Progress in circRNA-Targeted Therapy in Experimental Parkinson’s Disease
Abstract
:1. Introduction
2. Biogenesis and Functions of circRNAs
3. Function of circRNAs in the Cellular Metabolism
4. CircRNAs Regulating Gene Expression—Interaction with DNA
4.1. Direct Regulation of Gene Expression
4.2. Regulation of DNA Methylation
4.3. Retrotransposon
5. CircRNAs Regulating Gene Expression—Interaction with RNA
5.1. Regulation of Gene Expression
5.2. Regulation of mRNA Stability
5.3. Sponges of miRNAs
6. CircRNAs Regulating Cellular Metabolism—Interaction with Protein
6.1. Protein Translation
6.2. Sponges and Proteins
7. CircRNAs Relationship between Alpha-Synuclein and microRNAs in the Parkinson’s Disease
8. CircRNA in Neuroinflammation
9. Scientific Methodologies to Target circRNAs
9.1. Strategies to Downregulate circRNAs
9.1.1. Synthetic Small-Interfering RNAs (siRNAs)
9.1.2. Short-Hairpin RNAi Expressing Vectors
9.1.3. Antisense Oligonucleotides
9.1.4. CRISPR/Cas Systems for circRNA Knockout or Knockdown
9.2. Overexpression of circRNAs by Nonviral and Viral Vectors
9.3. Investigating the Role of circRNAs in Models of Neurodegenerative Diseases: siRNAs and Expression Vectors in Selected Studies
9.3.1. Paving the Path for circRNA Development: Drawing on the Success of siRNAs in Reaching the Market
9.3.2. Are circRNAs Gaining Traction in the Pharmaceutical Market?
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sanger, H.L.; Klotz, G.; Riesner, D.; Gross, H.J.; Kleinschmidt, A.K. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc. Natl. Acad. Sci. USA 1976, 73, 3852–3856. [Google Scholar] [CrossRef]
- Danan, M.; Schwartz, S.; Edelheit, S.; Sorek, R. Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res. 2012, 40, 3131–3142. [Google Scholar] [CrossRef]
- Lu, T.; Cui, L.; Zhou, Y.; Zhu, C.; Fan, D.; Gong, H.; Zhao, Q.; Zhou, C.; Zhao, Y.; Lu, D.; et al. Transcriptome-wide investigation of circular RNAs in rice. RNA 2015, 21, 2076–2087. [Google Scholar] [CrossRef] [Green Version]
- Salzman, J.; Gawad, C.; Wang, P.L.; Lacayo, N.; Brown, P.O. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 2012, 7, e30733. [Google Scholar] [CrossRef] [Green Version]
- Memczak, S.; Jens, M.; Elefsinioti, A.; Torti, F.; Krueger, J.; Rybak, A.; Maier, L.; Mackowiak, S.D.; Gregersen, L.H.; Munschauer, M.; et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495, 333–338. [Google Scholar] [CrossRef]
- Kristensen, L.S.; Andersen, M.S.; Stagsted, L.V.W.; Ebbesen, K.K.; Hansen, T.B.; Kjems, J. The biogenesis, biology and characterization of circular RNAs. Nat. Rev. Genet. 2019, 20, 675–691. [Google Scholar] [CrossRef] [PubMed]
- Ashwal-Fluss, R.; Meyer, M.; Pamudurti, N.R.; Ivanov, A.; Bartok, O.; Hanan, M.; Evantal, N.; Memczak, S.; Rajewsky, N.; Kadener, S. circRNA biogenesis competes with pre-mRNA splicing. Mol. Cell 2014, 56, 55–66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Z.; Huang, C.; Bao, C.; Chen, L.; Lin, M.; Wang, X.; Zhong, G.; Yu, B.; Hu, W.; Dai, L.; et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 2015, 22, 256–264. [Google Scholar] [CrossRef]
