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Article ; Online: Monogenic TCRβ Assembly and Expression Are Paramount for Uniform Antigen Receptor Specificity of Individual αβ T Lymphocytes.

Culberson, Erica J / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2022 Volume 209, Issue 1, Page(s) 93–98

Abstract: The ability of individual T and B cells to display Ag receptors of unique uniform specificity is the molecular basis of adaptive immunity. Most αβ T cells achieve uniform specificity by assembling in-frame genes on only one allelic copy of TCRβ and TCRα ... ...

Abstract	The ability of individual T and B cells to display Ag receptors of unique uniform specificity is the molecular basis of adaptive immunity. Most αβ T cells achieve uniform specificity by assembling in-frame genes on only one allelic copy of TCRβ and TCRα loci, while others prevent incorporation of TCRα protein from both alleles into TCRs. Analysis of mice expressing TCR proteins from a restricted combination of transgenes showed that TCR protein pairing restrictions achieve uniform specificity of cells expressing two types of TCRβ protein. However, whether this mechanism operates in the physiological context where each dual-TCRβ cell expresses one set of a vast number of different TCRβ proteins remains an open question, largely because there is a low, but significant, portion of cells carrying two in-frame TCRβ genes. To resolve this issue, we inactivated one allelic copy of the TCRα locus in a new mouse strain that assembles two in-frame TCRβ genes in an elevated fraction of cells. This genetic manipulation has no effect on the frequency of cells that display multiple types of αβ TCR, yet increases the representation of cells displaying TCRβ proteins that generate more highly expressed TCRs. Our data demonstrate that some TCRβ proteins exhibit differential functional pairing with TCRα proteins, but these restrictions have negligible contribution for ensuring uniform specificity of cells that express two types of TCRβ protein. Therefore, we conclude that mechanisms governing monogenic assembly and expression of TCRβ genes in individual cells are paramount for uniform specificity of αβ T lymphocytes.
MeSH term(s)	Alleles ; Animals ; Mice ; Receptors, Antigen/genetics ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; T-Lymphocytes ; Transgenes
Chemical Substances	Receptors, Antigen ; Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2022-06-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
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.2200176
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Article ; Online: Nemo-Dependent, ATM-Mediated Signals from RAG DNA Breaks at

Glynn, Rebecca A / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 208, Issue 2, Page(s) 371–383

Abstract: Monoallelic AgR gene expression underlies specific adaptive immune responses. AgR allelic exclusion is achieved by sequential initiation of V(D)J recombination between alleles and resultant protein from one allele signaling to prevent recombination of ... ...

Abstract	Monoallelic AgR gene expression underlies specific adaptive immune responses. AgR allelic exclusion is achieved by sequential initiation of V(D)J recombination between alleles and resultant protein from one allele signaling to prevent recombination of the other. The ATM kinase, a regulator of the DNA double-strand break (DSB) response, helps enforce allelic exclusion through undetermined mechanisms. ATM promotes repair of RAG1/RAG2 (RAG) endonuclease-induced DSBs and transduces signals from RAG DSBs during
MeSH term(s)	Animals ; Ataxia Telangiectasia Mutated Proteins/genetics ; Ataxia Telangiectasia Mutated Proteins/metabolism ; Cells, Cultured ; Clonal Anergy/genetics ; Clonal Anergy/immunology ; DNA Breaks, Double-Stranded ; DNA Repair/genetics ; DNA-Binding Proteins/genetics ; DNA-Binding Proteins/metabolism ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Immunoglobulin Variable Region/genetics ; Immunoglobulin Variable Region/immunology ; Immunoglobulins/genetics ; Immunoglobulins/immunology ; Intracellular Signaling Peptides and Proteins/genetics ; Intracellular Signaling Peptides and Proteins/metabolism ; Loss of Heterozygosity/genetics ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; V(D)J Recombination/genetics
Chemical Substances	DNA-Binding Proteins ; Homeodomain Proteins ; IgK ; Immunoglobulin Variable Region ; Immunoglobulins ; Intracellular Signaling Peptides and Proteins ; NEMO protein, mouse ; Rag2 protein, mouse ; RAG-1 protein (128559-51-3) ; Ataxia Telangiectasia Mutated Proteins (EC 2.7.11.1) ; Atm protein, mouse (EC 2.7.11.1)
Language	English
Publishing date	2021-12-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
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.2100696
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Article ; Online: Inefficient V(D)J recombination underlies monogenic T cell receptor β expression.

