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Circular RNA (circRNA) in Alzheimer’s disease (AD)
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GENERAL COMMENTARY article Front. Genet., 31 December 2013 | https://doi.org/10.3389/fgene.2013.00307
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![Figure 1 (A) Detection of circRNA for miRNA-7 (ciRS-7) in sporadic Alzheimer's disease (AD) and age-matched control hippocampal CA1 [control (C) N = 4; AD (A) N = 6]; the single upper ciRS-7 (~1400 nt) band contains ~70 selectively conserved miRNA-7 binding sites as previously described (Hansen et al., 2013); a lower 28S RNA served as an internal loading control; all samples depleted of rRNA were treated with 50 units of RNaseR prior to electrophoresis RNaseR is a processive, Mg++-dependent hydrolytic exoribonuclease that degrades linear but not circular RNA; see Hansen et al. (2013); predicted circular transcripts consistently resisted an RNaseR challenge; 30 ug total AD and control hippocampal CA1 RNA was separated on agarose gels, transferred and probed with biotinylated or radiolabeled miRNA-7 probes as previously described (Colangelo et al., 2002; Hansen et al., 2013); detection was performed using a nonisotopic BrightStar BioDetect Kit (Ambion, Austin, TX; detection limit ~100 fg) or by standard autoradiography (Lukiw et al., 1992); (B) AD ciRS-7 is significantly reduced to about 0.18-fold of control (con) in a study of 20 control and AD (AD) hippocampal CA1 samples; this implicates loss of miRNA-7 sponge effects, an ambient up-regulation of miRNA-7 (as is observed), and down-regulation of a family of miRNA-7-sensitive mRNAs in the sporadic AD brain; other circRNAs may be involved; there were no significant differences between age for control or AD tissues [mean ± 1 standard deviation (SD) = 75.4 ± 8.3 year vs. 77.5 ± 7.6 year]; all AD cases were for moderate-to-advanced stages of AD; all post-mortem intervals were 2.1 h or less (Colangelo et al., 2002); there were no significant differences in age, ApoE allele status, RNA quality (all RIN values were 8.1–9.0) or yield between the control or AD groups (p > 0.05, ANOVA); a dashed horizontal line at 1.0 indicates homeostatic (control) ciRS-7 levels for ease of comparison; *p < 0.001 (ANOVA).](/paper-figures/a4706fbfe0d3497e8b376957eb291493/circular-rna-circrna-in-alzheimers-disease-ad-figure-1.jpg)
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“In addition, dysregulation of ciRS-7 has been found in zebrafish with an impaired midbrain [71] and in the hippocampus of AD patients [45].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [45]
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Cites
Circular RNAs are a large class of animal RNAs with regulatory potency
Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S. D., Gregersen, L. H., Munschauer, M., et al. (2013) · Nature · doi:10.1038/nature11928 · Cited by 7,990 · cited 1×
“Intrinsically resistant to exonucleolytic RNA decay, circRNAs appear to be enriched in mammalian brain tissues (Hansen et al., 2013; Memczak et al., 2013).”
BackgroundNatural RNA circles function as efficient microRNA sponges
Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., & Kjems, J. (2013) · Nature · doi:10.1038/nature11993 · Cited by 7,985
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“Recently characterized, traditional methods of RNA detection and analysis requiring a free 5′ or 3′ ribonucleotide terminus may have significantly underestimated circRNA abundance and significance in eukaryotic cells (Salzman et al., 2012; Wilusz and Sharp, 2013; unpublished observations).”
Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., et al. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-14103 · Cited by 943 · cited 1×
“…or AD groups (p > 0.05, ANOVA); a dashed horizontal line at 1.0 indicates homeostatic (control) ciRS-7 levels for ease of comparison; ∗p < 0.001 (ANOVA). contribute to the down-regulation of selective miRNA-7-sensitive messenger RNA (mRNA) targets (Cogswell et al., 2008; unpublished observations).”
