CircRNAs as a Novel Class of Potential Diagnostic Biomarkers in Bipolar Disorders


Cite item

Full Text

Abstract

:Bipolar disorder (BD) is a severe mood disorder with uncertain causes and debilitating signs and symptoms. Gene expression is crucial to the pathophysiology of BD and could be influenced by genetic or epigenetic factors, by either direct modification of mRNA templates or by regulation of post-transcriptional translation. Recent evidence has shown that several critical processes in psychiatric diseases, such as neuronal activity or plasticity, synaptic transmission, and neuronal depolarization, have all been linked to circular RNAs (circRNAs). The circRNA profile of neuronal cells, which may be easily ascertained by a liquid biopsy, may shed light on the molecular pathophysiology of psychiatric disorders, including BD. This approach could aid in future development in diagnosis and treatment. In this review, we provide an in-depth understanding of the roles of circRNAs in the pathophysiology of BD and offer new insight into their potential as emerging diagnostic tools and therapeutic targets.

About the authors

Reza Asemi

Department of Internal Medicine, School of Medicine, Cancer Prevention Research Center, Seyyed Al-Shohada Hospital, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Amrollah Ebrahimi

Department of Health Psychology, School of Medicine, Isfahan University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

Michael Hamblin

Laser Research Centre, Faculty of Health Science, University of Johannesburg

Email: info@benthamscience.net

Hamed Mirzaei

Research Center for Biochemistry and Nutrition in Metabolic Diseases, Institute for Basic Sciences, Kashan University of Medical Sciences

Email: info@benthamscience.net

Zatollah Asemi

Research Center for Biochemistry and Nutrition in Metabolic Diseases, Institute for Basic Sciences, Kashan University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

