Pre-T cell receptor self-MHC sampling restricts thymocyte dedifferentiation.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
01 2023
Historique:
received: 03 09 2021
accepted: 11 11 2022
pubmed: 22 11 2022
medline: 21 1 2023
entrez: 21 11 2022
Statut: ppublish

Résumé

Programming T cells to distinguish self from non-self is a vital, multi-step process that occurs in the thymus

Identifiants

pubmed: 36410718
doi: 10.1038/s41586-022-05555-7
pii: 10.1038/s41586-022-05555-7
pmc: PMC9851994
mid: NIHMS1855620
doi:

Substances chimiques

Peptides 0
Receptors, Antigen, T-Cell 0
Histocompatibility Antigens Class I 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

565-574

Subventions

Organisme : NIAID NIH HHS
ID : P01 AI143565
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA006516
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI136301
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA006516-57
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Hosokawa, H. & Rothenberg, E. V. How transcription factors drive choice of the T cell fate. Nat. Rev. Immunol. 21, 162–176 (2021).
doi: 10.1038/s41577-020-00426-6
Koch, U. et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205, 2515–2523 (2008).
doi: 10.1084/jem.20080829
Rodewald, H. R., Ogawa, M., Haller, C., Waskow, C. & DiSanto, J. P. Pro-thymocyte expansion by c-kit and the common cytokine receptor γ chain is essential for repertoire formation. Immunity 6, 265–272 (1997).
doi: 10.1016/S1074-7613(00)80329-5
Shortman, K., Egerton, M., Spangrude, G. J. & Scollay, R. The generation and fate of thymocytes. Semin. Immunol. 2, 3–12 (1990).
Kreslavsky, T. et al. β-Selection-induced proliferation is required for αβ T cell differentiation. Immunity 37, 840–853 (2012).
doi: 10.1016/j.immuni.2012.08.020
von Boehmer, H. The thymus in immunity and in malignancy. Cancer Immunol. Res. 2, 592–597 (2014).
doi: 10.1158/2326-6066.CIR-14-0070
Das, D. K. et al. Pre-T cell receptors (Pre-TCRs) leverage Vβ complementarity determining regions (CDRs) and hydrophobic patch in mechanosensing thymic self-ligands. J. Biol. Chem. 291, 25292–25305 (2016).
doi: 10.1074/jbc.M116.752865
Li, X. et al. Pre-T cell receptors topologically sample self-ligands during thymocyte β-selection. Science 371, 181–185 (2021).
doi: 10.1126/science.abe0918
Mallis, R. J., Arthanari, H., Lang, M. J., Reinherz, E. L. & Wagner, G. NMR-directed design of pre-TCRβ and pMHC molecules implies a distinct geometry for pre-TCR relative to αβTCR recognition of pMHC. J. Biol. Chem. 293, 754–766 (2018).
doi: 10.1074/jbc.M117.813493
Mallis, R. J. et al. Pre-TCR ligand binding impacts thymocyte development before αβTCR expression. Proc. Natl Acad. Sci. USA 112, 8373–8378 (2015).
doi: 10.1073/pnas.1504971112
Davis, M. M. & Bjorkman, P. J. T-cell antigen receptor genes and T-cell recognition. Nature 334, 395–402 (1988).
doi: 10.1038/334395a0
Rudolph, M. G., Stanfield, R. L. & Wilson, I. A. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24, 419–466 (2006).
doi: 10.1146/annurev.immunol.23.021704.115658
Wang, J. H. & Reinherz, E. L. The structural basis of αβ T-lineage immune recognition: TCR docking topologies, mechanotransduction, and co-receptor function. Immunol. Rev. 250, 102–119 (2012).
doi: 10.1111/j.1600-065X.2012.01161.x
Saint-Ruf, C. et al. Analysis and expression of a cloned pre-T cell receptor gene. Science 266, 1208–1212 (1994).
doi: 10.1126/science.7973703
Xiong, J., Armato, M. A. & Yankee, T. M. Immature single-positive CD8
doi: 10.1093/intimm/dxq457
Petrie, H. T. et al. Multiple rearrangements in T cell receptor α chain genes maximize the production of useful thymocytes. J. Exp. Med. 178, 615–622 (1993).
doi: 10.1084/jem.178.2.615
Shinkai, Y. et al. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science 259, 822–825 (1993).
doi: 10.1126/science.8430336
Wilson, A., Held, W. & MacDonald, H. R. Two waves of recombinase gene expression in developing thymocytes. J. Exp. Med. 179, 1355–1360 (1994).
doi: 10.1084/jem.179.4.1355
Klein, L., Kyewski, B., Allen, P. M. & Hogquist, K. A. Positive and negative selection of the T cell repertoire: what thymocytes see (and don’t see). Nat. Rev. Immunol. 14, 377–391 (2014).
doi: 10.1038/nri3667
Fehling, H. J., Krotkova, A., Saint-Ruf, C. & von Boehmer, H. Crucial role of the pre-T-cell receptor α gene in development of αβ but not γδ T cells. Nature 375, 795–798 (1995).