- Jeck, W.R.; Sorrentino, J.A.; Wang, K.; Slevin, M.K.; Burd, C.E.; Liu, J.; Marzluff, W.F.; Sharpless, N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013, 19, 141–157. [Google Scholar] [CrossRef] [Green Version]
- Schwanhausser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control. Nature 2011, 473, 337–342. [Google Scholar] [CrossRef] [Green Version]
- Rybak-Wolf, A.; Stottmeister, C.; Glazar, P.; Jens, M.; Pino, N.; Giusti, S.; Hanan, M.; Behm, M.; Bartok, O.; Ashwal-Fluss, R.; et al. Circular RNAs in the Mammalian Brain Are Highly Abundant, Conserved, and Dynamically Expressed. Mol. Cell 2015, 58, 870–885. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haddad, G.; Lorenzen, J.M. Biogenesis and Function of Circular RNAs in Health and in Disease. Front. Pharmacol. 2019, 10, 428. [Google Scholar] [CrossRef]
- Zhou, W.Y.; Cai, Z.R.; Liu, J.; Wang, D.S.; Ju, H.Q.; Xu, R.H. Circular RNA: Metabolism, functions and interactions with proteins. Mol. Cancer 2020, 19, 172. [Google Scholar] [CrossRef] [PubMed]
- You, X.; Vlatkovic, I.; Babic, A.; Will, T.; Epstein, I.; Tushev, G.; Akbalik, G.; Wang, M.; Glock, C.; Quedenau, C.; et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat. Neurosci. 2015, 18, 603–610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xin, R.; Gao, Y.; Gao, Y.; Wang, R.; Kadash-Edmondson, K.E.; Liu, B.; Wang, Y.; Lin, L.; Xing, Y. isoCirc catalogs full-length circular RNA isoforms in human transcriptomes. Nat. Commun. 2021, 12, 266. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Sun, C.; Cui, H.; Sun, J.; Zhou, P. Role of circRNAs in neurodevelopment and neurodegenerative diseases. J. Mol. Neurosci. 2021, 71, 1743–1751. [Google Scholar] [CrossRef]
- D’Ambra, E.; Capauto, D.; Morlando, M. Exploring the Regulatory Role of Circular RNAs in Neurodegenerative Disorders. Int. J. Mol. Sci. 2019, 20, 5477. [Google Scholar] [CrossRef] [Green Version]
- Zhang, M.; Bian, Z. The Emerging Role of Circular RNAs in Alzheimer’s Disease and Parkinson’s Disease. Front. Aging Neurosci. 2021, 13, 691512. [Google Scholar] [CrossRef]
- Lu, S.; Yang, X.; Wang, C.; Chen, S.; Lu, S.; Yan, W.; Xiong, K.; Liu, F.; Yan, J. Current status and potential role of circular RNAs in neurological disorders. J. Neurochem. 2019, 150, 237–248. [Google Scholar] [CrossRef] [Green Version]
- Emamzadeh, F.N.; Surguchov, A. Parkinson’s Disease: Biomarkers, Treatment, and Risk Factors. Front. Neurosci. 2018, 12, 612. [Google Scholar] [CrossRef] [Green Version]
- Caba, L.; Florea, L.; Gug, C.; Dimitriu, D.C.; Gorduza, E.V. Circular RNA-Is the Circle Perfect? Biomolecules 2021, 11, 1755. [Google Scholar] [CrossRef]
- Eger, N.; Schoppe, L.; Schuster, S.; Laufs, U.; Boeckel, J.N. Circular RNA Splicing. Adv. Exp. Med. Biol. 2018, 1087, 41–52. [Google Scholar] [CrossRef]