References

  1. McIntyre, R.S.; Berk, M.; Brietzke, E.; Goldstein, B.I.; López-Jaramillo, C.; Kessing, L.V.; Malhi, G.S.; Nierenberg, A.A.; Rosenblat, J.D.; Majeed, A.; Vieta, E.; Vinberg, M.; Young, A.H.; Mansur, R.B. Bipolar disorders. Lancet, 2020, 396(10265), 1841-1856. doi: 10.1016/S0140-6736(20)31544-0 PMID: 33278937
  2. Shao, L.; Vawter, M.P. Shared gene expression alterations in schizophrenia and bipolar disorder. Biol. Psychiatry, 2008, 64(2), 89-97. doi: 10.1016/j.biopsych.2007.11.010 PMID: 18191109
  3. Craddock, N.; Sklar, P. Genetics of bipolar disorder. Lancet, 2013, 381(9878), 1654-1662. doi: 10.1016/S0140-6736(13)60855-7 PMID: 23663951
  4. Psychiatric GWAS Consortium Bipolar Disorder Working Group.. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat. Genet., 2011, 43(10), 977-983. doi: 10.1038/ng.943 PMID: 21926972
  5. Stahl, E.A.; Breen, G.; Forstner, A.J.; McQuillin, A.; Ripke, S.; Trubetskoy, V.; Mattheisen, M.; Wang, Y.; Coleman, J.R.I.; Gaspar, H.A.; de Leeuw, C.A.; Steinberg, S.; Pavlides, J.M.W.; Trzaskowski, M.; Byrne, E.M.; Pers, T.H.; Holmans, P.A.; Richards, A.L.; Abbott, L.; Agerbo, E.; Akil, H.; Albani, D.; Alliey-Rodriguez, N.; Als, T.D.; Anjorin, A.; Antilla, V.; Awasthi, S.; Badner, J.A.; Bækvad-Hansen, M.; Barchas, J.D.; Bass, N.; Bauer, M.; Belliveau, R.; Bergen, S.E.; Pedersen, C.B.; Bøen, E.; Boks, M.P.; Boocock, J.; Budde, M.; Bunney, W.; Burmeister, M.; Bybjerg-Grauholm, J.; Byerley, W.; Casas, M.; Cerrato, F.; Cervantes, P.; Chambert, K.; Charney, A.W.; Chen, D.; Churchhouse, C.; Clarke, T.K.; Coryell, W.; Craig, D.W.; Cruceanu, C.; Curtis, D.; Czerski, P.M.; Dale, A.M.; de Jong, S.; Degenhardt, F.; Del-Favero, J.; DePaulo, J.R.; Djurovic, S.; Dobbyn, A.L.; Dumont, A.; Elvsåshagen, T.; Escott-Price, V.; Fan, C.C.; Fischer, S.B.; Flickinger, M.; Foroud, T.M.; Forty, L.; Frank, J.; Fraser, C.; Freimer, N.B.; Frisén, L.; Gade, K.; Gage, D.; Garnham, J.; Giambartolomei, C.; Pedersen, M.G.; Goldstein, J.; Gordon, S.D.; Gordon-Smith, K.; Green, E.K.; Green, M.J.; Greenwood, T.A.; Grove, J.; Guan, W.; Guzman-Parra, J.; Hamshere, M.L.; Hautzinger, M.; Heilbronner, U.; Herms, S.; Hipolito, M.; Hoffmann, P.; Holland, D.; Huckins, L.; Jamain, S.; Johnson, J.S.; Juréus, A.; Kandaswamy, R.; Karlsson, R.; Kennedy, J.L.; Kittel-Schneider, S.; Knowles, J.A.; Kogevinas, M.; Koller, A.C.; Kupka, R.; Lavebratt, C.; Lawrence, J.; Lawson, W.B.; Leber, M.; Lee, P.H.; Levy, S.E.; Li, J.Z.; Liu, C.; Lucae, S.; Maaser, A.; MacIntyre, D.J.; Mahon, P.B.; Maier, W.; Martinsson, L.; McCarroll, S.; McGuffin, P.; McInnis, M.G.; McKay, J.D.; Medeiros, H.; Medland, S.E.; Meng, F.; Milani, L.; Montgomery, G.W.; Morris, D.W.; Mühleisen, T.W.; Mullins, N.; Nguyen, H.; Nievergelt, C.M.; Adolfsson, A.N.; Nwulia, E.A.; O’Donovan, C.; Loohuis, L.M.O.; Ori, A.P.S.; Oruc, L.; Ösby, U.; Perlis, R.H.; Perry, A.; Pfennig, A.; Potash, J.B.; Purcell, S.M.; Regeer, E.J.; Reif, A.; Reinbold, C.S.; Rice, J.P.; Rivas, F.; Rivera, M.; Roussos, P.; Ruderfer, D.M.; Ryu, E.; Sánchez-Mora, C.; Schatzberg, A.F.; Scheftner, W.A.; Schork, N.J.; Shannon Weickert, C.; Shehktman, T.; Shilling, P.D.; Sigurdsson, E.; Slaney, C.; Smeland, O.B.; Sobell, J.L.; Søholm Hansen, C.; Spijker, A.T.; St