Wu, Glendon S / Bassing, Craig H

Proceedings of the National Academy of Sciences of the United States of America

2020 Volume 117, Issue 31, Page(s) 18172–18174

Abstract: The assembly of T cell receptor (TCR) and immunoglobulin (Ig) genes by V(D)J recombination generates the antigen receptor (AgR) diversity that is vital for adaptive immunity. At most AgR loci, V(D)J recombination is regulated so that only one allele ... ...

Abstract	The assembly of T cell receptor (TCR) and immunoglobulin (Ig) genes by V(D)J recombination generates the antigen receptor (AgR) diversity that is vital for adaptive immunity. At most AgR loci, V(D)J recombination is regulated so that only one allele assembles a functional gene, ensuring that nearly every T and B cell expresses a single type, or specificity, of AgR. The genomic organizations of some AgR loci permit the assembly and expression of two distinct genes on each allele; however, this is prevented by undetermined mechanisms. We show that the poor qualities of recombination signal sequences (RSSs) flanking Vβ gene segments suppress the assembly and expression of two distinct TCRβ genes from a single allele. Our data demonstrate that an intrinsic genetic mechanism that stochastically limits Vβ recombination efficiency governs monogenic TCRβ expression, thereby restraining the expression of multiple AgRs on αβ T cells.
MeSH term(s)	Animals ; Female ; Gene Expression Regulation/physiology ; Genes, T-Cell Receptor beta/physiology ; Heterozygote ; Male ; Mice ; T-Lymphocytes ; V(D)J Recombination
Language	English
Publishing date	2020-07-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2010077117
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Article ; Online: Methods for Study of Mouse T Cell Receptor α and β Gene Rearrangements.

Dauphars, Danielle J / Wu, Glendon / Bassing, Craig H / Krangel, Michael S

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2580, Page(s) 261–282

Abstract: Quantitative real-time PCR and next-generation sequencing (NGS) are invaluable techniques to analyze T cell receptor (Tcr) gene rearrangements in mouse lymphocyte populations. Although these approaches are powerful, they also have limitations that must ... ...

Abstract	Quantitative real-time PCR and next-generation sequencing (NGS) are invaluable techniques to analyze T cell receptor (Tcr) gene rearrangements in mouse lymphocyte populations. Although these approaches are powerful, they also have limitations that must be accounted for in experimental design and data interpretation. Here, we provide relevant background required for understanding these limitations and then outline established quantitative real-time PCR and NGS methods that can be used for analysis of mouse Tcra and Tcrb gene rearrangements in mice.
MeSH term(s)	Mice ; Animals ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; Gene Rearrangement ; Polymerase Chain Reaction
Chemical Substances	Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2022-11-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2740-2_16
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Article ; Online: Locus folding mechanisms determine modes of antigen receptor gene assembly.

Allyn, Brittney M / Hayer, Katharina E / Oyeniran, Clement / Nganga, Vincent / Lee, Kyutae / Mishra, Bikash / Sacan, Ahmet / Oltz, Eugene M / Bassing, Craig H

The Journal of experimental medicine

2024 Volume 221, Issue 2

Abstract: The dynamic folding of genomes regulates numerous biological processes, including antigen receptor (AgR) gene assembly. We show that, unlike other AgR loci, homotypic chromatin interactions and bidirectional chromosome looping both contribute to ... ...

