Aging-associated HELIOS deficiency in naive CD4
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
15
01
2022
accepted:
24
10
2022
pmc-release:
01
01
2024
pubmed:
13
12
2022
medline:
6
1
2023
entrez:
12
12
2022
Statut:
ppublish
Résumé
Immune aging combines cellular defects in adaptive immunity with the activation of pathways causing a low-inflammatory state. Here we examined the influence of age on the kinetic changes in the epigenomic and transcriptional landscape induced by T cell receptor (TCR) stimulation in naive CD4
Identifiants
pubmed: 36510022
doi: 10.1038/s41590-022-01369-x
pii: 10.1038/s41590-022-01369-x
pmc: PMC10118794
mid: NIHMS1879118
doi:
Substances chimiques
Receptors, Antigen, T-Cell
0
STAT5 Transcription Factor
0
IKZF2 protein, human
0
Ikaros Transcription Factor
148971-36-2
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
96-109Subventions
Organisme : NIAID NIH HHS
ID : R01 AI129191
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL142068
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI108906
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI108891
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI057266
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR042527
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG045779
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL117913
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
O’Driscoll, M. et al. Age-specific mortality and immunity patterns of SARS-CoV-2. Nature 590, 140–145 (2021).
doi: 10.1038/s41586-020-2918-0
Rydyznski Moderbacher, C. et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 183, 996–1012 (2020).
doi: 10.1016/j.cell.2020.09.038
Gustafson, C. E., Kim, C., Weyand, C. M. & Goronzy, J. J. Influence of immune aging on vaccine responses. J. Allergy Clin. Immunol. 145, 1309–1321 (2020).
doi: 10.1016/j.jaci.2020.03.017
Weng, N. P. Aging of the immune system: how much can the adaptive immune system adapt? Immunity 24, 495–499 (2006).
doi: 10.1016/j.immuni.2006.05.001
Furman, D. et al. Chronic inflammation in the etiology of disease across the life span. Nat. Med. 25, 1822–1832 (2019).
doi: 10.1038/s41591-019-0675-0
Goronzy, J. J. & Weyand, C. M. Mechanisms underlying T cell ageing. Nat. Rev. Immunol. 19, 573–583 (2019).
doi: 10.1038/s41577-019-0180-1
Mittelbrunn, M. & Kroemer, G. Hallmarks of T cell aging. Nat. Immunol. 22, 687–698 (2021).
doi: 10.1038/s41590-021-00927-z
Whiting, C. C. et al. Large-scale and comprehensive immune profiling and functional analysis of normal human aging. PLoS ONE 10, e0133627 (2015).
doi: 10.1371/journal.pone.0133627
Qi, Q. et al. Diversity and clonal selection in the human T-cell repertoire. Proc. Natl Acad. Sci. USA 111, 13139–13144 (2014).
doi: 10.1073/pnas.1409155111
Fülöp, T. et al. Age-related impairment of p56lck and ZAP-70 activities in human T lymphocytes activated through the TcR/CD3 complex. Exp. Gerontol. 34, 197–216 (1999).
doi: 10.1016/S0531-5565(98)00061-8
Li, G. et al. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat. Med. 18, 1518–1524 (2012).
doi: 10.1038/nm.2963
Pereira, B. I. et al. Sestrins induce natural killer function in senescent-like CD8
doi: 10.1038/s41590-020-0643-3
Kim, C. et al. Activation of miR-21-regulated pathways in immune aging selects against signatures characteristic of memory T cells. Cell Rep. 25, 2148–2162 (2018).
doi: 10.1016/j.celrep.2018.10.074
Goronzy, J. J. & Weyand, C. M. Successful and maladaptive T cell aging. Immunity 46, 364–378 (2017).
doi: 10.1016/j.immuni.2017.03.010
Elyahu, Y. et al. Aging promotes reorganization of the CD4 T cell landscape toward extreme regulatory and effector phenotypes. Sci. Adv. 5, eaaw8330 (2019).
doi: 10.1126/sciadv.aaw8330
Almanzar, N. et al. A single-cell transcriptomic atlas characterizes ageing tissues in the mouse. Nature 583, 590–595 (2020).
