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Modeling of TREX1-Dependent Autoimmune Disease using Human Stem Cells Highlights L1 Accumulation as a Source of Neuroinflammation
Open accessAbstract
Three-prime repair exonuclease 1 (TREX1) is an anti-viral enzyme that cleaves nucleic acids in the cytosol, preventing accumulation and a subsequent type I interferon-associated inflammatory response. Autoimmune diseases, including Aicardi-Goutières syndrome (AGS) and systemic lupus erythematosus, can arise when TREX1 function is compromised. AGS is a neuroinflammatory disorder with severe and persistent intellectual and physical problems. Here we generated a human AGS model that recapitulates disease-relevant phenotypes using pluripotent stem cells lacking TREX1. We observed abundant extrachromosomal DNA in TREX1-deficient neural cells, of which endogenous Long Interspersed Element-1 retrotransposons were a major source. TREX1-deficient neurons also exhibited increased apoptosis and formed three-dimensional cortical organoids of reduced size. TREX1-deficient astrocytes further contributed to the observed neurotoxicity through increased type I interferon secretion. In this model, reverse-transcriptase inhibitors rescued the neurotoxicity of AGS neurons and organoids, highlighting their potential utility in therapeutic regimens for AGS and related disorders.
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“Retrotransposition is greatly diminished in non-dividing cells94, although low levels could be detected in senescent cells33 or neurons92, and it is possible that abortive products of these processes could accumulate.”
From The role of retrotransposable elements in ageing and age-associated diseases (2021) · cites this paper as [92]
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“Importantly, treatment with nucleoside reverse transcriptase inhibitor (NRTI) drugs that inhibit L1 reverse transcriptase, or a knockdown of L1 expression with shRNAs against active L1 families, decreased cytoplasmic L1 DNAs and ameliorated cGAS and IFN-I activation33, 34, 92.”
From The role of retrotransposable elements in ageing and age-associated diseases (2021) · cites this paper as [92]
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“Cells were routinely tested for mycoplasma contamination by PCR as previously described (58) using primers for-GGCGAATGGGTGAGTAACACG and rev-CGGATAACGCTTGCGACCTATG. Any mycoplasma-positive samples were immediately discarded.”
From Reduction of nemo-like kinase increases lysosome biogenesis and ameliorates TDP-43–related neurodegeneration (2023) · cites this paper as [58]
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“Brain organoid models have been shown to recapitulate cell proliferation effects in microcephaly (Thomas et al., 2017) and have been used to study neural migration defects in Timothy syndrome, a rare ASD form caused by mutations in the Cav1.2 calcium channel gene (Birey et al., 2017).”
From Getting to the cores of autism (2019) · cites this paper as Thomas et al., 2017
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“Although TPRT occurs in the nucleus, L1 cDNA has also been found in the cytosol in certain conditions, such as autoimmunity (Stetson et al., 2008; Thomas et al., 2017), and others which will be discussed in more detail below.”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Thomas et al., 2017
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Metadata
- Authors
- Thomas, C. A., Tejwani, L., Trujillo, C. A., Negraes, P. D., Herai, R. H., Mesci, P., Macia, A., Crow, Y. J., & Muotri, A. R.
- Affiliations
- University of California San Diego (US)
- Yale University (US)
- Pontifícia Universidade Católica do Paraná (BR)
- Hôpital Necker-Enfants Malades (FR)
- Corresponding author
- Muotri, Alysson R.
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2017-09
- Volume
- 21
- Issue
- 3
- Pages
- 319-331.e8
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC5591075
- OpenAlex
- W2745112353
- Cited by
- 330
- References
- 72
- Citations by year
- 2026: 19 · 2025: 40 · 2024: 30 · 2023: 35 · 2022: 49 · 2021: 43 · 2020: 53 · 2019: 35 · 2018: 21 · 2017: 5
- FWCI
- 14.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- NIH (R01MH108528, R01MH094753, R01MH109885, R01MH100175, R21MH107771, R56MH109587, U19MH107367)
- Ruth L. Kirschstein NRSA Fellowship (1F31NS076198)
- California Institute for Regenerative Medicine (CIRM) (DISC1-08825)
- UCSD CTRI
- NARSAD
- European Research Council (GA 309449)
- ERA-NET Neuron (MR/M501803/1)
- National Research Agency (ANR-10-IAHU-01)
- Roche Postdoc Fellowship Program
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- TREX1, Aicardi-Goutières syndrome, systemic lupus erythematosus, extrachromosomal DNA, neuroinflammation, type I interferon, cortical organoids, neuronal apoptosis, astrocytes, reverse transcriptase inhibitors, autoinflammatory disease
- MeSH terms
- Astrocytes, Autoimmune Diseases, Base Sequence, Cell Extracts, Child, Cytosol, DNA, Exodeoxyribonucleases, Humans, Infant, Infant, Newborn, Inflammation, Interferons, Male, Microcephaly, Nervous System, Neurons, Organoids, Phenotype, Phosphoproteins, Stem Cells, Up-Regulation, Long Interspersed Nucleotide Elements, Neural Stem Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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