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An atlas of cortical circular RNA expression in Alzheimer disease brains demonstrates clinical and pathological associations
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Parietal cortex RNA-sequencing (RNA-seq) data were generated from individuals with and without Alzheimer disease (AD; n control = 13; n AD = 83) from the Knight Alzheimer Disease Research Center (Knight ADRC). Using this and an independent (Mount Sinai Brain Bank (MSBB)) AD RNA-seq dataset, cortical circular RNA (circRNA) expression was quantified in the context of AD. Significant associations were identified between circRNA expression and AD diagnosis, clinical dementia severity and neuropathological severity. It was demonstrated that most circRNA-AD associations are independent of changes in cognate linear messenger RNA expression or estimated brain cell-type proportions. Evidence was provided for circRNA expression changes occurring early in presymptomatic AD and in autosomal dominant AD. It was also observed that AD-associated circRNAs co-expressed with known AD genes. Finally, potential microRNA-binding sites were identified in AD-associated circRNAs for miRNAs predicted to target AD genes. Together, these results highlight the importance of analyzing non-linear RNAs and support future studies exploring the potential roles of circRNAs in AD pathogenesis.
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“A very recent study has established an association between circRNA expression and AD [620].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [620]
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“Emerging evidence has demonstrated that dysregulated circRNAs exert a crucial role in human diseases, including cancer (14, 15), cardiovascular disease (16), diabetes (17), and Alzheimer’s disease (18).”
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Self-citationExportin 4 depletion leads to nuclear accumulation of a subset of circular RNAs
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InfluentialCircular RNA Encoded Amyloid Beta peptides—A Novel Putative Player in Alzheimer’s Disease
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“They are abundantly enriched in neural tissues, specifically derived from synapse-related genes, and their expression is regulated by synaptic plasticity [5, 6].”
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Inhibition of A1 Astrocytes and Activation of A2 Astrocytes for the Treatment of Spinal Cord Injury
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“A growing number of studies in recent years have discovered that circRNAs play an important role in central nervous system disorders such as stroke [101], Parkinson’s disease [102] and Alzheimer’s disease [103, 104].”
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Self-citationCircular RNAs: Emblematic Players of Neurogenesis and Neurodegeneration
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“circDOCK1 Axonal outgrowth, spine morphogenesis, neuroinflammation Brain, plasma Yes Dedicator of cytokinesis 1 [62,65]”
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“Meta-analysis showed that circHOMER1 was correlated with the clinical severity of AD patients [25].”
BackgroundResultWelden, J. R., Margvelani, G., Maquera, K. A. A., Gudlavalleti, B., Sardón, S. C. M., Campos, A. R., Robil, N., Lee, D. C., Hernandez, A. G., Wang, W., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac1129 · Cited by 43
“When taken together, the expression of 10 of these circRNAs predict clinical dementia in human post-mortem samples (61).”
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The Emerging Role of Circular RNAs in Alzheimer’s Disease and Parkinson’s Disease
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“In addition, circHOMER1 was also significantly related to Braak score and AD status (Dube et al., 2019).”
BackgroundUrdánoz‐Casado, A., de Gordoa, J. S., Robles, M., Acha, B., Roldán, M., Zelaya, M. V., Blanco‐Luquin, I., & Mendióroz, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179205 · Cited by 42
“Our result is concordant with a previous study where a RNAseq experiment was performed in human parietal lobe tissue to identify and quantify circRNAs related to AD [24].”
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Guo, L.-X., Wang, L., You, Z., Yu, C.-Q., Hu, M.-L. M., Zhao, B.-W., & Li, Y. (2024) · Briefings in Bioinformatics · doi:10.1093/bib/bbae020 · Cited by 41
“For instance, Wu et al . investigated the potential miRNA-binding sites in circRNAs associated with Alzheimer’s disease (AD), specifically focusing on miRNAs that are implicated in targeting AD-related genes [9].”
