptoms among individuals. Organs affected by the disease differ between patients, posing a challenge in diagnosing the affected organs. Although numerous studies have investigated the ... ...

Abstract	One hallmark of some autoimmune diseases is the variability of symptoms among individuals. Organs affected by the disease differ between patients, posing a challenge in diagnosing the affected organs. Although numerous studies have investigated the correlation between T cell antigen receptor (TCR) repertoires and the development of infectious and immune diseases, the correlation between TCR repertoires and variations in disease symptoms among individuals remains unclear. This study aimed to investigate the correlation of TCRα and β repertoires in blood T cells with the extent of autoimmune signs that varies among individuals. We sequenced TCRα and β of CD4
MeSH term(s)	Humans ; Mice ; Animals ; CD4-Positive T-Lymphocytes ; Autoimmune Diseases ; Receptors, Antigen, T-Cell/genetics ; Polyendocrinopathies, Autoimmune
Chemical Substances	Receptors, Antigen, T-Cell
Language	English
Publishing date	2023-11-01
Publishing country	England
Document type	Journal Article
ZDB-ID	1330000-3
ISSN	1365-2443 ; 1356-9597
ISSN (online)	1365-2443
ISSN	1356-9597
DOI	10.1111/gtc.13079
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Article ; Online: Acute irradiation causes a long-term disturbance in the heterogeneity and gene expression profile of medullary thymic epithelial cells.

Horie, Kenta / Namiki, Kano / Kinoshita, Kyouhei / Miyauchi, Maki / Ishikawa, Tatsuya / Hayama, Mio / Maruyama, Yuya / Hagiwara, Naho / Miyao, Takahisa / Murata, Shigeo / Kobayashi, Tetsuya J / Akiyama, Nobuko / Akiyama, Taishin

Frontiers in immunology

2023 Volume 14, Page(s) 1186154

Abstract: The thymus has the ability to regenerate from acute injury caused by radiation, infection, and stressors. In addition to thymocytes, thymic epithelial cells in the medulla (mTECs), which are crucial for T cell self-tolerance by ectopically expressing and ...

Abstract	The thymus has the ability to regenerate from acute injury caused by radiation, infection, and stressors. In addition to thymocytes, thymic epithelial cells in the medulla (mTECs), which are crucial for T cell self-tolerance by ectopically expressing and presenting thousands of tissue-specific antigens (TSAs), are damaged by these insults and recover thereafter. However, given recent discoveries on the high heterogeneity of mTECs, it remains to be determined whether the frequency and properties of mTEC subsets are restored during thymic recovery from radiation damage. Here we demonstrate that acute total body irradiation with a sublethal dose induces aftereffects on heterogeneity and gene expression of mTECs. Single-cell RNA-sequencing (scRNA-seq) analysis showed that irradiation reduces the frequency of mTECs expressing AIRE, which is a critical regulator of TSA expression, 15 days after irradiation. In contrast, transit-amplifying mTECs (TA-mTECs), which are progenitors of AIRE-expressing mTECs, and Ccl21a-expressing mTECs, were less affected. Interestingly, a detailed analysis of scRNA-seq data suggested that the proportion of a unique mTEC cluster expressing Ccl25 and a high level of TSAs was severely decreased by irradiation. In sum, we propose that the effects of acute irradiation disrupt the heterogeneity and properties of mTECs over an extended period, which potentially leads to an impairment of thymic T cell selection.
MeSH term(s)	Mice ; Animals ; Transcriptome ; Transcription Factors/metabolism ; Cell Differentiation ; Mice, Inbred C57BL ; Epithelial Cells/metabolism
Chemical Substances	Transcription Factors
Language	English
Publishing date	2023-11-02
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1186154
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Article ; Online: Mitochondrial protein C15ORF48 is a stress-independent inducer of autophagy that regulates oxidative stress and autoimmunity.