BackgroundInfluentialA Circuitous Route to Noncoding RNA
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“Recently characterized, traditional methods of RNA detection and analysis requiring a free 5′ or 3′ ribonucleotide terminus may have significantly underestimated circRNA abundance and significance in eukaryotic cells (Salzman et al., 2012; Wilusz and Sharp, 2013; unpublished observations).”
Colangelo, V., Schurr, J., Ball, M. J., Pelaez, R. P., Bazan, N. G., & Lukiw, W. J. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10351 · Cited by 517
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“…systems” and ambient up-regulation of specific inducible miRNAs may help explain the widely observed, generalized and progressive down-regulation of gene expression that is characteristic of the sporadic AD brain (Loring et al., 2001; Colangelo et al., 2002; Ginsberg et al., 2012; Lukiw, 2013).”
BackgroundInfluentialDeconstruction for Reconstruction: The Role of Proteolysis in Neural Plasticity and Disease
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“, 2013); detection was performed using a nonisotopic BrightStar BioDetect Kit (Ambion, Austin, TX; detection limit ∼100 fg) or by standard autoradiography (Lukiw et al., 1992); (B) AD ciRS-7 is significantly reduced to about 0.”
MethodInfluentialMicroRNA in schizophrenia: Genetic and expression analysis of miR-130b (22q11)
Burmistrova, O., Goltsov, A. Y., Abramova, L. I., Каледа, В. Г., Александровна, О. В., & Rogaev, E. I. (2007) · Biochemistry (Moscow) · doi:10.1134/s0006297907050161 · Cited by 101 · cited 1×
“…but are also associated with a circRNA for miRNA-7 (ciRS-7), in the same tissues; ciRS-7 contains multiple, tandem anti-miRNA-7 sequences (Burmistrova et al., 2007; Hansen et al., 2013; Lukiw et al., 2013). ciRS-7 thereby acts as a kind of endogenous, competing, anti-complementary miRNA…”
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Items 101–200 of 647
Genome-Wide Identification of Circular RNAs in Arabidopsis thaliana
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“Recent research has suggested that circRNAs are widely expressed in a complex tissue-, cell-type- or developmental-stagespecific manner, and their sequences and expression patterns are often conserved (Salzman et al., 2012; Jeck et al., 2013; Memczak et al., 2013; Zhang et al., 2013, 2014).”
BackgroundMethodInfluentialThe mechanism and function of circular RNAs in human diseases
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“…expression pathways and patterns whose abundances are highly sensitive to alterations in the biochemical, neurochemical, neuropathological, and/or cellular environment (Alexandrov et al., 2012; Lukiw, 2013a,b; Kumar and Reddy, 2019; Kumar et al., 2019; Kumar and Reddy, 2020; Lukiw and Pogue, 2020).”
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“For example, the circRNA ciRS-7 contains multiple tandem miRNA-7 binding sites, thereby acting as an endogenous miRNA ‘sponge’ to adsorb, and hence quench normal miRNA-7 function (27).”
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“They are reported to function as miRNA sponges (Hansen et al., 2013) or RNAbinding proteins (RBP) sponges (Ashwal-Fluss et al., 2014) and are ideal biomarkers (Lukiw, 2013).”
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Using plasma circRNA_002453 as a novel biomarker in the diagnosis of lupus nephritis
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“For instance, ciRS-7 serves as an endogenous sponge for miR-107 and quenches the normal function of miR-107, thereby alters levels of proteins such as ubiquitin protein ligase A (UBE2A), which is essential for clearance of amyloid peptides in AD [18].”
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“Furthermore, ciRS-7 deficiency leads to increased miR-7 availability which may lead to down-regulation of targets such as ubiquitin protein ligase A (UBE2A) which has been implicated in AD pathogenesis (Hansen et al., 2013a, b; Bingol and Sheng, 2011; Lukiw, 2013).”
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“may be abnormally regulated under certain disease conditions, such as colorectal cancer(28) or Alzheimer’s disease.(29) In addition, circRNA can have special functions, such as tissue-specific circRNAs involved in fetal development(30) and accumulating with age in the brain of Drosophila.”