doi: 10.1038/375795a0
Grusby, M. J. et al. Mice lacking major histocompatibility complex class I and class II molecules. Proc. Natl Acad. Sci. USA 90, 3913–3917 (1993).
doi: 10.1073/pnas.90.9.3913
Irving, B. A., Alt, F. W. & Killeen, N. Thymocyte development in the absence of pre-T cell receptor extracellular immunoglobulin domains. Science 280, 905–908 (1998).
doi: 10.1126/science.280.5365.905
Koller, B. H., Marrack, P., Kappler, J. W. & Smithies, O. Normal development of mice deficient in β2M, MHC class I proteins, and CD8
doi: 10.1126/science.2112266
Mizsei, R. et al. A general chemical crosslinking strategy for structural analyses of weakly interacting proteins applied to preTCR–pMHC complexes. J. Biol. Chem. 296, 100255 (2021).
doi: 10.1016/j.jbc.2021.100255
Xiao, S. Y., Li, Y. & Chen, W. F. Kinetics of thymocyte developmental process in fetal and neonatal mice. Cell Res. 13, 265–273 (2003).
doi: 10.1038/sj.cr.7290171
Mingueneau, M. et al. The transcriptional landscape of αβ T cell differentiation. Nat. Immunol. 14, 619–632 (2013).
doi: 10.1038/ni.2590
Allman, D. et al. Separation of Notch1 promoted lineage commitment and expansion/transformation in developing T cells. J. Exp. Med. 194, 99–106 (2001).
doi: 10.1084/jem.194.1.99
Forman, J. & Fischer Lindahl, K. Listing, location, binding motifs, and expression of nonclassical class i and related genes and molecules. Curr. Protoc. Immunol. 49, A.1M.1–A.1M.13 (2002).
Fujita, T., Yuno, M., Okuzaki, D., Ohki, R. & Fujii, H. Identification of non-coding RNAs associated with telomeres using a combination of enChIP and RNA sequencing. PLoS ONE 10, e0123387 (2015).
doi: 10.1371/journal.pone.0123387
Lin, Y. W. & Aplan, P. D. Gene expression profiling of precursor T-cell lymphoblastic leukemia/lymphoma identifies oncogenic pathways that are potential therapeutic targets. Leukemia 21, 1276–1284 (2007).
doi: 10.1038/sj.leu.2404685
Li, R. & Guan, M. X. Human mitochondrial leucyl-tRNA synthetase corrects mitochondrial dysfunctions due to the tRNA
doi: 10.1128/MCB.01614-09
Coustan-Smith, E. et al. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol. 10, 147–156 (2009).
doi: 10.1016/S1470-2045(08)70314-0
Vadillo, E., Dorantes-Acosta, E., Pelayo, R. & Schnoor, M. T cell acute lymphoblastic leukemia (T-ALL): New insights into the cellular origins and infiltration mechanisms common and unique among hematologic malignancies. Blood Rev. 32, 36–51 (2018).
doi: 10.1016/j.blre.2017.08.006
Dai, Y.-T. et al. Transcriptome-wide subtyping of pediatric and adult T cell acute lymphoblastic leukemia in an international study of 707 cases. Proc. Natl Acad. Sci. USA 119, e2120787119 (2022).
doi: 10.1073/pnas.2120787119
Pellicci, D. G., Koay, H. F. & Berzins, S. P. Thymic development of unconventional T cells: how NKT cells, MAIT cells and γδ T cells emerge. Nat. Rev. Immunol. 20, 756–770 (2020).
doi: 10.1038/s41577-020-0345-y
Thoms, J. A. I. et al. Disruption of a GATA2, TAL1, ERG regulatory circuit promotes erythroid transition in healthy and leukemic stem cells. Blood 138, 1441–1455 (2021).
doi: 10.1182/blood.2020009707
Ng, S. W. et al. A 17-gene stemness score for rapid determination of risk in acute leukaemia. Nature 540, 433–437 (2016).
doi: 10.1038/nature20598
Mandal, M. et al. The BCL2A1 gene as a pre-T cell receptor-induced regulator of thymocyte survival. J. Exp. Med. 201, 603–614 (2005).
doi: 10.1084/jem.20041924
Koyasu, S. et al. Pre-TCR signaling components trigger transcriptional activation of a rearranged TCR α gene locus and silencing of the pre-TCR α locus: implications for intrathymic differentiation. Int. Immunol. 9, 1475–1480 (1997).
doi: 10.1093/intimm/9.10.1475
Amson, R. et al. The human protooncogene product p33pim is expressed during fetal hematopoiesis and in diverse leukemias. Proc. Natl Acad. Sci. USA 86, 8857–8861 (1989).
doi: 10.1073/pnas.86.22.8857
Reinherz, E. L., Kung, P. C., Goldstein, G., Levey, R. H. & Schlossman, S. F. Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc. Natl Acad. Sci. USA 77, 1588–1592 (1980).
doi: 10.1073/pnas.77.3.1588
Van Vlierberghe, P. & Ferrando, A. The molecular basis of T cell acute lymphoblastic leukemia. J. Clin. Invest. 122, 3398–3406 (2012).
doi: 10.1172/JCI61269
