A CD4+ T cell population expanded in lupus blood provides B cell help through interleukin-10 and succinate
Open accessAbstract
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.
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In the blood of patients with SLE, concomitant oxidation of mitochondrial DNA and Notch pathway signalling induce expansion of a unique population of CD4+ T cells known as T helper 10 cells.
“In the blood of patients with SLE, concomitant oxidation of mtDNA and signalling through the Notch pathway induce the expansion of a unique population of CD4+ T cells (CXCR5−CXCR3+PD1hiCD4+ T cells, known as T helper 10 (TH10) cells)75,76”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [75]
The paper reports that CXCR5− CXCR3+ PD1hi CD4+ T cells are expanded in SLE blood and that similar cells can be generated in vitro using plasmacytoid dendritic cells activated by oxidized mtDNA (Abstract; passage [2]). It does not establish that oxidized mtDNA and Notch signalling act together to induce their expansion in patients, and our copy does not identify the cells as TH10 (searched: Notch, TH10). (LLM, conf=0.88)
Experimental — accuracy not yet measuredSuccinate accumulation in T helper 10 cells enables altered electron transport chain activity, leading to production of IL-10 and mitochondrial reactive oxygen species and acquisition of B cell helper functions.
“Accumulation of succinate in TH10 cells enables an altered type of electron transport chain activity, ultimately leading to the production of IL-10 and mtROS, and acquisition of B cell helper functions75”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [75]
The Abstract reports succinate-fueled reverse electron transport as the cause of mtROS accumulation in the lupus CD4+ T-cell population, and says the cells provide B-cell help through IL-10 and succinate. It does not establish that reverse electron transport leads to IL-10 production; the claim folds that separate finding into the same causal chain. (LLM, conf=0.84)
Experimental — accuracy not yet measuredT helper 10 cells might contribute to SLE pathogenesis and end organ damage by supporting extrafollicular humoral responses.
“These cells might contribute to SLE pathogenesis and end organ damage via supporting extrafollicular humoral responses75”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [75]
pDCs activated by oxidized mtDNA induce a unique CD4+ T cell population TH10 with altered metabolism, accumulated mtROS and succinate, and high IL-10 and IFNγ but not IL-21.
“Moreover, pDCs activated by oxidized mtDNA induce a unique population of CD4+ T cells, TH10 (CXCR5−CXCR3+PD1hiCD4+ T cell), that have altered metabolic features; these cells have accumulated levels of mtROS and succinate and produce large amounts of IL-10 and IFNγ but not IL-21 (REF.75).”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [75]
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- Authors
- Caielli, S., Veiga, D. T., Balasubramanian, P., Athale, S., Domic, B., Murat, E., Banchereau, R., Xu, Z., Chandra, M., Chung, C.-H., Walters, L., Baisch, J., Wright, T., Punaro, M., Nassi, L., Stewart, K., Fuller, J., Ucar, D., Ueno, H., Zhou, J., Banchereau, J., & Pascual, V.
- Affiliations
- Weill Cornell Medicine (US)
- The Jackson Laboratory for Genomic Medicine (US)
- Texas Scottish Rite Hospital for Children (US)
- Icahn School of Medicine at Mount Sinai (US)
- Pathologist Bio-Medical Laboratories (US)
- Corresponding author
- Pascual, Virginia
- ORCID
- Venue
- Nature Medicine
- Published
- 2018-11-26
- Volume
- 25
- Issue
- 1
- Pages
- 75-81
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC6325012
- OpenAlex
- W2900950647
- Cited by
- 263
- References
- 51
- Citations by year
- 2026: 13 · 2025: 25 · 2024: 44 · 2023: 32 · 2022: 46 · 2021: 38 · 2020: 35 · 2019: 28 · 2018: 2
- FWCI
- 22.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (U19AI082715)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (P50AR054083, P50AR070594)
- Topics
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Keywords
- systemic lupus erythematosus, lupus nephritis, CD4+ T cells, B cell help, IL-10, succinic acid, reverse electron transfer, mitochondrial reactive oxygen species, PD-1, T follicular helper cells, plasmacytoid dendritic cells, oxidized mitochondrial DNA, TLR9, autoantibody production
- MeSH terms
- B-Lymphocytes, Dendritic Cells, DNA, Mitochondrial, Humans, Immunologic Memory, Lupus Erythematosus, Systemic, Lupus Nephritis, Oxidation-Reduction, CD4-Positive T-Lymphocytes, Interleukin-10, Succinic Acid, Cell Proliferation
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