microRNA and the Post-Transcriptional Response to Oxidative Stress during Neuronal Differentiation: Implications for Neurodevelopmental and Psychiatric Disorders
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Culture and Differentiation
2.2. Application of Oxidative Stress
2.3. RNA Extraction and Integrity Analysis
2.4. Small RNA-Sequencing
2.5. Processing of Sequencing Data and Differential Expression Analysis
2.6. Identification of Psychiatry-Related Dysregulated miRNAs
2.7. miRNA-mRNA Correlation Analysis and Network Visualisation
2.8. Gene Set Enrichment Analysis (GSEA)
3. Results
3.1. Confirmation of Differentiation
3.2. miRNA Expression in Response to Oxidative Stress
3.3. Oxidative Stress-Associated miRNAs Related to Psychiatric Disorders
3.4. miRNA-mRNA Expression Correlation and Network Construction
3.5. Functional Enrichment Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Wilson, C.; Muñoz-Palma, E.; González-Billault, C. From birth to death: A role for reactive oxygen species in neuronal development. Semin. Cell Dev. Biol. 2018, 80, 43–49. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, Y.; Kanda, Y.; Sone, H.; Aoyama, H. Oxidative Stress as a Common Key Event in Developmental Neurotoxicity. Oxid. Med. Cell Longev. 2021, 2021, 6685204. [Google Scholar] [CrossRef]
- Hardingham, G.E.; Do, K.Q. Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis. Nat. Rev. Neurosci. 2016, 17, 125–134. [Google Scholar] [CrossRef] [PubMed]
- Gawryluk, J.W.; Wang, J.F.; Andreazza, A.C.; Shao, L.; Young, L.T. Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders. Int. J. Neuropsychopharmacol. 2011, 14, 123–130. [Google Scholar] [CrossRef]
- Pangrazzi, L.; Balasco, L.; Bozzi, Y. Oxidative Stress and Immune System Dysfunction in Autism Spectrum Disorders. Int. J. Mol. Sci. 2020, 21, 3293. [Google Scholar] [CrossRef] [PubMed]
- Kennedy, K.A.; Sandiford, S.D.; Skerjanc, I.S.; Li, S.S. Reactive oxygen species and the neuronal fate. Cell Mol. Life Sci. 2012, 69, 215–221. [Google Scholar] [CrossRef]
- Gysin, R.; Kraftsik, R.; Sandell, J.; Bovet, P.; Chappuis, C.; Conus, P.; Deppen, P.; Preisig, M.; Ruiz, V.; Steullet, P.; et al. Impaired glutathione synthesis in schizophrenia: Convergent genetic and functional evidence. Proc. Natl. Acad. Sci. USA 2007, 104, 16621–16626. [Google Scholar] [CrossRef]
- Rodríguez-Santiago, B.; Brunet, A.; Sobrino, B.; Serra-Juhé, C.; Flores, R.; Armengol, L.; Vilella, E.; Gabau, E.; Guitart, M.; Guillamat, R.; et al. Association of common copy number variants at the glutathione S-transferase genes and rare novel genomic changes with schizophrenia. Mol. Psychiatry 2010, 15, 1023–1033. [Google Scholar] [CrossRef]
- Kim, Y.; Vadodaria, K.C.; Lenkei, Z.; Kato, T.; Gage, F.H.; Marchetto, M.C.; Santos, R. Mitochondria, Metabolism, and Redox Mechanisms in Psychiatric Disorders. Antioxid. Redox Signal 2019, 31, 275–317. [Google Scholar] [CrossRef]
- Kulak, A.; Cuenod, M.; Do, K.Q. Behavioral phenotyping of glutathione-deficient mice: Relevance to schizophrenia and bipolar disorder. Behav. Brain Res. 2012, 226, 563–570. [Google Scholar] [CrossRef]
- Cabungcal, J.H.; Preissmann, D.; Delseth, C.; Cuénod, M.; Do, K.Q.; Schenk, F. Transitory glutathione deficit during brain development induces cognitive impairment in juvenile and adult rats: Relevance to schizophrenia. Neurobiol. Dis. 2007, 26, 634–645. [Google Scholar] [CrossRef] [PubMed]