- Gao, Y.; Wang, J.; Zhao, F. CIRI: An efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol. 2015, 16, 4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Conn, S.J.; Pillman, K.A.; Toubia, J.; Conn, V.M.; Salmanidis, M.; Phillips, C.A.; Roslan, S.; Schreiber, A.W.; Gregory, P.A.; Goodall, G.J. The RNA binding protein quaking regulates formation of circRNAs. Cell 2015, 160, 1125–1134. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Du, L.; Bai, Y.; Han, B.; He, C.; Gong, L.; Huang, R.; Shen, L.; Chao, J.; Liu, P.; et al. CircDYM ameliorates depressive-like behavior by targeting miR-9 to regulate microglial activation via HSP90 ubiquitination. Mol. Psychiatry 2020, 25, 1175–1190. [Google Scholar] [CrossRef]
- He, A.T.; Liu, J.; Li, F.; Yang, B.B. Targeting circular RNAs as a therapeutic approach: Current strategies and challenges. Signal Transduct. Target. Ther. 2021, 6, 185. [Google Scholar] [CrossRef]
- Du, W.W.; Yang, W.; Liu, E.; Yang, Z.; Dhaliwal, P.; Yang, B.B. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 2016, 44, 2846–2858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patop, I.L.; Wust, S.; Kadener, S. Past, present, and future of circRNAs. EMBO J. 2019, 38, e100836. [Google Scholar] [CrossRef]
- Hsu, M.T.; Coca-Prados, M. Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature 1979, 280, 339–340. [Google Scholar] [CrossRef]
- Cortes-Lopez, M.; Miura, P. Emerging Functions of Circular RNAs. Yale J. Biol. Med. 2016, 89, 527–537. [Google Scholar]
- Zhou, L.Y.; Zhai, M.; Huang, Y.; Xu, S.; An, T.; Wang, Y.H.; Zhang, R.C.; Liu, C.Y.; Dong, Y.H.; Wang, M.; et al. The circular RNA ACR attenuates myocardial ischemia/reperfusion injury by suppressing autophagy via modulation of the Pink1/ FAM65B pathway. Cell Death Differ. 2019, 26, 1299–1315. [Google Scholar] [CrossRef] [PubMed]
- Dong, R.; Zhang, X.O.; Zhang, Y.; Ma, X.K.; Chen, L.L.; Yang, L. CircRNA-derived pseudogenes. Cell Res. 2016, 26, 747–750. [Google Scholar] [CrossRef] [PubMed]
- Sinha, T.; Panigrahi, C.; Das, D.; Chandra Panda, A. Circular RNA translation, a path to hidden proteome. Wiley Interdiscip. Rev. RNA 2022, 13, e1685. [Google Scholar] [CrossRef] [PubMed]
- Hansen, T.B.; Jensen, T.I.; Clausen, B.H.; Bramsen, J.B.; Finsen, B.; Damgaard, C.K.; Kjems, J. Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495, 384–388. [Google Scholar] [CrossRef] [PubMed]
- Ng, W.L.; Marinov, G.K.; Liau, E.S.; Lam, Y.L.; Lim, Y.Y.; Ea, C.K. Inducible RasGEF1B circular RNA is a positive regulator of ICAM-1 in the TLR4/LPS pathway. RNA Biol. 2016, 13, 861–871. [Google Scholar] [CrossRef] [Green Version]
- Garikipati, V.N.S.; Verma, S.K.; Cheng, Z.; Liang, D.; Truongcao, M.M.; Cimini, M.; Yue, Y.; Huang, G.; Wang, C.; Benedict, C.; et al. Circular RNA CircFndc3b modulates cardiac repair after myocardial infarction via FUS/VEGF-A axis. Nat. Commun. 2019, 10, 4317. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Han, Y.; Wang, S.; Wu, X.; Cao, J.; Sun, T. Circular RNAs: Biogenesis, Biological Functions, and Roles in Myocardial Infarction. Int. J. Mol. Sci. 2023, 24, 4233. [Google Scholar] [CrossRef]
- Welden, J.R.; Stamm, S. Pre-mRNA structures forming circular RNAs. Biochim. Biophys. Acta Gene Regul. Mech. 2019, 1862, 194410. [Google Scholar] [CrossRef]