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Circular RNAs in Muscle Function and Disease
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“Neurological disease Alzheimer’s disease CDR1as Downregulated Deficiency of CDR1as contributes to AD through upregulation of miR-7 (14)”
BackgroundCircular RNAs: New Epigenetic Signatures in Viral Infections
Nahand, J. S., Jamshidi, S., Hamblin, M. R., Mahjoubin‐Tehran, M., Vosough, M., Jamali, M., Khatami, A., Moghoofei, M., Baghi, H. B., & Mirzaei, H. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01853 · Cited by 89
“…miRNA sponges may be associated with human disease, such as Alzheimer’s, Hirschsprung’s, diabetes, osteoarthritis, and several types of cancer (Lukiw, 2013; Wang et al., 2016; Zhao et al., 2016; Han et al., 2017; Peng et al., 2017; Zhao et al., 2017; Zhou and Yu, 2017; Zhou Z.-B. et al.,…”
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Abu, N., & Jamal, R. A. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00355 · Cited by 86
circDeep: deep learning approach for circular RNA classification from other long non-coding RNA
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“Non-coding RNA (ncRNA) (Mattick and Makunin, 2006) is functional RNA that is transcribed from DNA, but is incapable of being translated into protein. ncRNAs can be categorized into two groups based on length.”
BackgroundCharacterization of circular RNA s landscape in multiple system atrophy brain
Chen, B. J., Mills, J. D., Takenaka, K., Bliim, N., Halliday, G. M., & Janitz, M. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13752 · Cited by 84
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“They are reported to function as miRNA sponges [76] or RBP sponges [77] and are considered ideal biomarkers [78].”
BackgroundIdentification of differentially expressed circular RNAs in human colorectal cancer
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“Many researches indicated that the mutation and dysregulation of circRNAs may contribute to the progression of various diseases [7], [8], and circRNAs have been found to act as tumor oncogenes or suppressors in many diseases [6], such as cancers [9], neurodegeneration, and cerebrovascular diseases [10].”
BackgroundPresent Scenario of Circular RNAs (circRNAs) in Plants
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“…processes, such as insulin biosynthesis and secretion (Xu et al., 2015), neurological diseases (Satoh and Yamamura, 2004; Junn et al., 2009; Lukiw, 2013), degenerative diseases (Ashwal-Fluss et al., 2014; Liu Q. et al., 2016), cardiovascular diseases (Burd et al., 2010; Wang K. et al.,…”
BackgroundCircular RNAs—The Road Less Traveled
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Emerging Role of Circular RNAs in Cancer
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“Studies to date have reported that circRNAs are dysregulated in the pathophysiologic processes of several diseases, including cardiovascular disease (17), neurodegenerative disease such as Alzheimer’s disease (18), metabolic disorder (19), diseases caused by viral infection (20), and cancer,”
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“Studies reported the association of ciRS-7 with Alzheimer’s disease (14), the expression of cANRIL with increased risk of atherosclerotic vascular disease (15), and the downregulation of hsa-circ-002059 with gastric cancer tissues (16, 17).”
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BackgroundThe insights of Let‐7 miRNAs in oncogenesis and stem cell potency
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“CircRNA for miRNA-7 (ciRS-7) acts as an anti-complementary miRNA ‘sponge’ to adsorb and quench miRNA-7, and deficits in ciRS-7 were expected to increase ambient miRNA-7 [64].”
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“Furthermore, the most expressed and studied circRNA, CDR1-AS, was found reduced in hippocampal CA1 samples from sporadic AD patients compared to controls (Lukiw, 2013).”
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“In addition, expression of ciRS-7 is significantly reduced in hippocampus of AD patients (Lukiw, 2013), suggesting an abnormal miRNA-circRNA system may underline the disease mechanism of AD (Figure 2).”
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“For example, the deletion of cirs-7 in the brain tissue can lead to the up-regulation of miR-7 and the down regulation of multiple mRNA targets related to Alzheimer’s disease [17], [18].”
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“In addition, Lukiw (2013) revealed that circRNA ciRS-7 also acts as a ceRNA to absorb miRNA.”