- Khavari, B.; Mahmoudi, E.; Geaghan, M.P.; Cairns, M.J. Oxidative Stress Impact on the Transcriptome of Differentiating Neuroblastoma Cells: Implication for Psychiatric Disorders. Int. J. Mol. Sci. 2020, 21, 9182. [Google Scholar] [CrossRef] [PubMed]
- O’Brien, J.; Hayder, H.; Zayed, Y.; Peng, C. Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation. Front. Endocrinol. 2018, 9, 402. [Google Scholar] [CrossRef] [PubMed]
- Khavari, B.; Cairns, M.J. Epigenomic Dysregulation in Schizophrenia: In Search of Disease Etiology and Biomarkers. Cells 2020, 9, 1837. [Google Scholar] [CrossRef] [PubMed]
- Beveridge, N.J.; Cairns, M.J. MicroRNA dysregulation in schizophrenia. Neurobiol. Dis. 2012, 46, 263–271. [Google Scholar] [CrossRef] [PubMed]
- Geaghan, M.; Cairns, M.J. MicroRNA and Posttranscriptional Dysregulation in Psychiatry. Biol. Psychiatry 2015, 78, 231–239. [Google Scholar] [CrossRef] [PubMed]
- Smigielski, L.; Jagannath, V.; Rössler, W.; Walitza, S.; Grünblatt, E. Epigenetic mechanisms in schizophrenia and other psychotic disorders: A systematic review of empirical human findings. Mol. Psychiatry 2020, 25, 1718–1748. [Google Scholar] [CrossRef] [PubMed]
- Hollins, S.L.; Cairns, M.J. MicroRNA: Small RNA mediators of the brains genomic response to environmental stress. Prog. Neurobiol. 2016, 143, 61–81. [Google Scholar] [CrossRef] [PubMed]
- Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357–359. [Google Scholar] [CrossRef]
- Anders, S.; Pyl, P.T.; Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166–169. [Google Scholar] [CrossRef]
- Robinson, M.D.; McCarthy, D.J.; Smyth, G.K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26, 139–140. [Google Scholar] [CrossRef] [PubMed]
- Haunsberger, S.J.; Connolly, N.M.; Prehn, J.H. miRNAmeConverter: An R/bioconductor package for translating mature miRNA names to different miRBase versions. Bioinformatics 2017, 33, 592–593. [Google Scholar] [CrossRef]
- Kozomara, A.; Birgaoanu, M.; Griffiths-Jones, S. miRBase: From microRNA sequences to function. Nucleic Acids Res. 2019, 47, D155–D162. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, V.; Bell, G.W.; Nam, J.W.; Bartel, D.P. Predicting effective microRNA target sites in mammalian mRNAs. eLife 2015, 4, e05005. [Google Scholar] [CrossRef] [PubMed]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Bardes, E.E.; Aronow, B.J.; Jegga, A.G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 2009, 37, W305–W311. [Google Scholar] [CrossRef] [PubMed]
- Beveridge, N.J.; Gardiner, E.; Carroll, A.P.; Tooney, P.A.; Cairns, M.J. Schizophrenia is associated with an increase in cortical microRNA biogenesis. Mol. Psychiatry 2010, 15, 1176–1189. [Google Scholar] [CrossRef] [PubMed]
- Moreau, M.P.; Bruse, S.E.; David-Rus, R.; Buyske, S.; Brzustowicz, L.M. Altered microRNA expression profiles in postmortem brain samples from individuals with schizophrenia and bipolar disorder. Biol. Psychiatry 2011, 69, 188–193. [Google Scholar] [CrossRef] [PubMed]
- Santarelli, D.M.; Beveridge, N.J.; Tooney, P.A.; Cairns, M.J. Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol. Psychiatry 2011, 69, 180–187. [Google Scholar] [CrossRef]