Nature communications

2024 Volume 15, Issue 1, Page(s) 953

Abstract: Autophagy is primarily activated by cellular stress, such as starvation or mitochondrial damage. However, stress-independent autophagy is activated by unclear mechanisms in several cell types, such as thymic epithelial cells (TECs). Here we report that ... ...

Abstract	Autophagy is primarily activated by cellular stress, such as starvation or mitochondrial damage. However, stress-independent autophagy is activated by unclear mechanisms in several cell types, such as thymic epithelial cells (TECs). Here we report that the mitochondrial protein, C15ORF48, is a critical inducer of stress-independent autophagy. Mechanistically, C15ORF48 reduces the mitochondrial membrane potential and lowers intracellular ATP levels, thereby activating AMP-activated protein kinase and its downstream Unc-51-like kinase 1. Interestingly, C15ORF48-dependent induction of autophagy upregulates intracellular glutathione levels, promoting cell survival by reducing oxidative stress. Mice deficient in C15orf48 show a reduction in stress-independent autophagy in TECs, but not in typical starvation-induced autophagy in skeletal muscles. Moreover, C15orf48
MeSH term(s)	Mice ; Animals ; Mitochondrial Proteins/metabolism ; Autoimmunity ; Oxidative Stress ; Autophagy ; Epithelial Cells/metabolism ; AMP-Activated Protein Kinases/genetics ; AMP-Activated Protein Kinases/metabolism
Chemical Substances	Mitochondrial Proteins ; AMP-Activated Protein Kinases (EC 2.7.11.31)
Language	English
Publishing date	2024-02-01
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-45206-1
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Article ; Online: Aire Controls Heterogeneity of Medullary Thymic Epithelial Cells for the Expression of Self-Antigens.

Nishijima, Hitoshi / Matsumoto, Minoru / Morimoto, Junko / Hosomichi, Kazuyoshi / Akiyama, Nobuko / Akiyama, Taishin / Oya, Takeshi / Tsuneyama, Koichi / Yoshida, Hideyuki / Matsumoto, Mitsuru

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 208, Issue 2, Page(s) 303–320

Abstract: The deficiency of Aire, a transcriptional regulator whose defect results in the development of autoimmunity, is associated with reduced expression of tissue-restricted self-Ags (TRAs) in medullary thymic epithelial cells (mTECs). Although the mechanisms ... ...

Abstract	The deficiency of Aire, a transcriptional regulator whose defect results in the development of autoimmunity, is associated with reduced expression of tissue-restricted self-Ags (TRAs) in medullary thymic epithelial cells (mTECs). Although the mechanisms underlying Aire-dependent expression of TRAs need to be explored, the physical identification of the target(s) of Aire has been hampered by the low and promiscuous expression of TRAs. We have tackled this issue by engineering mice with augmented Aire expression. Integration of the transcriptomic data from Aire-augmented and Aire-deficient mTECs revealed that a large proportion of so-called Aire-dependent genes, including those of TRAs, may not be direct transcriptional targets downstream of Aire. Rather, Aire induces TRA expression indirectly through controlling the heterogeneity of mTECs, as revealed by single-cell analyses. In contrast, Ccl25 emerged as a canonical target of Aire, and we verified this both in vitro and in vivo. Our approach has illuminated the Aire's primary targets while distinguishing them from the secondary targets.
MeSH term(s)	Animals ; Autoantigens/immunology ; Autoimmunity/genetics ; Autoimmunity/immunology ; Chemokines, CC/genetics ; Chemokines, CC/metabolism ; Epithelial Cells/immunology ; Gene Expression Regulation ; Gene Knock-In Techniques ; Gene Knockout Techniques ; Mice ; Mice, Inbred C57BL ; Mice, Inbred NOD ; Mice, Transgenic ; Thymus Gland/cytology ; Thymus Gland/immunology ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcription, Genetic/genetics ; AIRE Protein
Chemical Substances	Autoantigens ; Ccl25 protein, mouse ; Chemokines, CC ; Transcription Factors
Language	English
Publishing date	2021-12-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2100692
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