Girardi, T., Vicente, C., Cools, J. & De Keersmaecker, K. The genetics and molecular biology of T-ALL. Blood 129, 1113–1123 (2017).
doi: 10.1182/blood-2016-10-706465
Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157–163 (2012).
doi: 10.1038/nature10725
Condorelli, G. L. et al. T-cell-directed TAL-1 expression induces T-cell malignancies in transgenic mice. Cancer Res. 56, 5113–5119 (1996).
Kelliher, M. A., Seldin, D. C. & Leder, P. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase IIα. EMBO J. 15, 5160–5166 (1996).
doi: 10.1002/j.1460-2075.1996.tb00900.x
De Keersmaecker, K. et al. The TLX1 oncogene drives aneuploidy in T cell transformation. Nat. Med. 16, 1321–1327 (2010).
doi: 10.1038/nm.2246
Rakowski, L. A., Lehotzky, E. A. & Chiang, M. Y. Transient responses to NOTCH and TLX1/HOX11 inhibition in T-cell acute lymphoblastic leukemia/lymphoma. PLoS ONE 6, e16761 (2011).
doi: 10.1371/journal.pone.0016761
Martins, V. C. et al. Cell competition is a tumour suppressor mechanism in the thymus. Nature 509, 465–470 (2014).
doi: 10.1038/nature13317
Paiva, R. A. et al. Self-renewal of double-negative 3 early thymocytes enables thymus autonomy but compromises the β-selection checkpoint. Cell Rep. 35, 108967 (2021).
doi: 10.1016/j.celrep.2021.108967
Khan, M., Siddiqi, R. & Naqvi, K. An update on classification, genetics, and clinical approach to mixed phenotype acute leukemia (MPAL). Ann. Hematol. 97, 945–953 (2018).
doi: 10.1007/s00277-018-3297-6
Kai, T. & Spradling, A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428, 564–569 (2004).
doi: 10.1038/nature02436
Cobaleda, C., Jochum, W. & Busslinger, M. Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors. Nature 449, 473–477 (2007).
doi: 10.1038/nature06159
Laiosa, C. V., Stadtfeld, M., Xie, H., de Andres-Aguayo, L. & Graf, T. Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBPα and PU.1 transcription factors. Immunity 25, 731–744 (2006).
doi: 10.1016/j.immuni.2006.09.011
Riddell, J. et al. Reprogramming committed murine blood cells to induced hematopoietic stem cells with defined factors. Cell 157, 549–564 (2014).
doi: 10.1016/j.cell.2014.04.006
Jacobs, H. et al. Oncogenic potential of a pre-T cell receptor lacking the TCRβ variable domain. Oncogene 12, 2089–2099 (1996).
Charnley, M., Ludford-Menting, M., Pham, K. & Russell, S. M. A new role for Notch in the control of polarity and asymmetric cell division of developing T cells. J. Cell Sci. 133, jcs235358 (2019).
doi: 10.1242/jcs.235358
Mohtashami, M. et al. Direct comparison of Dll1- and Dll4-mediated Notch activation levels shows differential lymphomyeloid lineage commitment outcomes. J. Immunol. 185, 867–876 (2010).
doi: 10.4049/jimmunol.1000782
Mamedov, I. Z. et al. Preparing unbiased T-cell receptor and antibody cDNA libraries for the deep next generation sequencing profiling. Front. Immunol. 4, 456 (2013).
doi: 10.3389/fimmu.2013.00456
Bolotin, D. A. et al. MiXCR: software for comprehensive adaptive immunity profiling. Nat. Methods 12, 380–381 (2015).
doi: 10.1038/nmeth.3364
Shugay, M. et al. VDJtools: unifying post-analysis of T cell receptor repertoires. PLoS Comput. Biol. 11, e1004503 (2015).
doi: 10.1371/journal.pcbi.1004503
Wang, X., Spandidos, A., Wang, H. & Seed, B. PrimerBank: a PCR primer database for quantitative gene expression analysis, 2012 update. Nucleic Acids Res. 40, D1144–D1149 (2012).
doi: 10.1093/nar/gkr1013
Ruijter, J. M. et al. Evaluation of qPCR curve analysis methods for reliable biomarker discovery: bias, resolution, precision, and implications. Methods 59, 32–46 (2013).
doi: 10.1016/j.ymeth.2012.08.011
Shugay, M. et al. Towards error-free profiling of immune repertoires. Nat. Methods 11, 653–655 (2014).
doi: 10.1038/nmeth.2960
Han, F. F. et al. Profiling the pattern of human TRB/IGH-CDR3 repertoire in liver transplantation patients via high-throughput sequencing analysis. Scand. J. Immunol. 92, e12912 (2020).
doi: 10.1111/sji.12912
Stevant, I. et al. Dissecting cell lineage specification and sex fate determination in gonadal somatic cells using single cell transcriptomics. Cell Rep. 26, 3272–3283.e3 (2019).
doi: 10.1016/j.celrep.2019.02.069
Godfrey, A. K. et al. Quantitative analysis of Y-chromosome gene expression across 36 human tissues. Genome Res. 30, 860–873 (2020).
doi: 10.1101/gr.261248.120