- Mahmoudi, E.; Cairns, M.J. MiR-137: An important player in neural development and neoplastic transformation. Mol. Psychiatry 2017, 22, 44–55. [Google Scholar] [CrossRef]
- Pantelis, C.; Papadimitriou, G.N.; Papiol, S.; Parkhomenko, E.; Pato, M.T.; Paunio, T.; Pejovic-Milovancevic, M.; Perkins, D.O.; Pietiläinen, O.; Pimm, J. Biological insights from 108 schizophrenia-associated genetic loci. Nature 2014, 511, 421–427. [Google Scholar] [CrossRef] [PubMed]
- Green, M.J.; Cairns, M.J.; Wu, J.; Dragovic, M.; Jablensky, A.; Tooney, P.A.; Scott, R.J.; Carr, V.J. Genome-wide supported variant MIR137 and severe negative symptoms predict membership of an impaired cognitive subtype of schizophrenia. Mol. Psychiatry 2013, 18, 774–780. [Google Scholar] [CrossRef] [PubMed]
- Mahmoudi, E.; Atkins, J.R.; Quide, Y.; Reay, W.R.; Cairns, H.M.; Fitzsimmons, C.; Carr, V.J.; Green, M.J.; Cairns, M.J. The MIR137 VNTR rs58335419 Is Associated with Cognitive Impairment in Schizophrenia and Altered Cortical Morphology. Schizophr. Bull. 2021, 47, 495–504. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Zhang, F.; Wang, X.; Shugart, Y.Y.; Zhao, Y.; Li, X.; Liu, Z.; Sun, N.; Yang, C.; Zhang, K.; et al. Diagnostic value of blood-derived microRNAs for schizophrenia: Results of a meta-analysis and validation. Sci. Rep. 2017, 7, 15328. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.; Zhang, R.; Nie, F.; Wang, X.; Jiang, C.; Liu, M.; Valenzuela, R.K.; Liu, W.; Shi, Y.; Ma, J. MicroRNA-137 Inhibits EFNB2 Expression Affected by a Genetic Variant and Is Expressed Aberrantly in Peripheral Blood of Schizophrenia Patients. EBioMedicine 2016, 12, 133–142. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Shang, S.; Wang, J.; Zhang, T.; Nie, F.; Song, X.; Heping, Z.; Zhu, C.; Zhang, R.; Hao, D. Identification of miR-22-3p, miR-92a-3p, and miR-137 in peripheral blood as biomarker for schizophrenia. Psychiatry Res. 2018, 265, 70–76. [Google Scholar] [CrossRef] [PubMed]
- Arakawa, Y.; Yokoyama, K.; Tasaki, S.; Kato, J.; Nakashima, K.; Takeyama, M.; Nakatani, A.; Suzuki, M. Transgenic mice overexpressing miR-137 in the brain show schizophrenia-associated behavioral deficits and transcriptome profiles. PLoS ONE 2019, 14, e0220389. [Google Scholar] [CrossRef] [PubMed]
- Mao, S.; Li, H.; Sun, Q.; Zen, K.; Zhang, C.Y.; Li, L. miR-17 regulates the proliferation and differentiation of the neural precursor cells during mouse corticogenesis. FEBS J. 2014, 281, 1144–1158. [Google Scholar] [CrossRef] [PubMed]
- Beveridge, N.J.; Tooney, P.A.; Carroll, A.P.; Tran, N.; Cairns, M.J. Down-regulation of miR-17 family expression in response to retinoic acid induced neuronal differentiation. Cell Signal 2009, 21, 1837–1845. [Google Scholar] [CrossRef]
- Chen, D.; Dixon, B.J.; Doycheva, D.M.; Li, B.; Zhang, Y.; Hu, Q.; He, Y.; Guo, Z.; Nowrangi, D.; Flores, J.; et al. IRE1α inhibition decreased TXNIP/NLRP3 inflammasome activation through miR-17-5p after neonatal hypoxic-ischemic brain injury in rats. J. Neuroinflamm. 2018, 15, 32. [Google Scholar] [CrossRef]
- Jovičić, A.; Roshan, R.; Moisoi, N.; Pradervand, S.; Moser, R.; Pillai, B.; Luthi-Carter, R. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J. Neurosci. 2013, 33, 5127–5137. [Google Scholar] [CrossRef]