BackgroundCircular RNAs: Promising biomarkers for cancer diagnosis and prognosis
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RNA-sequencing of peripheral blood circular RNAs in Parkinson disease
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“The expression of 2 circRNAs, hsa_circ_0001439 and hsa_circ_0014606, also were changed in Alzheimer disease.([38]) The expression of hsa_circ_0001439 was up-regulated in Brodmann Area 10 (BM10) of patients who suffered from Alzheimer disease.”
BackgroundUncovering the impact of noncoding variants in neurodegenerative brain diseases
Frydas, A., Wauters, E., van der Zee, J., & Broeckhoven, C. V. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.08.010 · Cited by 44
“Cyrano enables accumulation of circRNA Cdr1as, a circRNA that dampens neuronal function in mouse brain [118] and is differentially expressed in AD brain [108].”
BackgroundHatzimanolis, O., Sykes, A. M., & Cristino, A. S. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-02925-1 · Cited by 44
“A meta-analysis has provided an atlas of circRNA expression changes in cortical regions of AD patients, revealing signi fi cant correlations with clinical and neuropathological traits of AD [278].”
Liang, S., Dou, S., Li, W., & Huang, Y. (2020) · Aging · doi:10.18632/aging.103683 · Cited by 40
Ikeda, Y., Morikawa, S., Nakashima, M., Yoshikawa, S., Taniguchi, K., Sawamura, H., Suga, N., Tsuji, A., & Matsuda, S. (2023) · Non-Coding RNA · doi:10.3390/ncrna9020023 · Cited by 41
“Furthermore, circRNAs have been recognized as potential biomarkers in other diseases including amyotrophic lateral sclerosis (ALS), diabetes, and glioblastoma [43].”
BackgroundInfluentialMetabolomic and lipidomic signatures in autosomal dominant and late‐onset Alzheimer's disease brains
Novotny, B. C., Fernández, M. V., Wang, C., Budde, J., Bergmann, K., Eteleeb, A. M., Bradley, J. L., Webster, C., Ebl, C., Norton, J. B., et al. (2022) · Alzheimer s & Dementia · doi:10.1002/alz.12800 · Cited by 42
Self-citationCircular RNAs in human diseases
Wang, Y., Zhang, J., Yang, Y. S. H., Liu, Z., Sun, S., Li, R. F., Zhu, H., Tian, L., Zheng, J., Li, J., et al. (2024) · MedComm · doi:10.1002/mco2.699 · Cited by 41
de Bartolomeis, A., Barone, A., Buonaguro, E. F., Tomasetti, C., Vellucci, L., & Iasevoli, F. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104596 · Cited by 40
Wei, S.-H., Liu, M., Hu, J., & Zhang, C. (2022) · Analytical Chemistry · doi:10.1021/acs.analchem.2c01901 · Cited by 36
Fernández, M. V., Liu, M., Beric, A., Johnson, M., Cetin, A., Patel, M. R., Budde, J., Kohlfeld, P., Bergmann, K., Lowery, J., et al. (2024) · Scientific Data · doi:10.1038/s41597-024-03485-9 · Cited by 41
“GHTO researchers demonstrated for the first time that brain circRNAs are causally associated with AD 12 .”
BackgroundSelf-citationBiomarkers in neurodegenerative diseases: a broad overview
Sathish, S., & Ayyavoo, V. (2024) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2024.00075 · Cited by 39
Li, S., Hu, W., Deng, F., Chen, S., Zhu, P., Wang, M., Chen, X., Wang, Y., Hu, X., Zhao, B., et al. (2021) · DNA and Cell Biology · doi:10.1089/dna.2020.5662 · Cited by 35
“Indeed, multiple previous studies have explored the utility of circRNAs as novel biomarkers of human disease (Huang et al. , 2016; Shang et al. , 2016; Dube et al. , 2019; Wang et al. , 2019).”