- Kos, A.; Dijkema, R.; Arnberg, A.C.; van der Meide, P.H.; Schellekens, H. The hepatitis delta (delta) virus possesses a circular RNA. Nature 1986, 323, 558–560. [Google Scholar] [CrossRef] [PubMed]
- Holdt, L.M.; Kohlmaier, A.; Teupser, D. Circular RNAs as Therapeutic Agents and Targets. Front. Physiol. 2018, 9, 1262. [Google Scholar] [CrossRef] [Green Version]
- Ulshofer, C.J.; Pfafenrot, C.; Bindereif, A.; Schneider, T. Methods to study circRNA-protein interactions. Methods 2021, 196, 36–46. [Google Scholar] [CrossRef] [PubMed]
- Aufiero, S.; Reckman, Y.J.; Pinto, Y.M.; Creemers, E.E. Circular RNAs open a new chapter in cardiovascular biology. Nat. Rev. Cardiol. 2019, 16, 503–514. [Google Scholar] [CrossRef]
- Surguchov, A.; Surguchev, A. Synucleins: New Data on Misfolding, Aggregation and Role in Diseases. Biomedicines 2022, 10, 3241. [Google Scholar] [CrossRef] [PubMed]
- Meade, R.M.; Fairlie, D.P.; Mason, J.M. Alpha-synuclein structure and Parkinson’s disease-lessons and emerging principles. Mol. Neurodegener. 2019, 14, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. Alpha-synuclein in Lewy bodies. Nature 1997, 388, 839–840. [Google Scholar] [CrossRef]
- Titze-de-Almeida, R.; Titze-de-Almeida, S.S. miR-7 Replacement Therapy in Parkinson’s Disease. Curr. Gene Ther. 2018, 18, 143–153. [Google Scholar] [CrossRef] [PubMed]
- Poewe, W.; Seppi, K.; Tanner, C.M.; Halliday, G.M.; Brundin, P.; Volkmann, J.; Schrag, A.E.; Lang, A.E. Parkinson disease. Nat. Rev. Dis. Prim. 2017, 3, 17013. [Google Scholar] [CrossRef]
- Obeso, J.A.; Stamelou, M.; Goetz, C.G.; Poewe, W.; Lang, A.E.; Weintraub, D.; Burn, D.; Halliday, G.M.; Bezard, E.; Przedborski, S.; et al. Past, present, and future of Parkinson’s disease: A special essay on the 200th Anniversary of the Shaking Palsy. Mov. Disord. 2017, 32, 1264–1310. [Google Scholar] [CrossRef]
- Sang, Q.; Liu, X.; Wang, L.; Qi, L.; Sun, W.; Wang, W.; Sun, Y.; Zhang, H. CircSNCA downregulation by pramipexole treatment mediates cell apoptosis and autophagy in Parkinson’s disease by targeting miR-7. Aging 2018, 10, 1281–1293. [Google Scholar] [CrossRef] [PubMed]
- Kleaveland, B.; Shi, C.Y.; Stefano, J.; Bartel, D.P. A Network of Noncoding Regulatory RNAs Acts in the Mammalian Brain. Cell 2018, 174, 350–362.e17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piwecka, M.; Glazar, P.; Hernandez-Miranda, L.R.; Memczak, S.; Wolf, S.A.; Rybak-Wolf, A.; Filipchyk, A.; Klironomos, F.; Cerda Jara, C.A.; Fenske, P.; et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 2017, 357, eaam8526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeng, K.; Chen, X.; Xu, M.; Liu, X.; Hu, X.; Xu, T.; Sun, H.; Pan, Y.; He, B.; Wang, S. CircHIPK3 promotes colorectal cancer growth and metastasis by sponging miR-7. Cell Death Dis. 2018, 9, 417. [Google Scholar] [CrossRef] [Green Version]
- Kumar, L.; Shamsuzzama; Jadiya, P.; Haque, R.; Shukla, S.; Nazir, A. Functional Characterization of Novel Circular RNA Molecule, circzip-2 and Its Synthesizing Gene zip-2 in C. elegans Model of Parkinson’s Disease. Mol. Neurobiol. 2018, 55, 6914–6926. [Google Scholar] [CrossRef]