doi: 10.1038/s41586-020-2496-1
Mogilenko, D. A. et al. Comprehensive profiling of an aging immune system reveals clonal GZMK
doi: 10.1016/j.immuni.2020.11.005
den Braber, I. et al. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity 36, 288–297 (2012).
doi: 10.1016/j.immuni.2012.02.006
Zhang, H., Weyand, C. M. & Goronzy, J. J. Hallmarks of the aging T-cell system. FEBS J. 288, 7123–7142 (2021).
doi: 10.1111/febs.15770
Kaech, S. M., Hemby, S., Kersh, E. & Ahmed, R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111, 837–851 (2002).
doi: 10.1016/S0092-8674(02)01139-X
Kurachi, M. et al. The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8
doi: 10.1038/ni.2834
Davenport, M. P., Smith, N. L. & Rudd, B. D. Building a T cell compartment: how immune cell development shapes function. Nat. Rev. Immunol. 20, 499–506 (2020).
doi: 10.1038/s41577-020-0332-3
Roychoudhuri, R. et al. BACH2 regulates CD8
doi: 10.1038/ni.3441
Yao, C. et al. BACH2 enforces the transcriptional and epigenetic programs of stem-like CD8
doi: 10.1038/s41590-021-00868-7
Li, H. et al. Dysfunctional CD8 T cells form a proliferative, dynamically regulated compartment within human melanoma. Cell 176, 775–789 (2019).
doi: 10.1016/j.cell.2018.11.043
Pulko, V. et al. Human memory T cells with a naive phenotype accumulate with aging and respond to persistent viruses. Nat. Immunol. 17, 966–975 (2016).
doi: 10.1038/ni.3483
Simeonov, D. R. et al. Discovery of stimulation-responsive immune enhancers with CRISPR activation. Nature 549, 111–115 (2017).
doi: 10.1038/nature23875
Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996–1006 (2002).
doi: 10.1101/gr.229102
Rosenbloom, K. R. et al. ENCODE data in the UCSC genome browser: year 5 update. Nucleic Acids Res. 41, D56–D63 (2013).
doi: 10.1093/nar/gks1172
Kim, H. J. et al. Stable inhibitory activity of regulatory T cells requires the transcription factor Helios. Science 350, 334–339 (2015).
doi: 10.1126/science.aad0616
Thornton, A. M. et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3
doi: 10.4049/jimmunol.0904028
Yang, Z. et al. Restoring oxidant signaling suppresses proarthritogenic T cell effector functions in rheumatoid arthritis. Sci. Transl. Med. 8, 331ra338 (2016).
doi: 10.1126/scitranslmed.aad7151
Wang, E. S. et al. Acute pharmacological degradation of Helios destabilizes regulatory T cells. Nat. Chem. Biol. 17, 711–717 (2021).
doi: 10.1038/s41589-021-00802-w
Liao, W., Lin, J.-X., Wang, L., Li, P. & Leonard, W. J. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12, 551–559 (2011).
doi: 10.1038/ni.2030
Jin, J. et al. Activation of mTORC1 at late endosomes misdirects T cell fate decision in older individuals. Sci. Immunol. 6, 791–791 (2021).
doi: 10.1126/sciimmunol.abg0791
Pekalski, M. L. et al. Postthymic expansion in human CD4 naive T cells defined by expression of functional high-affinity IL-2 receptors. J. Immunol. 190, 2554–2566 (2013).
doi: 10.4049/jimmunol.1202914
Kalia, V. et al. Prolonged interleukin-2Rα expression on virus-specific CD8
doi: 10.1016/j.immuni.2009.11.010
Lindahl, L. M. et al. STAT5 induces miR-21 expression in cutaneous T cell lymphoma. Oncotarget 7, 45730–45744 (2016).
doi: 10.18632/oncotarget.10160
Johnston, R. J., Choi, Y. S., Diamond, J. A., Yang, J. A. & Crotty, S. STAT5 is a potent negative regulator of T
doi: 10.1084/jem.20111174
Canale, F. P. et al. CD39 expression defines cell exhaustion in tumor-infiltrating CD8
doi: 10.1158/0008-5472.CAN-16-2684
Cao, W. et al. Ecto-NTPDase CD39 is a negative checkpoint that inhibits follicular helper cell generation. J. Clin. Invest. 130, 3422–3436 (2020).