- Amoah, S.K.; Rodriguez, B.A.; Logothetis, C.N.; Chander, P.; Sellgren, C.M.; Weick, J.P.; Sheridan, S.D.; Jantzie, L.L.; Webster, M.J.; Mellios, N. Exosomal secretion of a psychosis-altered miRNA that regulates glutamate receptor expression is affected by antipsychotics. Neuropsychopharmacology 2020, 45, 656–665. [Google Scholar] [CrossRef]
- Harraz, M.M.; Xu, J.C.; Guiberson, N.; Dawson, T.M.; Dawson, V.L. MiR-223 regulates the differentiation of immature neurons. Mol. Cell Ther. 2014, 2, 18. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Z.; Jinde, S.; Koike, S.; Tada, M.; Satomura, Y.; Yoshikawa, A.; Nishimura, Y.; Takizawa, R.; Kinoshita, A.; Sakakibara, E.; et al. Altered expression of microRNA-223 in the plasma of patients with first-episode schizophrenia and its possible relation to neuronal migration-related genes. Transl. Psychiatry 2019, 9, 289. [Google Scholar] [CrossRef]
- Harraz, M.M.; Eacker, S.M.; Wang, X.; Dawson, T.M.; Dawson, V.L. MicroRNA-223 is neuroprotective by targeting glutamate receptors. Proc. Natl. Acad. Sci. USA 2012, 109, 18962–18967. [Google Scholar] [CrossRef]
- Siegel, G.; Obernosterer, G.; Fiore, R.; Oehmen, M.; Bicker, S.; Christensen, M.; Khudayberdiev, S.; Leuschner, P.F.; Busch, C.J.; Kane, C.; et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 2009, 11, 705–716. [Google Scholar] [CrossRef]
- Moyer, C.E.; Shelton, M.A.; Sweet, R.A. Dendritic spine alterations in schizophrenia. Neurosci. Lett. 2015, 601, 46–53. [Google Scholar] [CrossRef] [PubMed]
- Tatro, E.T.; Risbrough, V.; Soontornniyomkij, B.; Young, J.; Shumaker-Armstrong, S.; Jeste, D.V.; Achim, C.L. Short-term recognition memory correlates with regional CNS expression of microRNA-138 in mice. Am. J. Geriatr. Psychiatry 2013, 21, 461–473. [Google Scholar] [CrossRef] [PubMed]
- Schröder, J.; Ansaloni, S.; Schilling, M.; Liu, T.; Radke, J.; Jaedicke, M.; Schjeide, B.M.; Mashychev, A.; Tegeler, C.; Radbruch, H.; et al. MicroRNA-138 is a potential regulator of memory performance in humans. Front. Hum. Neurosci. 2014, 8, 501. [Google Scholar] [CrossRef]
- Yu, W.; Liang, X.; Li, X.; Zhang, Y.; Sun, Z.; Liu, Y.; Wang, J. MicroRNA-195: A review of its role in cancers. Onco Targets Ther. 2018, 11, 7109–7123. [Google Scholar] [CrossRef]
- Mellios, N.; Huang, H.S.; Grigorenko, A.; Rogaev, E.; Akbarian, S. A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum. Mol. Genet. 2008, 17, 3030–3042. [Google Scholar] [CrossRef] [PubMed]
- Wei, W.; Zhang, W.Y.; Bai, J.B.; Zhang, H.X.; Zhao, Y.Y.; Li, X.Y.; Zhao, S.H. The NF-κB-modulated microRNAs miR-195 and miR-497 inhibit myoblast proliferation by targeting Igf1r, Insr and cyclin genes. J. Cell Sci. 2016, 129, 39–50. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Guo, J.; Zhou, J.; Wang, D.; Kang, X.; Zhou, L. NF-κB maintains the stemness of colon cancer cells by downregulating miR-195-5p/497-5p and upregulating MCM2. J. Exp. Clin. Cancer Res. 2020, 39, 225. [Google Scholar] [CrossRef] [PubMed]
- Ai, J.; Sun, L.H.; Che, H.; Zhang, R.; Zhang, T.Z.; Wu, W.C.; Su, X.L.; Chen, X.; Yang, G.; Li, K.; et al. MicroRNA-195 protects against dementia induced by chronic brain hypoperfusion via its anti-amyloidogenic effect in rats. J. Neurosci. 2013, 33, 3989–4001. [Google Scholar] [CrossRef]
