m6A-dependent circular RNA formation mediates tau-induced neurotoxicity
Open accessAbstract
Circular RNAs (circRNAs), covalently closed RNA molecules that form due to back-splicing of RNA transcripts, have recently been implicated in Alzheimer’s disease and related tauopathies. circRNAs are regulated by N 6 -methyladenosine (m 6 A) RNA methylation, can serve as “sponges” for proteins and RNAs, and can be translated into protein via a cap-independent mechanism. Mechanisms underlying circRNA dysregulation in tauopathies and causal relationships between circRNA and neurodegeneration are currently unknown. In the current study, we aimed to determine whether pathogenic forms of tau drive circRNA dysregulation and whether such dysregulation causally mediates neurodegeneration. We identify circRNAs that are differentially expressed in the brain of a Drosophila model of tauopathy and in induced pluripotent stem cell (iPSC)-derived neurons carrying a tau mutation associated with autosomal dominant tauopathy. We leverage Drosophila to discover that depletion of circular forms of muscleblind ( circMbl) , a circRNA that is particularly abundant in brains of tau transgenic Drosophila , significantly suppresses tau neurotoxicity, suggesting that tau-induced circMbl elevation is neurotoxic. We detect a general elevation of m 6 A RNA methylation and circRNA methylation in tau transgenic Drosophila and find that tau-induced m 6 A methylation is a mechanistic driver of circMbl formation. Interestingly, we find that circRNA and m 6 A RNA accumulate within nuclear envelope invaginations of tau transgenic Drosophila and in iPSC-derived cerebral organoid models of tauopathy. Taken together, our studies add critical new insight into the mechanisms underlying circRNA dysregulation in tauopathy and identify m 6 A-modified circRNA as a causal factor contributing to neurodegeneration. These findings add to a growing literature implicating pathogenic forms of tau as drivers of altered RNA metabolism.
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Other groups have observed that m6A accumulates in models of tauopathy, as well as in other diseases with intracellular aggregates, including ALS and Huntington's disease.
“Other groups have also observed that m6A accumulates in models of tauopathy, as well as in other diseases with intracellular aggregates, including ALS and Huntington’s disease (McMillan et al., 2023; Nguyen et al., 2023; Atrian et al., 2024).”
From β-amyloid accumulation enhances microtubule associated protein tau pathology in an APPNL-G-F/MAPTP301S mouse model of Alzheimer’s disease (2024) · cites this paper as Atrian et al., 2024
The Results and Discussion report elevated m6A in tauopathy models, including tau-transgenic Drosophila and MAPT-mutant cerebral organoids. The Discussion mentions ALS and Huntington’s disease in connection with muscleblind, but does not report m6A accumulation in either disease. (LLM, conf=0.88)
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- Authors
- Atrian, F., Ramirez, P., De Mange, J., Marquez, M., Gonzalez, E. M., Minaya, M., Karch, C. M., & Frost, B.
- Affiliations
- The University of Texas at San Antonio Health Science Center (US)
- Washington University in St. Louis (US)
- Corresponding author
- Frost, Bess
- Venue
- bioRxiv (Cold Spring Harbor Laboratory)
- Publisher
- openRxiv
- Published
- 2024-01-25
- PMC
- PMC10849734
- OpenAlex
- W4391239563
- Cited by
- 7
- References
- 70
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 1
- Type
- posted content
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- Funders
- Brandeis University
- National Institutes of Health (IA 52242, NIH P40OD018537, P40OD018537)
- National Institute on Aging (R01AG057896, T32AG021890)
- National Institute of Neurological Disorders and Stroke (RF1NS110890)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
- Keywords
- circular RNA, m6A RNA methylation, tauopathy, back-splicing, neurodegeneration, Alzheimer's disease, Drosophila model, iPSC-derived neurons, brain organoids, nuclear envelope invaginations, RNA metabolism
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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