Clair, D.; Steffens, M.; Strauss, J.S.; Streit, F.; Strohmaier, J.; Szelinger, S.; Thompson, R.C.; Thorgeirsson, T.E.; Treutlein, J.; Vedder, H.; Wang, W.; Watson, S.J.; Weickert, T.W.; Witt, S.H.; Xi, S.; Xu, W.; Young, A.H.; Zandi, P.; Zhang, P.; Zöllner, S.; Adolfsson, R.; Agartz, I.; Alda, M.; Backlund, L.; Baune, B.T.; Bellivier, F.; Berrettini, W.H.; Biernacka, J.M.; Blackwood, D.H.R.; Boehnke, M.; Børglum, A.D.; Corvin, A.; Craddock, N.; Daly, M.J.; Dannlowski, U.; Esko, T.; Etain, B.; Frye, M.; Fullerton, J.M.; Gershon, E.S.; Gill, M.; Goes, F.; Grigoroiu-Serbanescu, M.; Hauser, J.; Hougaard, D.M.; Hultman, C.M.; Jones, I.; Jones, L.A.; Kahn, R.S.; Kirov, G.; Landén, M.; Leboyer, M.; Lewis, C.M.; Li, Q.S.; Lissowska, J.; Martin, N.G.; Mayoral, F.; McElroy, S.L.; McIntosh, A.M.; McMahon, F.J.; Melle, I.; Metspalu, A.; Mitchell, P.B.; Morken, G.; Mors, O.; Mortensen, P.B.; Müller-Myhsok, B.; Myers, R.M.; Neale, B.M.; Nimgaonkar, V.; Nordentoft, M.; Nöthen, M.M.; O’Donovan, M.C.; Oedegaard, K.J.; Owen, M.J.; Paciga, S.A.; Pato, C.; Pato, M.T.; Posthuma, D.; Ramos-Quiroga, J.A.; Ribasés, M.; Rietschel, M.; Rouleau, G.A.; Schalling, M.; Schofield, P.R.; Schulze, T.G.; Serretti, A.; Smoller, J.W.; Stefansson, H.; Stefansson, K.; Stordal, E.; Sullivan, P.F.; Turecki, G.; Vaaler, A.E.; Vieta, E.; Vincent, J.B.; Werge, T.; Nurnberger, J.I.; Wray, N.R.; Di Florio, A.; Edenberg, H.J.; Cichon, S.; Ophoff, R.A.; Scott, L.J.; Andreassen, O.A.; Kelsoe, J.; Sklar, P. Genome-wide association study identifies 30 loci associated with bipolar disorder. Nat. Genet., 2019, 51(5), 793-803. doi: 10.1038/s41588-019-0397-8 PMID: 31043756
  6. Cruceanu, C.; Ambalavanan, A.; Spiegelman, D.; Gauthier, J.; Lafrenière, R.G.; Dion, P.A.; Alda, M.; Turecki, G.; Rouleau, G.A. Family-based exome-sequencing approach identifies rare susceptibility variants for lithium-responsive bipolar disorder. Genome, 2013, 56(10), 634-640. doi: 10.1139/gen-2013-0081 PMID: 24237345
  7. Goes, F.S.; Pirooznia, M.; Parla, J.S.; Kramer, M.; Ghiban, E.; Mavruk, S.; Chen, Y.C.; Monson, E.T.; Willour, V.L.; Karchin, R.; Flickinger, M.; Locke, A.E.; Levy, S.E.; Scott, L.J.; Boehnke, M.; Stahl, E.; Moran, J.L.; Hultman, C.M.; Landén, M.; Purcell, S.M.; Sklar, P.; Zandi, P.P.; McCombie, W.R.; Potash, J.B. Exome sequencing of familial bipolar disorder. JAMA Psychiatry, 2016, 73(6), 590-597. doi: 10.1001/jamapsychiatry.2016.0251 PMID: 27120077
  8. Middleton, F.A.; Pato, C.N.; Gentile, K.L.; McGann, L.; Brown, A.M.; Trauzzi, M. Gene expression analysis of peripheral blood leukocytes from discordant sib-pairs with schizophrenia and bipolar disorder reveals points of convergence between genetic and functional genomic approaches. Am. J. Med. Genet. B Neuropsychiatr. Genet., 2005, 136B(1), 12-25. doi: 10.1002/ajmg.b.30171 PMID: 15892139
  9. Cardamone, G.; Paraboschi, E.M.; Soldà, G.; Liberatore, G.; Rimoldi, V.; Cibella, J.; Airi, F.; Tisato, V.; Cantoni, C.; Gallia, F.; Gemmati, D.; Piccio, L.; Duga, S.; Nobile-Orazio, E.; Asselta, R. The circular RNA landscape in multiple sclerosis: Disease-specific associated variants and exon methylation shape circular RNA expression profile. Mult. Scler. Relat. Disord., 2023, 69, 104426. doi: 10.1016/j.msard.2022.104426 PMID: 36446168
  10. Mahmoudi, E.; Green, M.J.; Cairns, M.J. Dysregulation of circRNA expression in the peripheral blood of individuals with schizophrenia and bipolar disorder. J. Mol. Med., 2021, 99(7), 981-991. doi: 10.1007/s00109-021-02070-6 PMID: 33782720
