دورية أكاديمية
أعرض في EDS

A CD4 + T cell population expanded in lupus blood provides B cell help through interleukin-10 and succinate.

التفاصيل البيبلوغرافية
العنوان: A CD4 + T cell population expanded in lupus blood provides B cell help through interleukin-10 and succinate.
المؤلفون: Caielli S; Baylor Institute for Immunology Research, Dallas, TX, USA.; Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA.; Department of Pediatrics, Weill Cornell Medicine, New York, NY, USA., Veiga DT; The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA., Balasubramanian P; Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA.; Department of Pediatrics, Weill Cornell Medicine, New York, NY, USA., Athale S; Baylor Institute for Immunology Research, Dallas, TX, USA., Domic B; Baylor Institute for Immunology Research, Dallas, TX, USA., Murat E; Baylor Institute for Immunology Research, Dallas, TX, USA.; Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA.; Department of Pediatrics, Weill Cornell Medicine, New York, NY, USA., Banchereau R; Baylor Institute for Immunology Research, Dallas, TX, USA., Xu Z; Baylor Institute for Immunology Research, Dallas, TX, USA., Chandra M; Baylor Institute for Immunology Research, Dallas, TX, USA., Chung CH; The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA., Walters L; Baylor Institute for Immunology Research, Dallas, TX, USA.; Texas Scottish Rite Hospital for Children, Dallas, TX, USA., Baisch J; Baylor Institute for Immunology Research, Dallas, TX, USA.; Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA.; Department of Pediatrics, Weill Cornell Medicine, New York, NY, USA., Wright T; Texas Scottish Rite Hospital for Children, Dallas, TX, USA.; Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, USA., Punaro M; Texas Scottish Rite Hospital for Children, Dallas, TX, USA.; Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, USA., Nassi L; Texas Scottish Rite Hospital for Children, Dallas, TX, USA.; Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, USA., Stewart K; Texas Scottish Rite Hospital for Children, Dallas, TX, USA.; Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, USA., Fuller J; Texas Scottish Rite Hospital for Children, Dallas, TX, USA.; Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, USA., Ucar D; The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA., Ueno H; Baylor Institute for Immunology Research, Dallas, TX, USA.; Mount Sinai School of Medicine, New York, NY, USA., Zhou J; Pathologists Bio-Medical Laboratories, Lewisville, TX, USA., Banchereau J; The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA., Pascual V; Baylor Institute for Immunology Research, Dallas, TX, USA. vip2021@med.cornell.edu.; Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA. vip2021@med.cornell.edu.; Department of Pediatrics, Weill Cornell Medicine, New York, NY, USA. vip2021@med.cornell.edu.; Texas Scottish Rite Hospital for Children, Dallas, TX, USA. vip2021@med.cornell.edu.
المصدر: Nature medicine [Nat Med] 2019 Jan; Vol. 25 (1), pp. 75-81. Date of Electronic Publication: 2018 Nov 26.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Company Country of Publication: United States NLM ID: 9502015 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1546-170X (Electronic) Linking ISSN: 10788956 NLM ISO Abbreviation: Nat Med Subsets: MEDLINE
أسماء مطبوعة: Publication: New York Ny : Nature Publishing Company
Original Publication: New York, NY : Nature Pub. Co., [1995-
مواضيع طبية MeSH: B-Lymphocytes/*immunology , CD4-Positive T-Lymphocytes/*immunology , Interleukin-10/*metabolism , Lupus Erythematosus, Systemic/*immunology , Succinic Acid/*metabolism, Cell Proliferation ; DNA, Mitochondrial/genetics ; Dendritic Cells/metabolism ; Humans ; Immunologic Memory ; Lupus Erythematosus, Systemic/pathology ; Lupus Nephritis/immunology ; Oxidation-Reduction
مستخلص: Understanding the mechanisms underlying autoantibody development will accelerate therapeutic target identification in autoimmune diseases such as systemic lupus erythematosus (SLE) 1 . Follicular helper T cells (T FH cells) have long been implicated in SLE pathogenesis. Yet a fraction of autoantibodies in individuals with SLE are unmutated, supporting that autoreactive B cells also differentiate outside germinal centers 2 . Here, we describe a CXCR5 - CXCR3 + programmed death 1 (PD1) hi CD4 + helper T cell population distinct from T FH cells and expanded in both SLE blood and the tubulointerstitial areas of individuals with proliferative lupus nephritis. These cells produce interleukin-10 (IL-10) and accumulate mitochondrial reactive oxygen species as the result of reverse electron transport fueled by succinate. Furthermore, they provide B cell help, independently of IL-21, through IL-10 and succinate. Similar cells are generated in vitro upon priming naive CD4 + T cells with plasmacytoid dendritic cells activated with oxidized mitochondrial DNA, a distinct class of interferogenic toll-like receptor 9 ligand 3 . Targeting this pathway might blunt the initiation and/or perpetuation of extrafollicular humoral responses in SLE.