- Liu, C.; Teng, Z.Q.; McQuate, A.L.; Jobe, E.M.; Christ, C.C.; von Hoyningen-Huene, S.J.; Reyes, M.D.; Polich, E.D.; Xing, Y.; Li, Y.; et al. An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation. PLoS ONE 2013, 8, e51436. [Google Scholar] [CrossRef] [PubMed]
- Cao, J.; Huang, M.; Guo, L.; Zhu, L.; Hou, J.; Zhang, L.; Pero, A.; Ng, S.; El Gaamouch, F.; Elder, G.; et al. MicroRNA-195 rescues ApoE4-induced cognitive deficits and lysosomal defects in Alzheimer’s disease pathogenesis. Mol. Psychiatry 2020, 26, 4687–4701. [Google Scholar] [CrossRef] [PubMed]
- Indrieri, A.; Carrella, S.; Carotenuto, P.; Banfi, S.; Franco, B. The Pervasive Role of the miR-181 Family in Development, Neurodegeneration, and Cancer. Int. J. Mol. Sci. 2020, 21, 2092. [Google Scholar] [CrossRef]
- Beveridge, N.J.; Tooney, P.A.; Carroll, A.P.; Gardiner, E.; Bowden, N.; Scott, R.J.; Tran, N.; Dedova, I.; Cairns, M.J. Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum. Mol. Genet. 2008, 17, 1156–1168. [Google Scholar] [CrossRef] [PubMed]
- Casey, S.; Goasdoue, K.; Miller, S.M.; Brennan, G.P.; Cowin, G.; O’Mahony, A.G.; Burke, C.; Hallberg, B.; Boylan, G.B.; Sullivan, A.M.; et al. Temporally Altered miRNA Expression in a Piglet Model of Hypoxic Ischemic Brain Injury. Mol. Neurobiol. 2020, 57, 4322–4344. [Google Scholar] [CrossRef]
- Lai, C.Y.; Yu, S.L.; Hsieh, M.H.; Chen, C.H.; Chen, H.Y.; Wen, C.C.; Huang, Y.H.; Hsiao, P.C.; Hsiao, C.K.; Liu, C.M.; et al. MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS ONE 2011, 6, e21635. [Google Scholar] [CrossRef]
- 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, 827–840. [Google Scholar] [CrossRef]
- Yu, H.C.; Wu, J.; Zhang, H.X.; Zhang, G.L.; Sui, J.; Tong, W.W.; Zhang, X.Y.; Nie, L.L.; Duan, J.H.; Zhang, L.R.; et al. Alterations of miR-132 are novel diagnostic biomarkers in peripheral blood of schizophrenia patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 2015, 63, 23–29. [Google Scholar] [CrossRef]
- Baulina, N.; Osmak, G.; Kiselev, I.; Popova, E.; Boyko, A.; Kulakova, O.; Favorova, O. MiRNAs from DLK1-DIO3 Imprinted Locus at 14q32 are Associated with Multiple Sclerosis: Gender-Specific Expression and Regulation of Receptor Tyrosine Kinases Signaling. Cells 2019, 8, 133. [Google Scholar] [CrossRef]
- Hollins, S.L.; Zavitsanou, K.; Walker, F.R.; Cairns, M.J. Alteration of imprinted Dlk1-Dio3 miRNA cluster expression in the entorhinal cortex induced by maternal immune activation and adolescent cannabinoid exposure. Transl. Psychiatry 2014, 4, e452. [Google Scholar] [CrossRef]
- Ruhrmann, S.; Stridh, P.; Kular, L.; Jagodic, M. Genomic imprinting: A missing piece of the Multiple Sclerosis puzzle? Int. J. Biochem. Cell Biol. 2015, 67, 49–57. [Google Scholar] [CrossRef]
- Andreassen, O.A.; Harbo, H.F.; Wang, Y.; Thompson, W.K.; Schork, A.J.; Mattingsdal, M.; Zuber, V.; Bettella, F.; Ripke, S.; Kelsoe, J.R.; et al. Genetic pleiotropy between multiple sclerosis and schizophrenia but not bipolar disorder: Differential involvement of immune-related gene loci. Mol. Psychiatry 2015, 20, 207–214. [Google Scholar] [CrossRef]
- Carta, M.G.; Moro, M.F.; Lorefice, L.; Trincas, G.; Cocco, E.; Del Giudice, E.; Fenu, G.; Colom, F.; Marrosu, M.G. The risk of Bipolar Disorders in Multiple Sclerosis. J. Affect. Disord. 2014, 155, 255–260. [Google Scholar] [CrossRef]