Abstract	The dynamic folding of genomes regulates numerous biological processes, including antigen receptor (AgR) gene assembly. We show that, unlike other AgR loci, homotypic chromatin interactions and bidirectional chromosome looping both contribute to structuring Tcrb for efficient long-range V(D)J recombination. Inactivation of the CTCF binding element (CBE) or promoter at the most 5'Vβ segment (Trbv1) impaired loop extrusion originating locally and extending to DβJβ CBEs at the opposite end of Tcrb. Promoter or CBE mutation nearly eliminated Trbv1 contacts and decreased RAG endonuclease-mediated Trbv1 recombination. Importantly, Trbv1 rearrangement can proceed independent of substrate orientation, ruling out scanning by DβJβ-bound RAG as the sole mechanism of Vβ recombination, distinguishing it from Igh. Our data indicate that CBE-dependent generation of loops cooperates with promoter-mediated activation of chromatin to juxtapose Vβ and DβJβ segments for recombination through diffusion-based synapsis. Thus, the mechanisms that fold a genomic region can influence molecular processes occurring in that space, which may include recombination, repair, and transcriptional programming.
MeSH term(s)	Receptors, Antigen ; Chromatin/genetics ; Endonucleases ; Mutation ; Promoter Regions, Genetic/genetics ; Receptors, Antigen, T-Cell, alpha-beta/genetics
Chemical Substances	Receptors, Antigen ; Chromatin ; Endonucleases (EC 3.1.-) ; Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2024-01-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20230985
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Article ; Online: The Cyclin D3 Protein Enforces Monogenic TCRβ Expression by Mediating TCRβ Protein-Signaled Feedback Inhibition of Vβ Recombination.

Culberson, Erica J / Shields, Kymberle C / Glynn, Rebecca A / Allyn, Brittney M / Hayer, Katharina E / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2024 Volume 212, Issue 4, Page(s) 534–540

Abstract: In jawed vertebrates, adaptive immunity depends on the process of V(D)J recombination creating vast numbers of T and B lymphocytes that each expresses unique Ag receptors of uniform specificity. The asynchronous initiation of V-to-(D)J rearrangement ... ...

Abstract	In jawed vertebrates, adaptive immunity depends on the process of V(D)J recombination creating vast numbers of T and B lymphocytes that each expresses unique Ag receptors of uniform specificity. The asynchronous initiation of V-to-(D)J rearrangement between alleles and the resulting protein from one allele signaling feedback inhibition of V recombination on the other allele ensures homogeneous receptor specificity of individual cells. Upon productive Vβ-to-DβJβ rearrangements in noncycling double-negative thymocytes, TCRβ protein signals induction of the cyclin D3 protein to accelerate cell cycle entry, thereby driving proliferative expansion of developing αβ T cells. Through undetermined mechanisms, the inactivation of cyclin D3 in mice causes an increased frequency of αβ T cells that express TCRβ proteins from both alleles, producing lymphocytes of heterogeneous specificities. To determine how cyclin D3 enforces monogenic TCRβ expression, we used our mouse lines with enhanced rearrangement of specific Vβ segments due to replacement of their poor-quality recombination signal sequence (RSS) DNA elements with a better RSS. We show that cyclin D3 inactivation in these mice elevates the frequencies of αβ T cells that display proteins from RSS-augmented Vβ segments on both alleles. By assaying mature αβ T cells, we find that cyclin D3 deficiency increases the levels of Vβ rearrangements that occur within developing thymocytes. Our data demonstrate that a component of the cell cycle machinery mediates TCRβ protein-signaled feedback inhibition in thymocytes to achieve monogenic TCRβ expression and resulting uniform specificity of individual αβ T cells.
MeSH term(s)	Animals ; Mice ; Alleles ; Cyclin D3/genetics ; Feedback ; Gene Rearrangement, beta-Chain T-Cell Antigen Receptor ; Lymphocytes ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; Thymocytes
Chemical Substances	Cyclin D3 ; Receptors, Antigen, T-Cell, alpha-beta ; Ccnd3 protein, mouse
Language	English
Publishing date	2024-01-18
Publishing country	United States
Document type	Journal Article
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.2300623
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Article ; Online: Poor-Quality Vβ Recombination Signal Sequences and the DNA Damage Response ATM Kinase Collaborate to Establish TCRβ Gene Repertoire and Allelic Exclusion.

