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Article ; Online: Aire in Autoimmunity.

Miller, Corey N / Waterfield, Michael R / Gardner, James M / Anderson, Mark S

2024

Abstract: The role of the autoimmune regulator (Aire) in central immune tolerance and thymic self-representation was first described more than 20 years ago, but fascinating new insights into its biology continue to emerge, particularly in the era of advanced ... ...

Abstract	The role of the autoimmune regulator (Aire) in central immune tolerance and thymic self-representation was first described more than 20 years ago, but fascinating new insights into its biology continue to emerge, particularly in the era of advanced single-cell genomics. We briefly describe the role of human genetics in the discovery of Aire, as well as insights into its function gained from genotype-phenotype correlations and the spectrum of Aire-associated autoimmunity-including insights from patients with Aire mutations with broad and diverse implications for human health. We then highlight emerging trends in Aire biology, focusing on three topic areas. First, we discuss medullary thymic epithelial diversity and the role of Aire in thymic epithelial development. Second, we highlight recent developments regarding the molecular mechanisms of Aire and its binding partners. Finally, we describe the rapidly evolving biology of the identity and function of extrathymic Aire-expressing cells (eTACs), and a novel eTAC subset called Janus cells, as well as their potential roles in immune homeostasis. Expected final online publication date for the
Language	English
Publishing date	2024-02-15
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	604953-9
ISSN	1545-3278 ; 0732-0582
ISSN (online)	1545-3278
ISSN	0732-0582
DOI	10.1146/annurev-immunol-090222-101050
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Article ; Online: Ikaros is a principal regulator of Aire

Sin, Jun Hyung / Sucharov, Juliana / Kashyap, Sujit / Wang, Yi / Proekt, Irina / Liu, Xian / Parent, Audrey V / Gupta, Alexander / Kastner, Philippe / Chan, Susan / Gardner, James M / Ntranos, Vasilis / Miller, Corey N / Anderson, Mark S / Schjerven, Hilde / Waterfield, Michael R

Science immunology

2023 Volume 8, Issue 88, Page(s) eabq3109

Abstract: Mutations in the gene encoding the zinc-finger transcription factor Ikaros ( ...

Abstract	Mutations in the gene encoding the zinc-finger transcription factor Ikaros (
MeSH term(s)	Humans ; Mice ; Animals ; Central Tolerance ; Cell Differentiation ; Thymus Gland ; Transcription Factors ; Gene Expression Regulation
Chemical Substances	Transcription Factors
Language	English
Publishing date	2023-10-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2470-9468
ISSN (online)	2470-9468
DOI	10.1126/sciimmunol.abq3109
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Article ; Online: Insights into immune tolerance from AIRE deficiency.

Proekt, Irina / Miller, Corey N / Lionakis, Michail S / Anderson, Mark S

Current opinion in immunology

2017 Volume 49, Page(s) 71–78

Abstract: AIRE is a well-established master regulator of central tolerance. It plays an essential role in driving expression of tissue-specific antigens in the thymus and shaping the development of positively selected T-cells. Humans and mice with compromised or ... ...

Abstract	AIRE is a well-established master regulator of central tolerance. It plays an essential role in driving expression of tissue-specific antigens in the thymus and shaping the development of positively selected T-cells. Humans and mice with compromised or absent AIRE function have markedly variable phenotypes that include a range of autoimmune manifestations. Recent evidence suggests that this variability stems from cooperation of autoimmune susceptibilities involving both central and peripheral tolerance checkpoints. Here we discuss the broadening understanding of the factors that influence Aire expression, modify AIRE function, and the impact and intersection of AIRE with peripheral immunity. This rapidly expanding body of knowledge will force a reexamination of the definition and clinical management of APS-1 patients as well as provide a foundation for the development of immunomodulatory strategies targeting central tolerance.
MeSH term(s)	Animals ; Autoantigens/genetics ; Autoantigens/metabolism ; Gene Expression Regulation ; Humans ; Immune Tolerance/immunology ; Mice ; Phenotype ; Polyendocrinopathies, Autoimmune/immunology ; Thymus Gland/immunology ; Transcription Factors/genetics ; Transcription Factors/metabolism ; AIRE Protein
Chemical Substances	Autoantigens ; Transcription Factors
Language	English
Publishing date	2017-10-21
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1035767-1
ISSN	1879-0372 ; 0952-7915
ISSN (online)	1879-0372
ISSN	0952-7915
DOI	10.1016/j.coi.2017.10.003
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Article ; Online: Combined transient ablation and single-cell RNA-sequencing reveals the development of medullary thymic epithelial cells.