- Feinstein, A.; Magalhaes, S.; Richard, J.F.; Audet, B.; Moore, C. The link between multiple sclerosis and depression. Nat. Rev. Neurol. 2014, 10, 507–517. [Google Scholar] [CrossRef]
- Arneth, B.M. Multiple Sclerosis and Schizophrenia. Int. J. Mol. Sci. 2017, 18, 1760. [Google Scholar] [CrossRef]
- Schratt, G.M.; Tuebing, F.; Nigh, E.A.; Kane, C.G.; Sabatini, M.E.; Kiebler, M.; Greenberg, M.E. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439, 283–289. [Google Scholar] [CrossRef]
- Rong, H.; Liu, T.B.; Yang, K.J.; Yang, H.C.; Wu, D.H.; Liao, C.P.; Hong, F.; Yang, H.Z.; Wan, F.; Ye, X.Y.; et al. MicroRNA-134 plasma levels before and after treatment for bipolar mania. J. Psychiatr. Res. 2011, 45, 92–95. [Google Scholar] [CrossRef]
- Zhang, H.P.; Liu, X.L.; Chen, J.J.; Cheng, K.; Bai, S.J.; Zheng, P.; Zhou, C.J.; Wang, W.; Wang, H.Y.; Zhong, L.M.; et al. Circulating microRNA 134 sheds light on the diagnosis of major depressive disorder. Transl. Psychiatry 2020, 10, 95. [Google Scholar] [CrossRef]
- Qi, L.; Hongjuan, H.; Ning, G.; Zhengbin, H.; Yanjiang, X.; Tiebo, Z.; Zhijun, H.; Qiong, W. miR-370 is stage-specifically expressed during mouse embryonic development and regulates Dnmt3a. FEBS Lett. 2013, 587, 775–781. [Google Scholar] [CrossRef]
- Lee, S.Y.; Lu, R.B.; Wang, L.J.; Chang, C.H.; Lu, T.; Wang, T.Y.; Tsai, K.W. Serum miRNA as a possible biomarker in the diagnosis of bipolar II disorder. Sci. Rep. 2020, 10, 1131. [Google Scholar] [CrossRef]
- Zhou, M.; Wang, M.; Wang, X.; Liu, K.; Wan, Y.; Li, M.; Liu, L.; Zhang, C. Abnormal Expression of MicroRNAs Induced by Chronic Unpredictable Mild Stress in Rat Hippocampal Tissues. Mol. Neurobiol. 2018, 55, 917–935. [Google Scholar] [CrossRef]
- Rodríguez-Rodríguez, P.; Ramiro-Cortijo, D.; Reyes-Hernández, C.G.; López de Pablo, A.L.; González, M.C.; Arribas, S.M. Implication of Oxidative Stress in Fetal Programming of Cardiovascular Disease. Front. Physiol. 2018, 9, 602. [Google Scholar] [CrossRef]
- Nielsen, R.E.; Banner, J.; Jensen, S.E. Cardiovascular disease in patients with severe mental illness. Nat. Rev. Cardiol. 2021, 18, 136–145. [Google Scholar] [CrossRef]
- Dill, T.L.; Naya, F.J. A Hearty Dose of Noncoding RNAs: The Imprinted DLK1-DIO3 Locus in Cardiac Development and Disease. J. Cardiovasc. Dev. Dis. 2018, 5, 37. [Google Scholar] [CrossRef]
- Lu, Y.; Hou, S.; Huang, D.; Luo, X.; Zhang, J.; Chen, J.; Xu, W. Expression profile analysis of circulating microRNAs and their effects on ion channels in Chinese atrial fibrillation patients. Int. J. Clin. Exp. Med. 2015, 8, 845–853. [Google Scholar]
- Liu, H.; Yang, N.; Fei, Z.; Qiu, J.; Ma, D.; Liu, X.; Cai, G.; Li, S. Analysis of plasma miR-208a and miR-370 expression levels for early diagnosis of coronary artery disease. Biomed. Rep. 2016, 5, 332–336. [Google Scholar] [CrossRef]
- Wang, X.; Jin, H.; Jiang, S.; Xu, Y. MicroRNA-495 inhibits the high glucose-induced inflammation, differentiation and extracellular matrix accumulation of cardiac fibroblasts through downregulation of NOD1. Cell Mol. Biol. Lett. 2018, 23, 23. [Google Scholar] [CrossRef]
- Wu, Y.H.; Zhao, H.; Zhou, L.P.; Zhao, C.X.; Wu, Y.F.; Zhen, L.X.; Li, J.; Ge, D.X.; Xu, L.; Lin, L.; et al. miR-134 Modulates the Proliferation of Human Cardiomyocyte Progenitor Cells by Targeting Meis2. Int. J. Mol. Sci. 2015, 16, 25199–25213. [Google Scholar] [CrossRef]