- Hanan, M.; Simchovitz, A.; Yayon, N.; Vaknine, S.; Cohen-Fultheim, R.; Karmon, M.; Madrer, N.; Rohrlich, T.M.; Maman, M.; Bennett, E.R.; et al. A Parkinson’s disease CircRNAs Resource reveals a link between circSLC8A1 and oxidative stress. EMBO Mol. Med. 2020, 12, e13551. [Google Scholar] [CrossRef]
- Jia, E.; Zhou, Y.; Liu, Z.; Wang, L.; Ouyang, T.; Pan, M.; Bai, Y.; Ge, Q. Transcriptomic Profiling of Circular RNA in Different Brain Regions of Parkinson’s Disease in a Mouse Model. Int. J. Mol. Sci. 2020, 21, 3006. [Google Scholar] [CrossRef] [Green Version]
- Curry-Hyde, A.; Gray, L.G.; Chen, B.J.; Ueberham, U.; Arendt, T.; Janitz, M. Cell type-specific circular RNA expression in human glial cells. Genomics 2020, 112, 5265–5274. [Google Scholar] [CrossRef]
- Wang, H.; Li, Z.; Gao, J.; Liao, Q. Circular RNA circPTK2 regulates oxygen-glucose deprivation-activated microglia-induced hippocampal neuronal apoptosis via miR-29b-SOCS-1-JAK2/STAT3-IL-1beta signaling. Int. J. Biol. Macromol. 2019, 129, 488–496. [Google Scholar] [CrossRef]
- Bai, X.; Tang, Y.; Yu, M.; Wu, L.; Liu, F.; Ni, J.; Wang, Z.; Wang, J.; Fei, J.; Wang, W.; et al. Downregulation of blood serum microRNA 29 family in patients with Parkinson’s disease. Sci. Rep. 2017, 7, 5411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, R.; Cai, L.; Ma, X.; Shen, K. Autophagy-mediated circHIPK2 promotes lipopolysaccharide-induced astrocytic inflammation via SIGMAR1. Int. Immunopharmacol. 2023, 117, 109907. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.; Zhang, Y.; Han, B.; Bai, Y.; Zhou, R.; Gan, G.; Chao, J.; Hu, G.; Yao, H. Circular RNA HIPK2 regulates astrocyte activation via cooperation of autophagy and ER stress by targeting MIR124-2HG. Autophagy 2017, 13, 1722–1741. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Doxakis, E. Cell-free microRNAs in Parkinson’s disease: Potential biomarkers that provide new insights into disease pathogenesis. Ageing Res. Rev. 2020, 58, 101023. [Google Scholar] [CrossRef]
- Zhang, Y.J.; Zhu, W.K.; Qi, F.Y.; Che, F.Y. CircHIPK3 promotes neuroinflammation through regulation of the miR-124-3p/STAT3/NLRP3 signaling pathway in Parkinson’s disease. Adv. Clin. Exp. Med. 2023, 32, 315–329. [Google Scholar] [CrossRef]
- Zhang, F.; Yao, Y.; Miao, N.; Wang, N.; Xu, X.; Yang, C. Neuroprotective effects of microRNA 124 in Parkinson’s disease mice. Arch. Gerontol. Geriatr. 2022, 99, 104588. [Google Scholar] [CrossRef]
- Yao, L.; Ye, Y.; Mao, H.; Lu, F.; He, X.; Lu, G.; Zhang, S. MicroRNA-124 regulates the expression of MEKK3 in the inflammatory pathogenesis of Parkinson’s disease. J. Neuroinflam. 2018, 15, 13. [Google Scholar] [CrossRef] [Green Version]
- Fire, A.; Xu, S.; Montgomery, M.K.; Kostas, S.A.; Driver, S.E.; Mello, C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391, 806–811. [Google Scholar] [CrossRef]
- Meister, G.; Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431, 343–349. [Google Scholar] [CrossRef]