Wells, Kristen L / Miller, Corey N / Gschwind, Andreas R / Wei, Wu / Phipps, Jonah D / Anderson, Mark S / Steinmetz, Lars M

eLife

2020 Volume 9

Abstract: Medullary thymic epithelial cells (mTECs) play a critical role in central immune tolerance by mediating negative selection of autoreactive T cells through the collective expression of the peripheral self-antigen compartment, including tissue-specific ... ...

Abstract	Medullary thymic epithelial cells (mTECs) play a critical role in central immune tolerance by mediating negative selection of autoreactive T cells through the collective expression of the peripheral self-antigen compartment, including tissue-specific antigens (TSAs). Recent work has shown that gene-expression patterns within the mTEC compartment are heterogenous and include multiple differentiated cell states. To further define mTEC development and medullary epithelial lineage relationships, we combined lineage tracing and recovery from transient in vivo mTEC ablation with single-cell RNA-sequencing in
MeSH term(s)	Animals ; Cell Differentiation/immunology ; Cell Lineage ; Epithelial Cells/cytology ; Mice ; Mice, Inbred C57BL ; Mice, Mutant Strains ; Sequence Analysis, RNA ; Single-Cell Analysis ; Thymus Gland/cytology
Language	English
Publishing date	2020-11-23
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.60188
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Article: SIV clearance from neonatal macaques following transient CCR5 depletion.

bioRxiv : the preprint server for biology

2023

Abstract: Treatment of people with HIV (PWH) with antiretroviral therapy (ART) results in sustained suppression of viremia, but HIV persists indefinitely as integrated provirus in CD4-expressing cells. Intact persistent provirus, the "rebound competent viral ... ...

Abstract	Treatment of people with HIV (PWH) with antiretroviral therapy (ART) results in sustained suppression of viremia, but HIV persists indefinitely as integrated provirus in CD4-expressing cells. Intact persistent provirus, the "rebound competent viral reservoir" (RCVR), is the primary obstacle to achieving a cure. Most variants of HIV enter CD4
Language	English
Publishing date	2023-05-01
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.01.533682
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Article ; Online: Single-cell transcriptional profiling of human thymic stroma uncovers novel cellular heterogeneity in the thymic medulla.

Bautista, Jhoanne L / Cramer, Nathan T / Miller, Corey N / Chavez, Jessica / Berrios, David I / Byrnes, Lauren E / Germino, Joe / Ntranos, Vasilis / Sneddon, Julie B / Burt, Trevor D / Gardner, James M / Ye, Chun J / Anderson, Mark S / Parent, Audrey V

Nature communications

2021 Volume 12, Issue 1, Page(s) 1096

Abstract: The thymus' key function in the immune system is to provide the necessary environment for the development of diverse and self-tolerant T lymphocytes. While recent evidence suggests that the thymic stroma is comprised of more functionally distinct ... ...

Abstract	The thymus' key function in the immune system is to provide the necessary environment for the development of diverse and self-tolerant T lymphocytes. While recent evidence suggests that the thymic stroma is comprised of more functionally distinct subpopulations than previously appreciated, the extent of this cellular heterogeneity in the human thymus is not well understood. Here we use single-cell RNA sequencing to comprehensively profile the human thymic stroma across multiple stages of life. Mesenchyme, pericytes and endothelial cells are identified as potential key regulators of thymic epithelial cell differentiation and thymocyte migration. In-depth analyses of epithelial cells reveal the presence of ionocytes as a medullary population, while the expression of tissue-specific antigens is mapped to different subsets of epithelial cells. This work thus provides important insight on how the diversity of thymic cells is established, and how this heterogeneity contributes to the induction of immune tolerance in humans.
MeSH term(s)	Adult ; Animals ; Cell Differentiation/genetics ; Cell Lineage/genetics ; Endothelial Cells/cytology ; Endothelial Cells/metabolism ; Epithelial Cells/metabolism ; Gene Expression Profiling/methods ; Genetic Heterogeneity ; Humans ; Mesoderm/cytology ; Mesoderm/metabolism ; Mice ; Pericytes/cytology ; Pericytes/metabolism ; Single-Cell Analysis/methods ; T-Lymphocytes/cytology ; T-Lymphocytes/metabolism ; Thymocytes/cytology ; Thymocytes/metabolism ; Thymus Gland/cytology ; Thymus Gland/embryology ; Thymus Gland/metabolism
Language	English
Publishing date	2021-02-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-21346-6
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Article ; Online: Revisiting the Road Map of Medullary Thymic Epithelial Cell Differentiation.

Michel, Chloé / Miller, Corey N / Küchler, Rita / Brors, Benedikt / Anderson, Mark S / Kyewski, Bruno / Pinto, Sheena

Journal of immunology (Baltimore, Md. : 1950)

2017 Volume 199, Issue 10, Page(s) 3488–3503

Abstract: The basic two-step terminal differentiation model of the medullary thymic epithelial cell (mTEC) lineage from immature MHC class II (MHCII) ...