Auteurs

Jonathan S Duke-Cohan (JS)

Laboratory of Immunobiology, Dana-Farber Cancer Institute, Boston, MA, USA. jonathan_duke-cohan@dfci.harvard.edu.
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. jonathan_duke-cohan@dfci.harvard.edu.
Department of Medicine, Harvard Medical School, Boston, MA, USA. jonathan_duke-cohan@dfci.harvard.edu.

Aoi Akitsu (A)

Laboratory of Immunobiology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Medicine, Harvard Medical School, Boston, MA, USA.

Robert J Mallis (RJ)

Laboratory of Immunobiology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Dermatology, Harvard Medical School, Boston, MA, USA.

Cameron M Messier (CM)

Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute, Boston, MA, USA.

Patrick H Lizotte (PH)

Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute, Boston, MA, USA.

Jon C Aster (JC)

Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.

Wonmuk Hwang (W)

Department of Biomedical Engineering, Texas A&M University, College Station, TX, USA.
Department of Materials Science and Engineering, Texas A&M University, College Station, TX, USA.
Department of Physics and Astronomy, Texas A&M University, College Station, TX, USA.

Matthew J Lang (MJ)

Department of Chemical and Biomolecular Engineering, Vanderbilt University, Nashville, TN, USA.
Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USA.

Ellis L Reinherz (EL)

Laboratory of Immunobiology, Dana-Farber Cancer Institute, Boston, MA, USA. ellis_reinherz@dfci.harvard.edu.
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. ellis_reinherz@dfci.harvard.edu.
Department of Medicine, Harvard Medical School, Boston, MA, USA. ellis_reinherz@dfci.harvard.edu.

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