- Carthew, R.W.; Sontheimer, E.J. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009, 136, 642–655. [Google Scholar] [CrossRef] [Green Version]
- Zamore, P.D.; Tuschl, T.; Sharp, P.A.; Bartel, D.P. RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101, 25–33. [Google Scholar] [CrossRef] [Green Version]
- Whitehead, K.A.; Langer, R.; Anderson, D.G. Knocking down barriers: Advances in siRNA delivery. Nat. Rev. Drug Discov. 2009, 8, 129–138. [Google Scholar] [CrossRef]
- Titze-de-Almeida, R.; David, C.; Titze-de-Almeida, S.S. The Race of 10 Synthetic RNAi-Based Drugs to the Pharmaceutical Market. Pharm. Res. 2017, 34, 1339–1363. [Google Scholar] [CrossRef]
- Setten, R.L.; Rossi, J.J.; Han, S.P. The current state and future directions of RNAi-based therapeutics. Nat. Rev. Drug Discov. 2019, 18, 421–446. [Google Scholar] [CrossRef]
- Moore, C.B.; Guthrie, E.H.; Huang, M.T.; Taxman, D.J. Short hairpin RNA (shRNA): Design, delivery, and assessment of gene knockdown. Methods Mol. Biol. 2010, 629, 141–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rossi, J.J. Expression strategies for short hairpin RNA interference triggers. Hum. Gene Ther. 2008, 19, 313–317. [Google Scholar] [CrossRef]
- Bennett, C.F.; Swayze, E.E. RNA targeting therapeutics: Molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol. 2010, 50, 259–293. [Google Scholar] [CrossRef] [PubMed]
- Rinaldi, C.; Wood, M.J.A. Antisense oligonucleotides: The next frontier for treatment of neurological disorders. Nat. Rev. Neurol. 2018, 14, 9–21. [Google Scholar] [CrossRef]
- Roberts, T.C.; Langer, R.; Wood, M.J.A. Advances in oligonucleotide drug delivery. Nat. Rev. Drug Discov. 2020, 19, 673–694. [Google Scholar] [CrossRef]
- Dhuri, K.; Bechtold, C.; Quijano, E.; Pham, H.; Gupta, A.; Vikram, A.; Bahal, R. Antisense Oligonucleotides: An Emerging Area in Drug Discovery and Development. J. Clin. Med. 2020, 9, 2004. [Google Scholar] [CrossRef]
- Lovendorf, M.B.; Holm, A.; Petri, A.; Thrue, C.A.; Uchida, S.; Veno, M.T.; Kauppinen, S. Knockdown of Circular RNAs Using LNA-Modified Antisense Oligonucleotides. Nucleic Acid Ther. 2023, 33, 45–57. [Google Scholar] [CrossRef]
- Deveau, H.; Garneau, J.E.; Moineau, S. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 2010, 64, 475–493. [Google Scholar] [CrossRef]
- Banan, M. Recent advances in CRISPR/Cas9-mediated knock-ins in mammalian cells. J. Biotechnol. 2020, 308, 1–9. [Google Scholar] [CrossRef]
- Ran, F.A.; Hsu, P.D.; Wright, J.; Agarwala, V.; Scott, D.A.; Zhang, F. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 2013, 8, 2281–2308. [Google Scholar] [CrossRef] [Green Version]
- Heidenreich, M.; Zhang, F. Applications of CRISPR-Cas systems in neuroscience. Nat. Rev. Neurosci. 2016, 17, 36–44. [Google Scholar] [CrossRef] [Green Version]
- Chavez, M.; Chen, X.; Finn, P.B.; Qi, L.S. Advances in CRISPR therapeutics. Nat. Rev. Nephrol. 2023, 19, 9–22. [Google Scholar] [CrossRef]
- Li, X.; Yang, L.; Chen, L.L. The Biogenesis, Functions, and Challenges of Circular RNAs. Mol. Cell 2018, 71, 428–442. [Google Scholar] [CrossRef] [Green Version]