Suster, I., & Feng, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136765 · Cited by 39
Nguyen, L. D., Chau, R. K., & Krichevsky, A. M. (2021) · Genes · doi:10.3390/genes12122005 · Cited by 36
New RNA-Based Breakthroughs in Alzheimer’s Disease Diagnosis and Therapeutics
Riscado, M., Baptista, B., & de Sousa, F. P. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13091397 · Cited by 34
“Dube and colleagues have shown that the expression of circRNAs changes before the appearance of significant onset symptoms of AD, demonstrating that circRNAs levels can be correlated with neuropathological and clinical evaluation of AD severity [75].”
BackgroundDysregulation of RNA modification systems in clinical populations with neurocognitive disorders
Knight, H. M., Öz, M. D., & PerezGrovas‐Saltijeral, A. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.385858 · Cited by 33
“As circular RNAs can regulate mRNA through binding to RNA-binding proteins and have been shown to be abnormally expressed in brain diseases (Dube et al., 2019), these observations highlight the potential for a more complex transcriptional regulatory system involving NSUN6 underlying AD and TBI…”
BackgroundLiu, X., Xiong, W., Ye, M., Lu, T., Yuan, K., Chang, S., Han, Y., Wang, Y., Lü, L., & Bao, Y. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01669-0 · Cited by 34
Circular RNAs in Alzheimer’s Disease: A New Perspective of Diagnostic and Therapeutic Targets
Vakili, O., Asili, P., Babaei, Z., Mirahmad, M., Keshavarzmotamed, A., Asemi, Z., & Mafi, A. (2022) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527321666220829164211 · Cited by 34
Regulatory mechanism of circular RNAs in neurodegenerative diseases
Xiao, F., He, Z., Wang, S., Li, J., Fan, X., Yan, T., Yang, M., & Yang, D. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14499 · Cited by 30
Non-Coding RNAs as Sensors of Oxidative Stress in Neurodegenerative Diseases
Gámez‐Valero, A., Guisado-Corcoll, A., Herrero‐Lorenzo, M., Solaguren‐Beascoa, M., & Martí, E. (2020) · Antioxidants · doi:10.3390/antiox9111095 · Cited by 34
“Specifically, ciRS-7 is downregulated in the grey matter of AD patients’ cortex [160,161].”
BackgroundCircular RNAs in the Central Nervous System
Li, M., Wang, W., & Jin, Z. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.629593 · Cited by 31
“levels are significantly correlated with both neuropathological and clinical measures of AD severity (Dube et al., 2019).”
BackgroundCircular RNAs: new biomarkers of chemoresistance in cancer
Wang, J., Zhang, Y., Liu, L., Yang, T., & Song, J. (2021) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0312 · Cited by 31
Self-citationCompeting endogenous RNA network mediated by circ_3205 in SARS-CoV-2 infected cells
Barbagallo, D., Palermo, C. I., Barbagallo, C., Battaglia, R., Caponnetto, A., Spina, V., Ragusa, M., Pietro, C. D., Scalia, G., & Purrello, M. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04119-8 · Cited by 31
“CircRNAs have been found aberrantly expressed in many cancers and degenerative diseases [19, 20] and are associated with several biological processes, both in physiological and pathological conditions [21–24].”
BackgroundChen, H., Eteleeb, A. M., Wang, C., Fernández, M. V., Budde, J., Bergmann, K., Norton, J. B., Wang, F., Ebl, C., Morris, J. C., et al. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01328-5 · Cited by 29
“A previous study [20], demonstrated that expression changes of circRNAs in pre-symptomatic AD, sporadic AD, and ADAD are different and not always related to severity of the disease.”