  11. Ren, Z.; Chu, C.; Pang, Y.; Cai, H.; Jia, L. A circular RNA blood panel that differentiates Alzheimer’s disease from other dementia types. Biomark. Res., 2022, 10(1), 63. doi: 10.1186/s40364-022-00405-0 PMID: 35982472
  12. Dorostgou, Z.; Yadegar, N.; Dorostgou, Z.; Khorvash, F.; Vakili, O. Novel insights into the role of circular RNAS in Parkinson disease: An emerging renaissance in the management of neurodegenerative diseases. J. Neurosci. Res., 2022, 100(9), 1775-1790. doi: 10.1002/jnr.25094 PMID: 35642104
  13. Mao, Q.; Tian, L.; Wei, J.; Zhou, X.; Cheng, H.; Zhu, X.; Li, X.; Gao, Z.; Zhang, X.; Liang, L. Transcriptome analysis of microRNAs, circRNAs, and mRNAs in the dorsal root ganglia of paclitaxel-induced mice with neuropathic pain. Front. Mol. Neurosci., 2022, 15, 990260. doi: 10.3389/fnmol.2022.990260 PMID: 36117915
  14. Özerdem, A.; Ceylan, D.; Can, G. Neurobiology of risk for bipolar disorder. Curr. Treat. Options Psychiatry, 2016, 3(4), 315-329. doi: 10.1007/s40501-016-0093-6 PMID: 27867834
  15. 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(1), 55-66. doi: 10.1016/j.molcel.2014.08.019 PMID: 25242144
  16. Li, Z.; Huang, C.; Bao, C.; Chen, L.; Lin, M.; Wang, X.; Zhong, G.; Yu, B.; Hu, W.; Dai, L.; Zhu, P.; Chang, Z.; Wu, Q.; Zhao, Y.; Jia, Y.; Xu, P.; Liu, H.; Shan, G. Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol., 2015, 22(3), 256-264. doi: 10.1038/nsmb.2959 PMID: 25664725
  17. Zhang, X.O.; Wang, H.B.; Zhang, Y.; Lu, X.; Chen, L.L.; Yang, L. Complementary sequence-mediated exon circularization. Cell, 2014, 159(1), 134-147. doi: 10.1016/j.cell.2014.09.001 PMID: 25242744
  18. Starke, S.; Jost, I.; Rossbach, O.; Schneider, T.; Schreiner, S.; Hung, L.H.; Bindereif, A. Exon circularization requires canonical splice signals. Cell Rep., 2015, 10(1), 103-111. doi: 10.1016/j.celrep.2014.12.002 PMID: 25543144
  19. Bachmayr-Heyda, A.; Reiner, A.T.; Auer, K.; Sukhbaatar, N.; Aust, S.; Bachleitner-Hofmann, T.; Mesteri, I.; Grunt, T.W.; Zeillinger, R.; Pils, D. Correlation of circular RNA abundance with proliferation – exemplified with colorectal and ovarian cancer, idiopathic lung fibrosis and normal human tissues. Sci. Rep., 2015, 5(1), 8057. doi: 10.1038/srep08057 PMID: 25624062
  20. Li, Y.; Zheng, Q.; Bao, C.; Li, S.; Guo, W.; Zhao, J.; Chen, D.; Gu, J.; He, X.; Huang, S. Circular RNA is enriched and stable in exosomes: A promising biomarker for cancer diagnosis. Cell Res., 2015, 25(8), 981-984. doi: 10.1038/cr.2015.82 PMID: 26138677
  21. Lukiw, W.J. Circular RNA (circRNA) in Alzheimer’s disease (AD). Front. Genet., 2013, 4, 307. doi: 10.3389/fgene.2013.00307 PMID: 24427167
  22. Memczak, S.; Jens, M.; Elefsinioti, A.; Torti, F.; Krueger, J.; Rybak, A.; Maier, L.; Mackowiak, S.D.; Gregersen, L.H.; Munschauer, M.; Loewer, A.; Ziebold, U.; Landthaler, M.; Kocks, C.; le Noble, F.; Rajewsky, N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013, 495(7441), 333-338. doi: 10.1038/nature11928 PMID: 23446348
  23. 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(7441), 384-388. doi: 10.1038/nature11993 PMID: 23446346
  24. Guo, J.U.; Agarwal, V.; Guo, H.; Bartel, D.P. Expanded identification and characterization of mammalian circular RNAs. Genome Biol., 2014, 15(7), 409. doi: 10.1186/s13059-014-0409-z PMID: 25070500