- Meganck, R.M.; Borchardt, E.K.; Castellanos Rivera, R.M.; Scalabrino, M.L.; Wilusz, J.E.; Marzluff, W.F.; Asokan, A. Tissue-Dependent Expression and Translation of Circular RNAs with Recombinant AAV Vectors In Vivo. Mol. Ther. Nucleic Acids 2018, 13, 89–98. [Google Scholar] [CrossRef] [Green Version]
- Meganck, R.M.; Liu, J.; Hale, A.E.; Simon, K.E.; Fanous, M.M.; Vincent, H.A.; Wilusz, J.E.; Moorman, N.J.; Marzluff, W.F.; Asokan, A. Engineering highly efficient backsplicing and translation of synthetic circRNAs. Mol. Ther. Nucleic Acids 2021, 23, 821–834. [Google Scholar] [CrossRef] [PubMed]
- Mecozzi, N.; Nenci, A.; Vera, O.; Bok, I.; Falzone, A.; DeNicola, G.M.; Karreth, F.A. Genetic tools for the stable overexpression of circular RNAs. RNA Biol. 2022, 19, 353–363. [Google Scholar] [CrossRef]
- Feng, Z.; Zhang, L.; Wang, S.; Hong, Q. Circular RNA circDLGAP4 exerts neuroprotective effects via modulating miR-134-5p/CREB pathway in Parkinson’s disease. Biochem. Biophys. Res. Commun. 2020, 522, 388–394. [Google Scholar] [CrossRef]
- Bai, Y.; Zhang, Y.; Han, B.; Yang, L.; Chen, X.; Huang, R.; Wu, F.; Chao, J.; Liu, P.; Hu, G.; et al. Circular RNA DLGAP4 Ameliorates Ischemic Stroke Outcomes by Targeting miR-143 to Regulate Endothelial-Mesenchymal Transition Associated with Blood-Brain Barrier Integrity. J. Neurosci. 2018, 38, 32–50. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Li, Q.; Zhang, R.; Wang, H.; Li, Y.; Liu, Z.; Xie, W.; Geng, D.; Wang, L. circ-Pank1 promotes dopaminergic neuron neurodegeneration through modulating miR-7a-5p/alpha-syn pathway in Parkinson’s disease. Cell Death Dis. 2022, 13, 477. [Google Scholar] [CrossRef]
- Cheng, Q.; Wang, J.; Li, M.; Fang, J.; Ding, H.; Meng, J.; Zhang, J.; Fang, X.; Liu, H.; Ma, C.; et al. CircSV2b participates in oxidative stress regulation through miR-5107-5p-Foxk1-Akt1 axis in Parkinson’s disease. Redox Biol. 2022, 56, 102430. [Google Scholar] [CrossRef]
- Titze-de-Almeida, S.S.; Brandao, P.R.P.; Faber, I.; Titze-de-Almeida, R. Leading RNA Interference Therapeutics Part 1: Silencing Hereditary Transthyretin Amyloidosis, with a Focus on Patisiran. Mol. Diagn. Ther. 2020, 24, 49–59. [Google Scholar] [CrossRef]
- de Paula Brandao, P.R.; Titze-de-Almeida, S.S.; Titze-de-Almeida, R. Leading RNA Interference Therapeutics Part 2: Silencing Delta-Aminolevulinic Acid Synthase 1, with a Focus on Givosiran. Mol. Diagn. Ther. 2020, 24, 61–68. [Google Scholar] [CrossRef]
- Titze de Almeida, S.S.; Horst, C.H.; Soto-Sanchez, C.; Fernandez, E.; Titze de Almeida, R. Delivery of miRNA-Targeted Oligonucleotides in the Rat Striatum by Magnetofection with Neuromag((R)). Molecules 2018, 23, 1825. [Google Scholar] [CrossRef] [Green Version]
- Marks, W.J., Jr.; Bartus, R.T.; Siffert, J.; Davis, C.S.; Lozano, A.; Boulis, N.; Vitek, J.; Stacy, M.; Turner, D.; Verhagen, L.; et al. Gene delivery of AAV2-neurturin for Parkinson’s disease: A double-blind, randomised, controlled trial. Lancet Neurol. 2010, 9, 1164–1172. [Google Scholar] [CrossRef]