InfluentialSelf-citationSystematic review and meta-analysis on microRNAs in amyotrophic lateral sclerosis
Liu, H., Lan, S., Shi, X., Fan, F.-C., Liu, Q., Cong, L., & Cheng, Y. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.01.005 · Cited by 31
Vascular endothelial‐cadherin as a marker of endothelial injury in preclinical Alzheimer disease
Tarawneh, R. M., Kasper, R. S., Sanford, J., Phuah, C., Hassenstab, J. J., & Cruchaga, C. (2022) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51685 · Cited by 29
“Post-mortem brain sections were available from a subset of participants (n = 96) with preclinical AD (n = 83)(52,53) and healthy controls (n = 13) and evaluated by singlenucleus RNA (snRNA) sequence analyses for differential VEC brain expression levels.(54,55) Functional pathway analyses for VEC in human brains were p…”
MethodSelf-citationConserved gene signatures shared among MAPT mutations reveal defects in calcium signaling
Minaya, M., Mahali, S. K., Iyer, A. K., Eteleeb, A. M., Martinez, R. J., Huang, G., Budde, J., Temple, S., Nana, A. L., Seeley, W. W., et al. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1051494 · Cited by 29
“To determine whether gene expression changes in iPSC-neuron models reflect a more general impact on neurodegenerative pathways, we examined gene expression profiles isolated from tissue of FTLD-TDP caused by rare mutations theGRN,C9ORF72 expansions, or from sporadic cases (Knight ADRC)(Li et al., 2018; Dube et al., 20…”
BackgroundSelf-citationLi, Y., Wang, F., Teng, P., Ku, L., Chen, L., Feng, Y., & Yao, B. (2022) · Genome biology · doi:10.1186/s13059-022-02621-1 · Cited by 27
“Mounting evidence has also demonstrated that dysregulation of circRNAs is involved in human neurological disorders, including Alzheimer’s disease, Parkinson’s disease, and Schizophrenia [17, 18, 75].”
BackgroundSelf-citationPierouli, K., Papakonstantinou, E., Papageorgiou, L., Diakou, I., Mitsis, Τ., Dragoumani, K., Spandidos, D. A., Bacopoulou, F., Chrousos, G. P., Goulielmos, G. N., et al. (2022) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2022.5208 · Cited by 29
“miR‐520c (42) circHOMER1 (63,84) piR‐34393 (92) NAT‐Rad18 (104,105)”
Expression and function of circular RNAs in the mammalian brain
Xu, K., Zhang, Y., & Li, J. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03780-3 · Cited by 28
Decoding the complexity of circular RNAs in cardiovascular disease
Rai, A. K., Lee, B., Hebbard, C., Uchida, S., & Garikipati, V. N. S. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105766 · Cited by 28
CircSNHG5 Sponges Mir-495-3p and Modulates CITED2 to Protect Cartilage Endplate From Degradation
Zhang, J., Hu, S., Ding, R., Yuan, J., Jia, J., Wu, T., & Cheng, X. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.668715 · Cited by 28
Circular RNAs in atherosclerosis
Huang, X., Zhao, Y., Zhou, H., & Li, Y. (2022) · Clinica Chimica Acta · doi:10.1016/j.cca.2022.03.016 · Cited by 27
Metadata
- Authors
- Dube, U., Del-Aguila, J. L., Li, Z., Budde, J. P., Jiang, S., Hsu, S., Ibanez, L., Fernandez, M. V., Farias, F., Norton, J., Gentsch, J., Wang, F., the Dominantly Inherited Alzheimer Network (DIAN), Allegri, R., Amtashar, F., Benzinger, T., Berman, S., Bodge, C., Brandon, S., Brooks, W., Buck, J., Buckles, V., Chea, S., Chrem, P., Chui, H., Cinco, J., Clifford, J., D’Mello, M., Donahue, T., Douglas, J., Edigo, N., Erekin-Taner, N., Fagan, A., Farlow, M., Farrar, A., Feldman, H., Flynn, G., Fox, N., Franklin, E., Fujii, H., Gant, C., Gardener, S., Ghetti, B., Goate, A., Goldman, J., Gordon, B., Gray, J., Gurney, J., Hassenstab, J., Hirohara, M., Holtzman, D., Hornbeck, R., DiBari, S. H., Ikeuchi, T., Ikonomovic, S., Jerome, G., Jucker, M., Kasuga, K., Kawarabayashi, T., Klunk, W., Koeppe, R., Kuder-Buletta, E., Laske, C., Levin, J., Marcus, D., Martins, R., Mason, N. S., Maue-Dreyfus, D., McDade, E., Montoya, L., Mori, H., Nagamatsu, A., Neimeyer, K., Noble, J., Norton, J., Perrin, R., Raichle, M., Ringman, J., Roh, J. H., Schofield, P., Shimada, H., Shiroto, T., Shoji, M., Sigurdson, W., Sohrabi, H., Sparks, P., Suzuki, K., Swisher, L., Taddei, K., Wang, J., Wang, P., Weiner, M., Wolfsberger, M., Xiong, C., Xu, X., Salloway, S., Masters, C. L., Lee, J.-H., Graff-Radford, N. R., Chhatwal, J. P., Bateman, R. J., Morris, J. C., Karch, C. M., Harari, O., & Cruchaga, C.