- Xiao, J.; Jing, Z.C.; Ellinor, P.T.; Liang, D.; Zhang, H.; Liu, Y.; Chen, X.; Pan, L.; Lyon, R.; Liu, Y.; et al. MicroRNA-134 as a potential plasma biomarker for the diagnosis of acute pulmonary embolism. J. Transl. Med. 2011, 9, 159. [Google Scholar] [CrossRef]
- Pape, K.; Tamouza, R.; Leboyer, M.; Zipp, F. Immunoneuropsychiatry-novel perspectives on brain disorders. Nat. Rev. Neurol. 2019, 15, 317–328. [Google Scholar] [CrossRef]
- Radhakrishnan, R.; Kaser, M.; Guloksuz, S. The Link between the Immune System, Environment, and Psychosis. Schizophr. Bull. 2017, 43, 693–697. [Google Scholar] [CrossRef]
- Danese, A.; Moffitt, T.E.; Pariante, C.M.; Ambler, A.; Poulton, R.; Caspi, A. Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Arch. Gen. Psychiatry 2008, 65, 409–415. [Google Scholar] [CrossRef]
- Danese, A.; Pariante, C.M.; Caspi, A.; Taylor, A.; Poulton, R. Childhood maltreatment predicts adult inflammation in a life-course study. Proc. Natl. Acad. Sci. USA 2007, 104, 1319–1324. [Google Scholar] [CrossRef]
- Khandaker, G.M.; Pearson, R.M.; Zammit, S.; Lewis, G.; Jones, P.B. Association of serum interleukin 6 and C-reactive protein in childhood with depression and psychosis in young adult life: A population-based longitudinal study. JAMA Psychiatry 2014, 71, 1121–1128. [Google Scholar] [CrossRef]
- Chiocchetti, A.G.; Haslinger, D.; Stein, J.L.; de la Torre-Ubieta, L.; Cocchi, E.; Rothämel, T.; Lindlar, S.; Waltes, R.; Fulda, S.; Geschwind, D.H.; et al. Transcriptomic signatures of neuronal differentiation and their association with risk genes for autism spectrum and related neuropsychiatric disorders. Transl. Psychiatry 2016, 6, e864. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.Y.; Min, K.; Paik, H.Y.; Lee, S.K. Sex omission and male bias are still widespread in cell experiments. Am. J. Physiol. Cell Physiol. 2021, 320, C742–C749. [Google Scholar] [CrossRef]
- Lopez-Suarez, L.; Awabdh, S.A.; Coumoul, X.; Chauvet, C. The SH-SY5Y human neuroblastoma cell line, a relevant in vitro cell model for investigating neurotoxicology in human: Focus on organic pollutants. Neurotoxicology 2022, 92, 131–155. [Google Scholar] [CrossRef]
- Hoffmann, L.F.; Martins, A.; Majolo, F.; Contini, V.; Laufer, S.; Goettert, M.I. Neural regeneration research model to be explored: SH-SY5Y human neuroblastoma cells. Neural Regen. Res. 2023, 18, 1265–1266. [Google Scholar] [CrossRef]
- Goldie, B.J.; Barnett, M.M.; Cairns, M.J. BDNF and the maturation of posttranscriptional regulatory networks in human SH-SY5Y neuroblast differentiation. Front. Cell Neurosci. 2014, 8, 325. [Google Scholar] [CrossRef]
Condition | miRNA ID | Direction of Change | Previous Reports | ||||
---|---|---|---|---|---|---|---|
New | Old | Diagnosis | Tissue | Direction of Change | Reference (in Smigielski et al. [17]) | ||
Co-treatment | hsa-miR-17-5p | hsa-miR-17 | Down | SZ, SZAD | STG, DLPFC, PFC, serum | Up (brain) and down (serum) | 103, 184, 185, 186, 195 |
hsa-miR-432-5p | hsa-miR-432 | Up | SZ | PBMCs, leukocyte | Down | 191, 192, 204 | |
hsa-miR-106b-5p | hsa-miR-106b | Down | SZ | PFC | Up and down | 179, 180, 185 | |
hsa-miR-30b-5p | hsa-miR-30b | Down | SZ, SZAD | PFC, STG | Up and down | 178, 180, 181 | |