- Chu, Y.; Bartus, R.T.; Manfredsson, F.P.; Olanow, C.W.; Kordower, J.H. Long-term post-mortem studies following neurturin gene therapy in patients with advanced Parkinson’s disease. Brain 2020, 143, 960–975. [Google Scholar] [CrossRef]
- Diener, C.; Keller, A.; Meese, E. Emerging concepts of miRNA therapeutics: From cells to clinic. Trends Genet. 2022, 38, 613–626. [Google Scholar] [CrossRef]
- Mumtaz, P.T.; Taban, Q.; Dar, M.A.; Mir, S.; Haq, Z.U.; Zargar, S.M.; Shah, R.A.; Ahmad, S.M. Deep Insights in Circular RNAs: From biogenesis to therapeutics. Biol. Proced. Online 2020, 22, 10. [Google Scholar] [CrossRef]
- Santer, L.; Bar, C.; Thum, T. Circular RNAs: A Novel Class of Functional RNA Molecules with a Therapeutic Perspective. Mol. Ther. 2019, 27, 1350–1363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merck and Orna Therapeutics Collaborate to Advance Orna’s Next Generation of RNA Technology. Available online: https://www.merck.com/news/merck-and-orna-therapeutics-collaborate-to-advance-ornas-next-generation-of-rna-technology/ (accessed on 23 July 2023).
- Mehta, S.L.; Dempsey, R.J.; Vemuganti, R. Role of circular RNAs in brain development and CNS diseases. Prog. Neurobiol. 2020, 186, 101746. [Google Scholar] [CrossRef] [PubMed]
- Garbo, S.; Maione, R.; Tripodi, M.; Battistelli, C. Next RNA Therapeutics: The Mine of Non-Coding. Int. J. Mol. Sci. 2022, 23, 7471. [Google Scholar] [CrossRef]
- Titze-de-Almeida, S.S.; Soto-Sanchez, C.; Fernandez, E.; Koprich, J.B.; Brotchie, J.M.; Titze-de-Almeida, R. The Promise and Challenges of Developing miRNA-Based Therapeutics for Parkinson’s Disease. Cells 2020, 9, 841. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J.; Zhao, M.; Yan, R.; Liu, J.; Maddila, S.; Junn, E.; Mouradian, M.M. MicroRNA-7 Protects Against Neurodegeneration Induced by alpha-Synuclein Preformed Fibrils in the Mouse Brain. Neurotherapeutics 2021, 18, 2529–2540. [Google Scholar] [CrossRef] [PubMed]
- Christine, C.W.; Richardson, R.M.; Van Laar, A.D.; Thompson, M.E.; Fine, E.M.; Khwaja, O.S.; Li, C.; Liang, G.S.; Meier, A.; Roberts, E.W.; et al. Safety of AADC Gene Therapy for Moderately Advanced Parkinson Disease: Three-Year Outcomes From the PD-1101 Trial. Neurology 2022, 98, e40–e50. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Titze-de-Almeida, S.S.; Titze-de-Almeida, R. Progress in circRNA-Targeted Therapy in Experimental Parkinson’s Disease. Pharmaceutics 2023, 15, 2035. https://doi.org/10.3390/pharmaceutics15082035
Titze-de-Almeida SS, Titze-de-Almeida R. Progress in circRNA-Targeted Therapy in Experimental Parkinson’s Disease. Pharmaceutics. 2023; 15(8):2035. https://doi.org/10.3390/pharmaceutics15082035
Chicago/Turabian StyleTitze-de-Almeida, Simoneide Souza, and Ricardo Titze-de-Almeida. 2023. "Progress in circRNA-Targeted Therapy in Experimental Parkinson’s Disease" Pharmaceutics 15, no. 8: 2035. https://doi.org/10.3390/pharmaceutics15082035
APA StyleTitze-de-Almeida, S. S., & Titze-de-Almeida, R. (2023). Progress in circRNA-Targeted Therapy in Experimental Parkinson’s Disease. Pharmaceutics, 15(8), 2035. https://doi.org/10.3390/pharmaceutics15082035