Wu, Glendon S / Culberson, Erica J / Allyn, Brittney M / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2022 Volume 208, Issue 11, Page(s) 2583–2592

Abstract: The monoallelic expression (allelic exclusion) of diverse lymphocyte Ag receptor genes enables specific immune responses. Allelic exclusion is achieved by asynchronous initiation of V(D)J recombination between alleles and protein encoded by successful ... ...

Abstract	The monoallelic expression (allelic exclusion) of diverse lymphocyte Ag receptor genes enables specific immune responses. Allelic exclusion is achieved by asynchronous initiation of V(D)J recombination between alleles and protein encoded by successful rearrangement on the first allele signaling permanent inhibition of V rearrangement on the other allele. The ATM kinase that guides DNA repair and transiently suppresses V(D)J recombination also helps impose allelic exclusion through undetermined mechanisms. At the TCRβ locus, one Vβ gene segment (
MeSH term(s)	Alleles ; Animals ; DNA Damage ; DNA Repair/genetics ; Gene Rearrangement, beta-Chain T-Cell Antigen Receptor/genetics ; Mice ; Protein Sorting Signals/genetics ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; V(D)J Recombination/genetics
Chemical Substances	Protein Sorting Signals ; Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2022-05-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
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.2100489
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Article ; Online: From RAG2 to T Cell Riches and Future Fortunes.

Glynn, Rebecca A / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2019 Volume 202, Issue 5, Page(s) 1315–1316

MeSH term(s)	Animals ; DNA-Binding Proteins/deficiency ; DNA-Binding Proteins/genetics ; DNA-Binding Proteins/immunology ; Humans ; Mice ; Mice, Knockout ; Nuclear Proteins/genetics ; Nuclear Proteins/immunology ; Receptors, Antigen, T-Cell/genetics ; Receptors, Antigen, T-Cell/immunology ; T-Lymphocytes/immunology
Chemical Substances	DNA-Binding Proteins ; Nuclear Proteins ; RAG2 protein, human ; Rag2 protein, mouse ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2019-02-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
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.1900010
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Article ; Online: Two Successive Inversional Vβ Rearrangements on a Single

Lee, Kyutae D / Bassing, Craig H

Journal of immunology (Baltimore, Md. : 1950)

2019 Volume 204, Issue 1, Page(s) 78–86

Abstract: Mammalian TCRβ loci contain 30 Vβ gene segments upstream and in the same transcriptional orientation as two DJCβ clusters, and a downstream Vβ (TRBV31) in the opposite orientation. The textbook view is upstream Vβs rearrange only by deletion and TRBV31 ... ...

Abstract	Mammalian TCRβ loci contain 30 Vβ gene segments upstream and in the same transcriptional orientation as two DJCβ clusters, and a downstream Vβ (TRBV31) in the opposite orientation. The textbook view is upstream Vβs rearrange only by deletion and TRBV31 rearranges only by inversion to create VβDJCβ genes. In this study, we show in mice that upstream Vβs recombine through inversion to the DJCβ2 cluster on alleles carrying a preassembled
MeSH term(s)	Alleles ; Animals ; Genes, T-Cell Receptor beta/genetics ; Genes, T-Cell Receptor beta/immunology ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; T-Lymphocytes/immunology
Language	English
Publishing date	2019-11-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
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.1901105
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Article ; Online: Flip the switch: BTG2-PRMT1 protein complexes antagonize pre-B-cell proliferation to promote B-cell development.

Wu, Glendon S / Bassing, Craig H

Cellular & molecular immunology

2018 Volume 15, Issue 9, Page(s) 808–811

MeSH term(s)	Cell Proliferation ; Cyclin D3 ; Precursor Cells, B-Lymphoid
Chemical Substances	Cyclin D3
Language	English
Publishing date	2018-02-12
Publishing country	China
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Comment
ZDB-ID	2435097-7
ISSN	2042-0226 ; 1672-7681
ISSN (online)	2042-0226
ISSN	1672-7681
DOI	10.1038/cmi.2017.156
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