hsa-miR-29c-3p | hsa-miR-29c | Down | SZ, SZAD | PFC exosomes, DLPFC, PFC | Up and down | 103, 170, 180 | |
hsa-miR-328-3p | hsa-miR-328 | Up | SZ, SZAD | STG, DLPFC | Up | 103, 181, 184 | |
hsa-miR-652-3p | hsa-miR-652 | Down | SZ, SZAD | DLPFC, leukocyte, plasma | Up | 184, 192, 199 | |
hsa-miR-33a-5p | hsa-miR-33 | Down | SZ | PFC exosomes, PFC, DLPFC | Up and down | 103, 170, 179 | |
Pre-treatment | hsa-miR-195-5p | hsa-miR-195 | Up | SZ, SZAD | STG, PFC, plasma, whole blood, serum, PBMCs | Up and down | 103, 180, 182, 188, 194, 195, 198 |
hsa-miR-181b-5p | hsa-miR-181b | Up | SZ | STG, DLPFC, whole blood, serum, plasma | Up | 102, 103, 194, 195, 196, 197 | |
hsa-miR-107 | hsa-miR-107 | Up | SZ, SZAD | STG, PFC, DLPFC, PBMCs | Up and down | 103, 123, 184, 191 | |
hsa-miR-432-5p | hsa-miR-432 | Up | SZ | PBMCs, leukocyte | Down | 191, 192, 204 | |
hsa-miR-193b-3p | hsa-miR-193b | Down | SZ | PFC, plasma, whole blood | Up and down | 179, 199, 205 | |
hsa-miR-134-5p | hsa-miR-134 | Down | SZ, SZAD | DLPFC, PBMCs | Up and down | 184, 191, 204 | |
hsa-miR-409-3p | hsa-miR-409-3p | Down | SZ | STG, DLPFC, PBMCs, whole blood | Up and down | 103, 191, 205 | |
hsa-miR-346 | hsa-miR-346 | Down | SZ | DLPFC, serum, plasma | Up and down | 187, 195, 197 |
miRNA | Log2FC | Gardiner et al. [61] | Hollins et al. [63] | Baulina et al. [64] | ||
---|---|---|---|---|---|---|
Significantly Down-Regulated in SZ after Multiple Testing Correction | Average Expression Reduction in SZ, but Insignificant after Multiple Testing Correction | Significant DE in the Left Hemisphere after Multiple Testing Correction | DE in the Left Hemisphere, But Insignificant after Multiple Testing Correction | Significantly Up-Regulated in Male Patients with MS after Multiple Testing Correction | ||
Co-treatment | ||||||
miR-432-5p | 1.3 | ✓ | ✓ | |||
miR-370-3p | 1.2 | ✓ | ✓ | ✓ | ||
miR-485-3p | 1 | ✓ | ✓ | ✓ | ||
miR-495-3p | −1.6 | ✓ | ✓ | ✓ | ||
miR-376b-3p | −1.4 | ✓ | ✓ | ✓ | ||
miR-889-3p | −0.88 | ✓ | ✓ | |||
miR-758-3p | −1.7 | ✓ | ✓ | |||
miR-655-3p | −2 | |||||
miR-496 | −2 | |||||
miR-369-3p | −0.8 | |||||
Pre-Treatment | ||||||
miR-432-5p | 1.3 | ✓ | ✓ | |||
miR-323a-3p | −1.5 | ✓ | ✓ | |||
miR-134-5p | −1.8 | ✓ | ✓ | ✓ | ||
miR-485-5p | −1.9 | ✓ | ✓ | ✓ |
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. |
© 2024 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
Khavari, B.; Barnett, M.M.; Mahmoudi, E.; Geaghan, M.P.; Graham, A.; Cairns, M.J. microRNA and the Post-Transcriptional Response to Oxidative Stress during Neuronal Differentiation: Implications for Neurodevelopmental and Psychiatric Disorders. Life 2024, 14, 562. https://doi.org/10.3390/life14050562
Khavari B, Barnett MM, Mahmoudi E, Geaghan MP, Graham A, Cairns MJ. microRNA and the Post-Transcriptional Response to Oxidative Stress during Neuronal Differentiation: Implications for Neurodevelopmental and Psychiatric Disorders. Life. 2024; 14(5):562. https://doi.org/10.3390/life14050562
Chicago/Turabian StyleKhavari, Behnaz, Michelle M. Barnett, Ebrahim Mahmoudi, Michael P. Geaghan, Adam Graham, and Murray J. Cairns. 2024. "microRNA and the Post-Transcriptional Response to Oxidative Stress during Neuronal Differentiation: Implications for Neurodevelopmental and Psychiatric Disorders" Life 14, no. 5: 562. https://doi.org/10.3390/life14050562