doi: 10.1172/JCI132417
Fang, F. et al. Expression of CD39 on activated T cells impairs their survival in older individuals. Cell Rep. 14, 1218–1231 (2016).
doi: 10.1016/j.celrep.2016.01.002
Hetemäki, I. et al. Loss-of-function mutation in IKZF2 leads to immunodeficiency with dysregulated germinal center reactions and reduction of MAIT cells. Sci. Immunol. 6, 3454 (2021).
doi: 10.1126/sciimmunol.abe3454
Serre, K. et al. Helios is associated with CD4 T cells differentiating to T helper 2 and follicular helper T cells in vivo independently of Foxp3 expression. PLoS ONE 6, e20731 (2011).
doi: 10.1371/journal.pone.0020731
Shahin, T. et al. Germline biallelic mutation affecting the transcription factor Helios causes pleiotropic defects of immunity. Sci. Immunol. 6, 3981 (2021).
doi: 10.1126/sciimmunol.abe3981
Baine, I., Basu, S., Ames, R., Sellers, R. S. & Macian, F. Helios induces epigenetic silencing of IL2 gene expression in regulatory T cells. J. Immunol. 190, 1008 (2013).
doi: 10.4049/jimmunol.1200792
Sheng, W. et al. STAT5 programs a distinct subset of GM-CSF-producing T helper cells that is essential for autoimmune neuroinflammation. Cell Res. 24, 1387–1402 (2014).
doi: 10.1038/cr.2014.154
Fu, Y. et al. STAT5 promotes accessibility and is required for BATF-mediated plasticity at the Il9 locus. Nat. Commun. 11, 1–16 (2020).
doi: 10.1038/s41467-020-18648-6
Hu, B. et al. Transcription factor networks in aged naive CD4 T cells bias lineage differentiation. Aging Cell 18, e12957 (2019).
doi: 10.1111/acel.12957
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.21–21.29.29 (2015).
doi: 10.1002/0471142727.mb2129s109
Schep, A. N., Wu, B., Buenrostro, J. D. & Greenleaf, W. J. chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat. Methods 14, 975–978 (2017).
doi: 10.1038/nmeth.4401
Hansen, K. D., Irizarry, R. A. & Wu, Z. Removing technical variability in RNA-seq data using conditional quantile normalization. Biostatistics 13, 204–216 (2012).
doi: 10.1093/biostatistics/kxr054
McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495–501 (2010).
doi: 10.1038/nbt.1630
Yu, G., Wang, L.-G. & He, Q.-Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382–2383 (2015).
doi: 10.1093/bioinformatics/btv145
Granja, J. M. et al. ArchR is a scalable software package for integrative single-cell chromatin accessibility analysis. Nat. Genet. 53, 403–411 (2021).
doi: 10.1038/s41588-021-00790-6
Liberzon, A. et al. Molecular signatures database (MSigDB) 3.0. Bioinformatics 27, 1739–1740 (2011).
doi: 10.1093/bioinformatics/btr260
Subramanian, A. et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
doi: 10.1073/pnas.0506580102
Abbas, A. R. et al. Immune response in silico (IRIS): immune-specific genes identified from a compendium of microarray expression data. Genes Immun. 6, 319–331 (2005).
doi: 10.1038/sj.gene.6364173
Kolmykov, S. et al. GTRD: an integrated view of transcription regulation. Nucleic Acids Res. 49, D104–D111 (2021).
doi: 10.1093/nar/gkaa1057
Marzec, M. et al. Differential effects of interleukin-2 and interleukin-15 versus interleukin-21 on CD4
doi: 10.1158/0008-5472.CAN-07-2403
Wen, Z. et al. N-myristoyltransferase deficiency impairs activation of kinase AMPK and promotes synovial tissue inflammation. Nat. Immunol. 20, 313–325 (2019).
doi: 10.1038/s41590-018-0296-7
Wu, B. et al. Mitochondrial aspartate regulates TNF biogenesis and autoimmune tissue inflammation. Nat. Immunol. 22, 1551–1562 (2021).
doi: 10.1038/s41590-021-01065-2
Moskowitz, D. M. et al. Epigenomics of human CD8 T cell differentiation and aging. Sci. Immunol. 2, eaag0192 (2017).
doi: 10.1126/sciimmunol.aag0192