Abstract	The basic two-step terminal differentiation model of the medullary thymic epithelial cell (mTEC) lineage from immature MHC class II (MHCII)
MeSH term(s)	Animals ; Apoptosis ; Biomarkers/metabolism ; Cell Differentiation ; Cell Lineage ; Cells, Cultured ; Epithelial Cells/physiology ; Female ; Gene Expression Regulation ; Histocompatibility Antigens Class II/genetics ; Histocompatibility Antigens Class II/metabolism ; Humans ; Lectins/metabolism ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Pregnancy ; Rats ; Rats, Sprague-Dawley ; Thymus Gland/anatomy & histology ; Thymus Gland/cytology ; Transcription Factors/genetics ; Transcription Factors/metabolism ; AIRE Protein
Chemical Substances	Biomarkers ; Histocompatibility Antigens Class II ; Lectins ; Transcription Factors ; fucose-binding lectin
Language	English
Publishing date	2017-10-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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.1700203
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Zs.MG 28: Show issues

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Article ; Online: Detection of Succinate by Intestinal Tuft Cells Triggers a Type 2 Innate Immune Circuit.

Nadjsombati, Marija S / McGinty, John W / Lyons-Cohen, Miranda R / Jaffe, James B / DiPeso, Lucian / Schneider, Christoph / Miller, Corey N / Pollack, Joshua L / Nagana Gowda, G A / Fontana, Mary F / Erle, David J / Anderson, Mark S / Locksley, Richard M / Raftery, Daniel / von Moltke, Jakob

Immunity

2018 Volume 49, Issue 1, Page(s) 33–41.e7

Abstract: In the small intestine, type 2 responses are regulated by a signaling circuit that involves tuft cells and group 2 innate lymphoid cells (ILC2s). Here, we identified the microbial metabolite succinate as an activating ligand for small intestinal (SI) ... ...

Abstract	In the small intestine, type 2 responses are regulated by a signaling circuit that involves tuft cells and group 2 innate lymphoid cells (ILC2s). Here, we identified the microbial metabolite succinate as an activating ligand for small intestinal (SI) tuft cells. Sequencing analyses of tuft cells isolated from the small intestine, gall bladder, colon, thymus, and trachea revealed that expression of tuft cell chemosensory receptors is tissue specific. SI tuft cells expressed the succinate receptor (SUCNR1), and providing succinate in drinking water was sufficient to induce a multifaceted type 2 immune response via the tuft-ILC2 circuit. The helminth Nippostrongylus brasiliensis and a tritrichomonad protist both secreted succinate as a metabolite. In vivo sensing of the tritrichomonad required SUCNR1, whereas N. brasiliensis was SUCNR1 independent. These findings define a paradigm wherein tuft cells monitor microbial metabolites to initiate type 2 immunity and suggest the existence of other sensing pathways triggering the response to helminths.
MeSH term(s)	Animals ; Cell Line ; Female ; Immunity, Mucosal/drug effects ; Intestinal Mucosa/cytology ; Intestinal Mucosa/immunology ; Intestinal Mucosa/metabolism ; Intestine, Small/drug effects ; Intestine, Small/immunology ; Male ; Mice, Inbred C57BL ; Mice, Knockout ; Nippostrongylus/drug effects ; Nippostrongylus/immunology ; Nippostrongylus/metabolism ; Organ Specificity ; Protozoan Infections/immunology ; Receptors, G-Protein-Coupled/immunology ; Receptors, G-Protein-Coupled/metabolism ; Signal Transduction/drug effects ; Signal Transduction/immunology ; Species Specificity ; Strongylida Infections/immunology ; Succinic Acid/pharmacology ; TRPM Cation Channels/metabolism ; Th2 Cells/immunology ; Tritrichomonas/drug effects ; Tritrichomonas/immunology ; Tritrichomonas/metabolism
Chemical Substances	GPR91 protein, mouse ; Receptors, G-Protein-Coupled ; TRPM Cation Channels ; Trpm5 protein, mouse ; Succinic Acid (AB6MNQ6J6L)
Language	English
Publishing date	2018-07-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1217235-2
ISSN	1097-4180 ; 1074-7613
ISSN (online)	1097-4180
ISSN	1074-7613
DOI	10.1016/j.immuni.2018.06.016
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Article ; Online: LYN- and AIRE-mediated tolerance checkpoint defects synergize to trigger organ-specific autoimmunity.