- Affiliations
- Washington University in St. Louis (US)
- Fundación para la Lucha contra las Enfermedades Neurológicas de la Infancia (AR)
- University of Pittsburgh (US)
- Indiana University Bloomington (US)
- Mayo Clinic (US)
- University of Southern California (US)
- Edith Cowan University (AU)
- Columbia University (US)
- Hirosaki University (JP)
- German Center for Neurodegenerative Diseases (DE)
- University of Michigan (US)
- Osaka City University (JP)
- The University of Tokyo (JP)
- Asan Medical Center (KR)
- Brigham and Women's Hospital (US)
- University of California, San Francisco (US)
- The University of Melbourne (AU)
- University of Ulsan (KR)
- Harvard University (US)
- Corresponding author
- Cruchaga, Carlos
- ORCID
- Dube, Umber
- Li, Zeran
- Budde, John P
- Jiang, Shan
- Hsu, Simon
- Wang, Fengxian
- Allegri, Ricardo
- Benzinger, Tammie
- Berman, Sarah
- Brooks, William
- D’Mello, Mirelle
- Fagan, Anne
- Feldman, Howard
- Fox, Nick
- Franklin, Erin
- Fujii, Hisako
- Gardener, Samantha
- Ghetti, Bernardino
- Goate, Alison
- Goldman, Jill
- Gordon, Brian
- Gurney, Jenny
- Hassenstab, Jason
- Holtzman, David
- Hornbeck, Russ
- Ikeuchi, Takeshi
- Jucker, Mathias
- Kasuga, Kensaku
- Kawarabayashi, Takeshi
- Klunk, William
- Laske, Christoph
- Levin, Johannes
- Martins, Ralph
- McDade, Eric
- Mori, Hiroshi
- Noble, James
- Perrin, Richard
- Ringman, John
- Roh, Jee Hoon
- Schofield, Peter
- Shoji, Mikio
- Sohrabi, Hamid
- Suzuki, Kazushi
- Taddei, Kevin
- Wang, Jen
- Xiong, Chengjie
- Salloway, Stephen
- Masters, Colin L
- Lee, Jae-Hong
- Chhatwal, Jasmeer P
- Bateman, Randall J
- Morris, John C
- Karch, Celeste M
- Harari, Oscar
- Cruchaga, Carlos
- Venue
- Nature Neuroscience
- Published
- 2019-10-07
- Volume
- 22
- Issue
- 11
- Pages
- 1903-1912
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6858549
- OpenAlex
- W2977553419
- Cited by
- 345
- References
- 63
- Citations by year
- 2026: 22 · 2025: 43 · 2024: 45 · 2023: 53 · 2022: 69 · 2021: 60 · 2020: 48 · 2019: 3
- FWCI
- 14.89
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Murdoch University Research Portal (submittedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Edith Cowan University Research Online (Edith Cowan University) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- DZNE Pub (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute on Aging (RF1AG053303, R01AG058501, RF1AG058501)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- circular RNA, Alzheimer's disease, parietal cortex, autosomal dominant Alzheimer's disease, microRNA binding sites, non-coding RNA, brain transcriptome
- MeSH terms
- RNA, Circular, Alzheimer Disease, Atlases as Topic, Humans, Parietal Lobe, RNA, Messenger, Severity of Illness Index, Case-Control Studies, Sequence Analysis, RNA, Gene Expression Profiling, MicroRNAs
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