التعليقات: Comment in: Nat Rev Rheumatol. 2019 Feb;15(2):63. doi: 10.1038/s41584-018-0150-1. (PMID: 30552381)
Comment in: Ann Rheum Dis. 2019 Jun;78(6):e59. doi: 10.1136/annrheumdis-2019-215597. (PMID: 31088799)
References: Tsokos, G. C. Systemic lupus erythematosus. N. Engl. J. Med. 365, 2110–2121 (2011). (PMID: 10.1056/NEJMra1100359)
Tipton, C. M. et al. Diversity, cellular origin and autoreactivity of antibody-secreting cell population expansions in acute systemic lupus erythematosus. Nat. Immunol. 16, 755–765 (2015). (PMID: 10.1038/ni.3175)
Caielli, S. et al. Oxidized mitochondrial nucleoids released by neutrophils drive type I interferon production in human lupus. J. Exp. Med. 213, 697–713 (2016). (PMID: 10.1084/jem.20151876)
Guiducci, C. et al. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature 465, 937–941 (2010). (PMID: 10.1038/nature09102)
Means, T. K. et al. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Investig. 115, 407–417 (2005). (PMID: 10.1172/JCI23025)
Gilliet, M. & Liu, Y. J. Human plasmacytoid-derived dendritic cells and the induction of T-regulatory cells. Hum. Immunol. 63, 1149–1155 (2002). (PMID: 10.1016/S0198-8859(02)00753-X)
Jego, G. et al. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19, 225–234 (2003). (PMID: 10.1016/S1074-7613(03)00208-5)
Ito, T. et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J. Exp. Med. 204, 105–115 (2007). (PMID: 10.1084/jem.20061660)
Gilliet, M., Cao, W. & Liu, Y. J. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8, 594–606 (2008). (PMID: 10.1038/nri2358)
Grouard, G. et al. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185, 1101–1111 (1997). (PMID: 10.1084/jem.185.6.1101)
Penna, G., Sozzani, S. & Adorini, L. Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J. Immunol. 167, 1862–1866 (2001). (PMID: 10.4049/jimmunol.167.4.1862)
Glimcher, L. H. & Murphy, K. M. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 14, 1693–1711 (2000). (PMID: 10898785)
Acosta-Rodriguez, E. V. et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8, 639–646 (2007). (PMID: 10.1038/ni1467)
Jackson, S. K., DeLoose, A. & Gilbert, K. M. The ability of antigen, but not interleukin-2, to promote n-butyrate-induced T helper 1 cell anergy is associated with increased expression and altered association patterns of cyclin-dependent kinase inhibitors. Immunology 106, 486–495 (2002). (PMID: 10.1046/j.1365-2567.2002.01457.x)
Sena, L. A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013). (PMID: 10.1016/j.immuni.2012.10.020)
Nag, S., Picard, P. & Stewart, D. J. Expression of nitric oxide synthases and nitrotyrosine during blood-brain barrier breakdown and repair after cold injury. Lab. Investig. 81, 41–49 (2001). (PMID: 10.1038/labinvest.3780210)
Guaras, A. et al. The CoQH 2 /CoQ ratio serves as a sensor of respiratory chain efficiency. Cell Rep. 15, 197–209 (2016). (PMID: 10.1016/j.celrep.2016.03.009)
Murphy, M. P. How mitochondria produce reactive oxygen species. Biochem. J. 417, 1–13 (2009). (PMID: 10.1042/BJ20081386)
Tannahill, G. M. et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1ɑ. Nature 496, 238–242 (2013). (PMID: 10.1038/nature11986)
Oaks, Z., Winans, T., Huang, N., Banki, K. & Perl, A. Activation of the mechanistic target of rapamycin in SLE: explosion of evidence in the last five years. Curr. Rheumatol. Rep. 18, 73 (2016). (PMID: 10.1007/s11926-016-0622-8)
Rousset, F. et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl Acad. Sci. USA 89, 1890–1893 (1992). (PMID: 10.1073/pnas.89.5.1890)
Moore, K. W., de Waal Malefyt, R., Coffman, R. L. & O’Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683–765 (2001). (PMID: 10.1146/annurev.immunol.19.1.683)
Ueno, H., Banchereau, J. & Vinuesa, C. G. Pathophysiology of T follicular helper cells in humans and mice. Nat. Immunol. 16, 142–152 (2015). (PMID: 10.1038/ni.3054)
Mills, E. & O’Neill, L. A. Succinate: a metabolic signal in inflammation. Trends Cell Biol. 24, 313–320 (2014). (PMID: 10.1016/j.tcb.2013.11.008)
Buck, M. D., O’Sullivan, D. & Pearce, E. L. T cell metabolism drives immunity. J. Exp. Med. 212, 1345–1360 (2015). (PMID: 10.1084/jem.20151159)
Keir, M. E., Butte, M. J., Freeman, G. J. & Sharpe, A. H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26, 677–704 (2008). (PMID: 10.1146/annurev.immunol.26.021607.090331)
Locci, M. et al. Human circulating PD-1 + CXCR3 − CXCR5 + memory T FH cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity 39, 758–769 (2013). (PMID: 10.1016/j.immuni.2013.08.031)
Morita, R. et al. Human blood CXCR5 + CD4 + T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 34, 108–121 (2011). (PMID: 10.1016/j.immuni.2010.12.012)
Patil, V. S. et al. Precursors of human CD4 + cytotoxic T lymphocytes identified by single-cell transcriptome analysis. Sci. Immunol, 3, eaan8664 (2018).