Proekt, Irina / Miller, Corey N / Jeanne, Marion / Fasano, Kayla J / Moon, James J / Lowell, Clifford A / Gould, Douglas B / Anderson, Mark S / DeFranco, Anthony L

The Journal of clinical investigation

2016 Volume 126, Issue 10, Page(s) 3758–3771

Abstract: Studies of the genetic factors associated with human autoimmune disease suggest a multigenic origin of susceptibility; however, how these factors interact and through which tolerance pathways they operate generally remain to be defined. One key ... ...

Abstract	Studies of the genetic factors associated with human autoimmune disease suggest a multigenic origin of susceptibility; however, how these factors interact and through which tolerance pathways they operate generally remain to be defined. One key checkpoint occurs through the activity of the autoimmune regulator AIRE, which promotes central T cell tolerance. Recent reports have described a variety of dominant-negative AIRE mutations that likely contribute to human autoimmunity to a greater extent than previously thought. In families with these mutations, the penetrance of autoimmunity is incomplete, suggesting that other checkpoints play a role in preventing autoimmunity. Here, we tested whether a defect in LYN, an inhibitory protein tyrosine kinase that is implicated in systemic autoimmunity, could combine with an Aire mutation to provoke organ-specific autoimmunity. Indeed, mice with a dominant-negative allele of Aire and deficiency in LYN spontaneously developed organ-specific autoimmunity in the eye. We further determined that a small pool of retinal protein-specific T cells escaped thymic deletion as a result of the hypomorphic Aire function and that these cells also escaped peripheral tolerance in the presence of LYN-deficient dendritic cells, leading to highly destructive autoimmune attack. These findings demonstrate how 2 distinct tolerance pathways can synergize to unleash autoimmunity and have implications for the genetic susceptibility of autoimmune disease.
MeSH term(s)	Animals ; Antigen Presentation ; Autoantibodies/metabolism ; Autoimmune Diseases/genetics ; Autoimmune Diseases/immunology ; Autoimmunity ; CD4-Positive T-Lymphocytes/immunology ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Eye Proteins/immunology ; Gastrointestinal Microbiome/immunology ; Mice, Inbred C57BL ; Mice, Transgenic ; Organ Specificity ; Retinol-Binding Proteins/immunology ; Transcription Factors/physiology ; Uveitis, Posterior/genetics ; Uveitis, Posterior/immunology ; src-Family Kinases/physiology ; AIRE Protein
Chemical Substances	Autoantibodies ; Eye Proteins ; Retinol-Binding Proteins ; Transcription Factors ; interstitial retinol-binding protein ; lyn protein-tyrosine kinase (EC 2.7.10.2) ; src-Family Kinases (EC 2.7.10.2)
Language	English
Publishing date	2016-08-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	3067-3
ISSN	1558-8238 ; 0021-9738
ISSN (online)	1558-8238
ISSN	0021-9738
DOI	10.1172/JCI84440
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Article ; Online: Thymic regulatory T cells arise via two distinct developmental programs.

Nature immunology

2019 Volume 20, Issue 2, Page(s) 195–205

Abstract: The developmental programs that generate a broad repertoire of regulatory T cells ( ... ...

Abstract	The developmental programs that generate a broad repertoire of regulatory T cells (T
MeSH term(s)	Animals ; Autoantigens/immunology ; Cell Differentiation/immunology ; Colitis/immunology ; Disease Models, Animal ; Encephalomyelitis, Autoimmune, Experimental/immunology ; Forkhead Transcription Factors/genetics ; Forkhead Transcription Factors/metabolism ; Freund's Adjuvant/administration & dosage ; Freund's Adjuvant/immunology ; Humans ; Immune Tolerance/immunology ; Interleukin-2 Receptor alpha Subunit/metabolism ; Lymphoid Progenitor Cells/physiology ; Lymphoid Progenitor Cells/transplantation ; Mice ; Mice, Transgenic ; Mycobacterium tuberculosis/immunology ; Myelin-Oligodendrocyte Glycoprotein/administration & dosage ; Myelin-Oligodendrocyte Glycoprotein/immunology ; Peptide Fragments/administration & dosage ; Peptide Fragments/immunology ; Signal Transduction ; Specific Pathogen-Free Organisms ; T-Lymphocytes, Regulatory/physiology ; Thymus Gland/cytology ; Thymus Gland/growth & development ; Thymus Gland/immunology
Chemical Substances	Autoantigens ; Forkhead Transcription Factors ; Foxp3 protein, mouse ; Il2ra protein, mouse ; Interleukin-2 Receptor alpha Subunit ; Myelin-Oligodendrocyte Glycoprotein ; Peptide Fragments ; myelin oligodendrocyte glycoprotein (35-55) ; Freund's Adjuvant (9007-81-2)
Language	English
Publishing date	2019-01-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-018-0289-6
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