  25. Han, D.; Li, J.; Wang, H.; Su, X.; Hou, J.; Gu, Y.; Qian, C.; Lin, Y.; Liu, X.; Huang, M.; Li, N.; Zhou, W.; Yu, Y.; Cao, X. Circular RNA circMTO1 acts as the sponge of microRNA-9 to suppress hepatocellular carcinoma progression. Hepatology, 2017, 66(4), 1151-1164. doi: 10.1002/hep.29270 PMID: 28520103
  26. 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(6), 2846-2858. doi: 10.1093/nar/gkw027 PMID: 26861625
  27. You, X.; Vlatkovic, I.; Babic, A.; Will, T.; Epstein, I.; Tushev, G.; Akbalik, G.; Wang, M.; Glock, C.; Quedenau, C.; Wang, X.; Hou, J.; Liu, H.; Sun, W.; Sambandan, S.; Chen, T.; Schuman, E.M.; Chen, W. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat. Neurosci., 2015, 18(4), 603-610. doi: 10.1038/nn.3975 PMID: 25714049
  28. 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(6), 1125-1134. doi: 10.1016/j.cell.2015.02.014 PMID: 25768908
  29. Yang, Y.; Fan, X.; Mao, M.; Song, X.; Wu, P.; Zhang, Y.; Jin, Y.; Yang, Y.; Chen, L.L.; Wang, Y.; Wong, C.C.L.; Xiao, X.; Wang, Z. Extensive translation of circular RNAs driven by N6-methyladenosine. Cell Res., 2017, 27(5), 626-641. doi: 10.1038/cr.2017.31 PMID: 28281539
  30. Legnini, I.; Di Timoteo, G.; Rossi, F.; Morlando, M.; Briganti, F.; Sthandier, O.; Fatica, A.; Santini, T.; Andronache, A.; Wade, M.; Laneve, P.; Rajewsky, N.; Bozzoni, I. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol. Cell, 2017, 66(1), 22-37.e9. doi: 10.1016/j.molcel.2017.02.017 PMID: 28344082
  31. Rybak-Wolf, A.; Stottmeister, C.; Glažar, P.; Jens, M.; Pino, N.; Giusti, S.; Hanan, M.; Behm, M.; Bartok, O.; Ashwal-Fluss, R.; Herzog, M.; Schreyer, L.; Papavasileiou, P.; Ivanov, A.; Öhman, M.; Refojo, D.; Kadener, S.; Rajewsky, N. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell, 2015, 58(5), 870-885. doi: 10.1016/j.molcel.2015.03.027 PMID: 25921068
  32. Sekar, S.; Liang, W.S. Circular RNA expression and function in the brain. Noncoding RNA Res., 2019, 4(1), 23-29. doi: 10.1016/j.ncrna.2019.01.001 PMID: 30891534
  33. Hanan, M.; Soreq, H.; Kadener, S. CircRNAs in the brain. RNA Biol., 2017, 14(8), 1028-1034. doi: 10.1080/15476286.2016.1255398 PMID: 27892769
  34. Luykx, J.J.; Giuliani, F.; Giuliani, G.; Veldink, J. Coding and non-coding RNA abnormalities in bipolar disorder. Genes, 2019, 10(11), 946. doi: 10.3390/genes10110946 PMID: 31752442
  35. Dines, M.; Lamprecht, R. The role of ephs and ephrins in memory formation. Int. J. Neuropsychopharmacol., 2016, 19(4), pyv106. doi: 10.1093/ijnp/pyv106 PMID: 26371183
  36. Dines, M.; Lamprecht, R. EphrinA4 mimetic peptide targeted to EphA binding site impairs the formation of long-term fear memory in lateral amygdala. Transl. Psychiatry, 2014, 4(9), e450. doi: 10.1038/tp.2014.76 PMID: 25268254
  37. Attwood, B.K.; Bourgognon, J.M.; Patel, S.; Mucha, M.; Schiavon, E.; Skrzypiec, A.E.; Young, K.W.; Shiosaka, S.; Korostynski, M.; Piechota, M.; Przewlocki, R.; Pawlak, R. Neuropsin cleaves EphB2 in the amygdala to control anxiety. Nature, 2011, 473(7347), 372-375. doi: 10.1038/nature09938 PMID: 21508957
  38. Shi, Y.; Song, R.; Wang, Z.; Zhang, H.; Zhu, J.; Yue, Y.; Zhao, Y.; Zhang, Z. Potential clinical value of circular RNAs as peripheral biomarkers for the diagnosis and treatment of major depressive disorder. EBioMedicine, 2021, 66, 103337. doi: 10.1016/j.ebiom.2021.103337 PMID: 33862583