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013). (PMID: 10.1038/nmeth.2688)
Arce, E. et al. Increased frequency of pre-germinal center B cells and plasma cell precursors in the blood of children with systemic lupus erythematosus. J. Immunol. 167, 2361–2369 (2001). (PMID: 10.4049/jimmunol.167.4.2361)
Dorner, T. & Lipsky, P. E. Correlation of circulating CD27 high plasma cells and disease activity in systemic lupus erythematosus. Lupus 13, 283–289 (2004). (PMID: 10.1191/0961203304lu1014oa)
Rubtsov, A. V. et al. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c + B-cell population is important for the development of autoimmunity. Blood 118, 1305–1315 (2011). (PMID: 10.1182/blood-2011-01-331462)
Wang, S. et al. IL-21 drives expansion and plasma cell differentiation of autoreactive CD11c hi T-bet + B cells in SLE. Nat. Commun. 9, 1758 (2018). (PMID: 10.1038/s41467-018-03750-7)
Blanco, P. et al. Increase in activated CD8 + T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum. 52, 201–211 (2005). (PMID: 10.1002/art.20745)
Chang, A. et al. In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J. Immunol. 186, 1849–1860 (2011). (PMID: 10.4049/jimmunol.1001983)
Rao, D. A. et al. Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis. Nature 542, 110–114 (2017). (PMID: 10.1038/nature20810)
Peti-Peterdi, J. High glucose and renin release: the role of succinate and GPR91. Kidney Int. 78, 1214–1217 (2010). (PMID: 10.1038/ki.2010.333)
Weening, J. J. et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int. 65, 521–530 (2004). (PMID: 10.1111/j.1523-1755.2004.00443.x)
Hochberg, M. C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40, 1725 (1997). (PMID: 10.1002/art.1780400928)
Anoopkumar-Dukie, S. et al. Resazurin assay of radiation response in cultured cells. Br. J. Radiol. 78, 945–947 (2005). (PMID: 10.1259/bjr/54004230)
Schmitt, N. et al. The cytokine TGF-β co-opts signaling via STAT3-STAT4 to promote the differentiation of human TFH cells. Nat. Immunol. 15, 856–865 (2014). (PMID: 10.1038/ni.2947)
Garrone, P. et al. Fas ligation induces apoptosis of CD40-activated human B lymphocytes. J. Exp. Med. 182, 1265–1273 (1995). (PMID: 10.1084/jem.182.5.1265)
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). (PMID: 10.1093/bioinformatics/btu170)
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009). (PMID: 10.1093/bioinformatics/btp324)
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). (PMID: 10.1093/bioinformatics/btv145)
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010). (PMID: 10.1016/j.molcel.2010.05.004)
Salabei, J. K., Gibb, A. A. & Hill, B. G. Comprehensive measurement of respiratory activity in permeabilized cells using extracellular flux analysis. Nat. Protoc. 9, 421–438 (2014). (PMID: 10.1038/nprot.2014.018)
معلومات مُعتمدة: P50 AR054083 United States AR NIAMS NIH HHS; P50 AR070594 United States AR NIAMS NIH HHS; U19 AI082715 United States AI NIAID NIH HHS
المشرفين على المادة: 0 (DNA, Mitochondrial)
130068-27-8 (Interleukin-10)
AB6MNQ6J6L (Succinic Acid)
تواريخ الأحداث: Date Created: 20181128 Date Completed: 20190510 Latest Revision: 20240610
رمز التحديث: 20240610
مُعرف محوري في PubMed: PMC6325012
DOI: 10.1038/s41591-018-0254-9
PMID: 30478422
قاعدة البيانات: MEDLINE
الوصف
تدمد:1546-170X
DOI:10.1038/s41591-018-0254-9