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Roles of Non-Coding RNA in Alzheimer’s Disease Pathophysiology
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Novel RNA Modifications in the Nervous System: Form and Function
Satterlee, J. S., Basanta‐Sanchez, M., Blanco, S., Li, J. B., Meyer, K. D., Pollock, J. D., Sadri‐Vakili, G., & Rybak‐Wolf, A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3236-14.2014 · Cited by 63
The epigenetic dimension of Alzheimer's disease: causal, consequence, or curiosity?
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Circular RNAs: Novel Promising Biomarkers in Ocular Diseases
Guo, N., Liu, X., Pant, O. P., Zhou, D., Hao, J., & Lu, C. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.29750 · Cited by 64
“Abnormally expressed circRNAs were found in numerous human diseases including, malignancy, vascular, inflammatory and nervous diseases [9-11].”
BackgroundAtCircDB: a tissue-specific database forArabidopsiscircular RNAs
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Circular RNAs in Urine of Kidney Transplant Patients with Acute T Cell-Mediated Allograft Rejection
Kölling, M., Haddad, G., Wegmann, U. A., Kistler, A. D., Bosakova, A., Seeger, H., Hübel, K., Haller, H. G., Mueller, T., Wuthrich, R. P., et al. (2019) · Clinical Chemistry · doi:10.1373/clinchem.2019.305854 · Cited by 61
Non-coding RNAs: Emerging from the discovery to therapeutic applications
Baptista, B., Riscado, M., Queiroz, J. A., Pichon, C., & de Sousa, F. P. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114469 · Cited by 64
Fusion of multiple heterogeneous networks for predicting circRNA-disease associations
Deng, L., Zhang, W., Shi, Y., & Tang, Y. (2019) · Scientific Reports · doi:10.1038/s41598-019-45954-x · Cited by 62
Liu, L., Chen, X., Chen, Y., & Zhang, K. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.601965 · Cited by 61
“CiRS-7 contains multiple, tandem anti-miRNA-7 sequences that act as endogenous, anticomplementary miRNA “sponges” to adsorb and quench normal miRNA-7 functions (Lukiw, 2013; Akhter, 2018).”
BackgroundInfluentialCircular RNA: a new star in neurological diseases
Li, T., Jia, Y., Wang, Q., Shao, X.-Q., & Lv, R. (2016) · International Journal of Neuroscience · doi:10.1080/00207454.2016.1236382 · Cited by 63
“Lukiw stated that it had a high likelihood of down-regulating AD-relevant targets, such as the ubiquitin protein ligase A (UPLA), which is essential in the clearance of amyloid peptides in AD [37,51,52].”
BackgroundCircRNAs: A new perspective of biomarkers in the nervous system
Ma, Y., Liu, Y., & Jiang, Z. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110251 · Cited by 61
Circular RNA: New Regulatory Molecules
Belousova, E. A., Филипенко, М. Л., & Кушлинский, Н. Е. (2018) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-018-4084-z · Cited by 61
Zhang, X., Lu, J., Zhang, Q., Luo, Q., & Liu, B. (2021) · Biological Research · doi:10.1186/s40659-021-00335-5 · Cited by 61
Biological roles and therapeutic potential of circular RNAs in osteoarthritis
Mao, X., Cao, Y., Guo, Z., Wang, L., & Xiang, C. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.04.006 · Cited by 61
Circular RNAs: New layer of complexity evading breast cancer heterogeneity
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Cieślik, M., Czapski, G. A., Wójtowicz, S., Wieczorek, I., Wencel, P. L., Strosznajder, R. P., Jaber, V. R., Lukiw, W. J., & Strosznajder, J. B. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-01819-y · Cited by 61
“circuit development, maturation and function [77, 78].”
Circular RNAs: The Brain Transcriptome Comes Full Circle
Gokoolparsadh, A., Loy, C. T., Halliday, G. M., & Voineagu, I. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.07.007 · Cited by 61
Wang, Z., Wen, Z.-J., Xu, H.-M., Zhang, Y., & Zhang, Y.-F. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1004221 · Cited by 61
“…can function as miRNA sponges, protein inhibition, and regulators of splicing and transcription; and they also can bind RBP, as well as translate into peptides and proteins, which contribute to neurodegenerative diseases up to a point (Lukiw, 2013; Fanale et al., 2018; Welden et al., 2018).”
BackgroundInfluentialChanges in circular RNA expression patterns during human foetal brain development
Chen, B. J., Huang, S., & Janitz, M. (2018) · Genomics · doi:10.1016/j.ygeno.2018.04.015 · Cited by 60
Circular RNA expression and function in the brain
Sekar, S., & Liang, W. S. (2019) · Non-coding RNA Research · doi:10.1016/j.ncrna.2019.01.001 · Cited by 64
“Furthermore, the expression of CDR1as was reduced in hippocampal CA1 samples from sporadic AD patients compared to controls [85].”
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“While their functions remain largely elusive, emerging data suggest that circRNAs could regulate gene expression [125, 126] and are pathologically involved in the progression of some diseases, such as cancer [127] and neurological disorders [128].”
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Methods for analysis of circular RNAs
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“Accordingly, circRNAs have been implicated in several pathologies, including cancer, Alzheimer's disease, Parkinson's disease, cardiovascular disease, and atherosclerosis (Floris, Zhang, Follesa, & Sun, 2017; Holdt et al., 2016; Lukiw, 2013; D. Yang, Yang, & Yang, 2018; Zhao & Shen, 2017).”
Liu, W., Feng, R., Li, X., Li, D., & Zhai, W. (2019) · Aging · doi:10.18632/aging.102405 · Cited by 59
Cai, Y., & Wan, J. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00370 · Cited by 59
“Furthermore, certain circRNAs (such as ciRS-7) contain numerous binding sites for miRNAs (such as miR-7), which indicates the existence of potent endogenous RNA sponges (Lukiw, 2013; Jens and Rajewsky, 2015).”
BackgroundInferring Potential CircRNA–Disease Associations via Deep Autoencoder-Based Classification
Deepthi, K., & Jereesh, A. S. (2020) · Molecular Diagnosis & Therapy · doi:10.1007/s40291-020-00499-y · Cited by 58
Construction and analysis of circular RNA molecular regulatory networks in liver cancer
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“For example, the circular RNA ciRS-7/ CRD1as contains multiple, tandem miR-7 binding sites, and, thereby, acts as an endogenous miRNA “sponge” to adsorb, and hence quench, normal miR-7 functions.(27) It has been demonstrated that miR-7 involves numerous pathways, and that miR-7 could directly down-regulate several onc…”
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Recent insights into the roles of circular RNAs in human brain development and neurologic diseases
Najafi, S., Zarch, S. M. A., Majidpoor, J., Pordel, S., Aghamiri, S., Rasul, M. F., Asemani, Y., Vakili, O., Mohammadi, V., Movahedpour, A., et al. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.11.166 · Cited by 56
Microarray expression profile analysis of circular RNAs in pancreatic cancer
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“Recently, some studies have demonstrated that circRNAs can play very crucial role in biological process and progression of disease via miRNA sponge (20,21).”
Current status and potential role of circular RNAs in neurological disorders
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Metadata
- Authors
- Lukiw, W. J.
- Affiliations
- Louisiana State University (US)
- Corresponding author
- Lukiw, Walter J.
- ORCID
- Lukiw, Walter J.
- Venue
- Frontiers in Genetics
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 4
- Pages
- 307-307
- ISSN
- 1664-8021 (ISSN-L)
- PMC
- PMC3875874
- OpenAlex
- W2095799789
- Cited by
- 636
- References
- 14
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 25 · 2023: 48 · 2022: 57 · 2021: 85 · 2020: 103 · 2019: 88 · 2018: 89 · 2017: 66 · 2016: 32 · 2015: 14 · 2014: 6
- FWCI
- 7.76
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Instytut Medycyny Doswiadczalnej i Klinicznej im. M. Mossakowskiego, Polskiej Akademii Nauk
- National Institute on Aging (AG038834, NIA AG038834, R01AG038834)
- National Eye Institute (NEI-EY-006311, R01EY006311, EY-006311)
- 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, non-coding RNA, RNA circularization
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