  39. Zimmerman, A.J.; Hafez, A.K.; Amoah, S.K.; Rodriguez, B.A.; Dell’Orco, M.; Lozano, E.; Hartley, B.J.; Alural, B.; Lalonde, J.; Chander, P.; Webster, M.J.; Perlis, R.H.; Brennand, K.J.; Haggarty, S.J.; Weick, J.; Perrone-Bizzozero, N.; Brigman, J.L.; Mellios, N. A psychiatric disease-related circular RNA controls synaptic gene expression and cognition. Mol. Psychiatry, 2020, 25(11), 2712-2727. doi: 10.1038/s41380-020-0653-4 PMID: 31988434
  40. Yang, L.; Han, B.; Zhang, Z.; Wang, S.; Bai, Y.; Zhang, Y.; Tang, Y.; Du, L.; Xu, L.; Wu, F.; Zuo, L.; Chen, X.; Lin, Y.; Liu, K.; Ye, Q.; Chen, B.; Li, B.; Tang, T.; Wang, Y.; Shen, L.; Wang, G.; Ju, M.; Yuan, M.; Jiang, W.; Zhang, J.H.; Hu, G.; Wang, J.; Yao, H. Extracellular vesicle–mediated delivery of circular RNA SCMH1 promotes functional recovery in rodent and nonhuman primate ischemic stroke models. Circulation, 2020, 142(6), 556-574. doi: 10.1161/CIRCULATIONAHA.120.045765 PMID: 32441115
  41. Pan, R.Y.; Liu, P.; Zhou, H.T.; Sun, W.X.; Song, J.; Shu, J.; Cui, G.J.; Yang, Z.J.; Jia, E.Z. Circular RNAs promote TRPM3 expression by inhibiting hsa-miR-130a-3p in coronary artery disease patients. Oncotarget, 2017, 8(36), 60280-60290. doi: 10.18632/oncotarget.19941 PMID: 28947970
  42. Haque, S.; Harries, L. Circular RNAs (circRNAs) in Health and Disease. Genes, 2017, 8(12), 353. doi: 10.3390/genes8120353 PMID: 29182528
  43. Gardiner, E.; Beveridge, N.J.; Wu, J.Q.; Carr, V.; Scott, R.J.; Tooney, P.A.; Cairns, M.J. Imprinted DLK1-DIO3 region of 14q32 defines a schizophrenia-associated miRNA signature in peripheral blood mononuclear cells. Mol. Psychiatry, 2012, 17(8), 827-840. doi: 10.1038/mp.2011.78 PMID: 21727898
  44. Lin, R.; Lopez, J.P.; Cruceanu, C.; Pierotti, C.; Fiori, L.M.; Squassina, A.; Chillotti, C.; Dieterich, C.; Mellios, N.; Turecki, G. Circular RNA circCCNT2 is upregulated in the anterior cingulate cortex of individuals with bipolar disorder. Transl. Psychiatry, 2021, 11(1), 629. doi: 10.1038/s41398-021-01746-4 PMID: 34893581
  45. Cruceanu, C.; Tan, P.P.C.; Rogic, S.; Lopez, J.P.; Torres-Platas, S.G.; Gigek, C.O.; Alda, M.; Rouleau, G.A.; Pavlidis, P.; Turecki, G. Transcriptome sequencing of the anterior cingulate in bipolar disorder: Dysregulation of G protein-coupled receptors. Am. J. Psychiatry, 2015, 172(11), 1131-1140. doi: 10.1176/appi.ajp.2015.14101279 PMID: 26238605
  46. Liu, Y.; Guo, J.; Shen, K.; Wang, R.; Chen, C.; Liao, Z.; Zhou, J. Paclitaxel suppresses hepatocellular carcinoma tumorigenesis through regulating Circ-BIRC6/miR-877-5p/YWHAZ axis. OncoTargets Ther., 2020, 13, 9377-9388. doi: 10.2147/OTT.S261700 PMID: 33061425
  47. Yu, Y.; Bian, L.; Liu, R.; Wang, Y.; Xiao, X. Circular RNA hsa_circ_0061395 accelerates hepatocellular carcinoma progression via regulation of the miR-877-5p/PIK3R3 axis. Cancer Cell Int., 2021, 21(1), 10. doi: 10.1186/s12935-020-01695-w PMID: 33407443
  48. Fu, Y.; He, W.; Zhou, C.; Fu, X.; Wan, Q.; He, L.; Wei, B. Bioinformatics analysis of circRNA expression and construction of "circRNA-miRNA-mRNA" competing endogenous RNAs networks in bipolar disorder patients. Front. Genet., 2021, 12, 718976. doi: 10.3389/fgene.2021.718976 PMID: 34422020

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers