scholarly journals MicroRNA and their target mRNAs change expression in whole blood of patients after intracerebral hemorrhage

2019 ◽  
Vol 40 (4) ◽  
pp. 775-786 ◽  
Author(s):  
Xiyuan Cheng ◽  
Bradley P Ander ◽  
Glen C Jickling ◽  
Xinhua Zhan ◽  
Heather Hull ◽  
...  
Keyword(s):  
Intracerebral Hemorrhage ◽  
Whole Blood ◽  
Killer Cell ◽  
Transcriptome Profiling ◽  
Rna Degradation ◽  
Differentially Expressed ◽  
Mrna Levels ◽  
Target Mrnas ◽  
Mrna Targets ◽  
Differentially Expressed Mirnas

Previous studies showed changes in mRNA levels in whole blood of rats and humans, and in miRNA in whole blood of rats following intracerebral hemorrhage (ICH). Thus, this study assessed miRNA and their putative mRNA targets in whole blood of humans following ICH. Whole transcriptome profiling identified altered miRNA and mRNA levels in ICH patients compared to matched controls. Target mRNAs of the differentially expressed miRNAs were identified, and functional analysis of the miRNA-mRNA targets was performed. Twenty-nine miRNAs (22 down, 7 up) and 250 target mRNAs (136 up, 114 down), and 7 small nucleolar RNA changed expression after ICH compared to controls (FDR < 0.05, and fold change ≥ |1.2|). These included Let7i, miR-146a-5p, miR210-5p, miR-93-5p, miR-221, miR-874, miR-17-3p, miR-378a-5p, miR-532-5p, mir-4707, miR-4450, mir-1183, Let-7d-3p, miR-3937, miR-4288, miR-4741, miR-92a-1-3p, miR-4514, mir-4658, mir-3689d-1, miR-4760-3p, and mir-3183. Pathway analysis showed regulated miRNAs/mRNAs were associated with toll-like receptor, natural killer cell, focal adhesion, TGF-β, phagosome, JAK-STAT, cytokine–cytokine receptor, chemokine, apoptosis, vascular smooth muscle, and RNA degradation signaling. Many of these pathways have been implicated in ICH. The differentially expressed miRNA and their putative mRNA targets and associated pathways may provide diagnostic biomarkers as well as point to therapeutic targets for ICH treatments in humans.

scholarly journals Whole Blood Transcriptome Analysis in Children with Sickle Cell Anemia

2022 ◽  
Vol 12 ◽  
Author(s):  
Beatrice E. Gee ◽  
Andrea Pearson ◽  
Iris Buchanan-Perry ◽  
Roger P. Simon ◽  
David R. Archer ◽  
...  
Keyword(s):  
Gene Expression ◽  
Rna Sequencing ◽  
Sickle Cell ◽  
Sickle Cell Anemia ◽  
Whole Blood ◽  
Differentially Expressed ◽  
Mrna Levels ◽  
Control Subjects ◽  
Non Coding Rna ◽  
And Control

Whole transcriptome RNA-sequencing was performed to quantify RNA expression changes in whole blood samples collected from steady state sickle cell anemia (SCA) and control subjects. Pediatric SCA and control subjects were recruited from Atlanta (GA)—based hospital(s) systems and consented for RNA sequencing. RNA sequencing was performed on an Ion Torrent S5 sequencer, using the Ion Total RNA-seq v2 protocol. Data were aligned to the hg19 reference genome and analyzed in the Partek Genomics studio package (v7.0). 223 genes were differentially expressed between SCA and controls (± 1.5 fold change FDR p &lt; 0.001) and 441 genes show differential transcript expression (± 1.5 fold FDR p &lt; 0.001). Differentially expressed RNA are enriched for hemoglobin associated genes and ubiquitin-proteasome pathway genes. Further analysis shows higher gamma globin gene expression in SCA (33-fold HBG1 and 49-fold HBG2, both FDR p &lt; 0.05), which did not correlate with hemoglobin F protein levels. eQTL analysis identified SNPs in novel non-coding RNA RYR2 gene as having a potential regulatory role in HBG1 and HBG2 expression levels. Gene expression correlation identified JHDM1D-AS1(KDM7A-DT), a non-coding RNA associated with angiogenesis, enhanced GATA1 and decreased JAK-STAT signaling to correlate with HBG1 and HBG2 mRNA levels. These data suggest novel regulatory mechanisms for fetal hemoglobin regulation, which may offer innovative therapeutic approaches for SCA.

Immunoglobulin-Like Transcript 2 (ILT2) Is Not Differentially Expressed in MGUS and Myeloma, but Appears To Be Downregulated at an Earlier Stage of Plasma Cell Disease.

Blood ◽  
2006 ◽  
Vol 108 (11) ◽  
pp. 5039-5039
Author(s):  
Martin Schreder ◽  
Wolfgang Huebl ◽  
Gudrun Koch ◽  
Kathrin Strasser-Weippl ◽  
Niklas Zojer ◽  
...  
Keyword(s):  
Differential Expression ◽  
Plasma Cell ◽  
Plasma Cells ◽  
Killer Cell ◽  
Differentially Expressed ◽  
Expression Level ◽  
Prognostic Impact ◽  
Clinical Parameters ◽  
Mrna Levels ◽  
Normal Plasma

Abstract Background: Immunoglobulin-like transcript 2 (ILT2/CD85j) belongs to the Ig superfamily and has homology to the killer cell inhibitory receptors (KIRs). It is expressed on natural killer (NK) cells, monocytes, macrophages, dendritic cells and (naive) B lymphocytes. A differential expression of ILT2 was described for monoclonal gammopathy of undetermined significance (MGUS) and multiple myeloma (MM). Gene expression profiling studies found ILT2 to be downregulated 8.26 fold in myeloma as compared to MGUS, being the most differentially expressed gene between these two subsets. However, as RNA from CD138+ cells was used in this analysis, a varying percentage of normal, non-malignant plasma cells will impact on the results, especially in MGUS cases. Aims: We aimed to delineate ILT2 expression in different plasma cell subsets (normal compared to monoclonal cells) in MGUS and MM and the eventual prognostic impact of a differential expression level. Methods: ILT2 expression was measured by flow cytometry using a PE-conjugated antibody (clone HP-F1, Beckman Coulter) in a series of 30 MGUS patients and 91 myeloma patients. Phenotypically normal and malignant plasma cells were defined by differential expression of CD38, CD45, CD19 and CD56. Expression levels are given as mean fluorescence intensity (MFI) after correction for background staining. Results: ILT2 was not differentially expressed in monoclonal plasma cells from patients with MGUS (MFI median 112.0, range 13.5–274.4) and myeloma (MFI median 96.6, range 0.4–454.5). In contrast, monoclonal cells from MGUS and MM showed a significantly lower expression of ILT2 as compared to phenotypically normal plasma cells in the majority of samples (p=0.007). Results were confirmed by quantitative real time PCR studies in 25 MM patients showing a linear correlation of ILT2 mRNA levels with the intensity of ILT2 protein expression. ILT2 levels did not vary with state of disease and showed no correlation with clinical parameters or prognosis in our series of myeloma patients. Conclusions: In the majority of patients with monoclonal plasma cell disorders, ILT2 seems to be downregulated at an early stage of disease, i.e. upon transformation from a normal plasma cell to the MGUS/MM stage. The expression level of ILT2 in monoclonal plasma cells is neither correlated with the state of disease (MGUS versus newly diagnosed myeloma versus advanced disease) nor to prognosis of myeloma patients or other clinical parameters.

scholarly journals Gene expression profiling in whole blood of patients with coronary artery disease

2010 ◽  
Vol 119 (8) ◽  
pp. 335-343 ◽  
Author(s):  
Chiara Taurino ◽  
William H. Miller ◽  
Martin W. McBride ◽  
John D. McClure ◽  
Raya Khanin ◽  
...  
Keyword(s):  
Gene Expression ◽  
Coronary Artery Disease ◽  
Coronary Artery ◽  
Gene Expression Profiling ◽  
Whole Blood ◽  
Expression Profiling ◽  
Gene Expression Analysis ◽  
Differentially Expressed ◽  
Differentially Expressed Mirnas ◽  
Artery Disease

Owing to the dynamic nature of the transcriptome, gene expression profiling is a promising tool for discovery of disease-related genes and biological pathways. In the present study, we examined gene expression in whole blood of 12 patients with CAD (coronary artery disease) and 12 healthy control subjects. Furthermore, ten patients with CAD underwent whole-blood gene expression analysis before and after the completion of a cardiac rehabilitation programme following surgical coronary revascularization. mRNA and miRNA (microRNA) were isolated for expression profiling. Gene expression analysis identified 365 differentially expressed genes in patients with CAD compared with healthy controls (175 up- and 190 down-regulated in CAD), and 645 in CAD rehabilitation patients (196 up- and 449 down-regulated post-rehabilitation). Biological pathway analysis identified a number of canonical pathways, including oxidative phosphorylation and mitochondrial function, as being significantly and consistently modulated across the groups. Analysis of miRNA expression revealed a number of differentially expressed miRNAs, including hsa-miR-140-3p (control compared with CAD, P=0.017), hsa-miR-182 (control compared with CAD, P=0.093), hsa-miR-92a and hsa-miR-92b (post- compared with pre-exercise, P<0.01). Global analysis of predicted miRNA targets found significantly reduced expression of genes with target regions compared with those without: hsa-miR-140-3p (P=0.002), hsa-miR-182 (P=0.001), hsa-miR-92a and hsa-miR-92b (P=2.2×10−16). In conclusion, using whole blood as a ‘surrogate tissue’ in patients with CAD, we have identified differentially expressed miRNAs, differentially regulated genes and modulated pathways which warrant further investigation in the setting of cardiovascular function. This approach may represent a novel non-invasive strategy to unravel potentially modifiable pathways and possible therapeutic targets in cardiovascular disease.

scholarly journals Mir-671-5p, Mir-193b-5p, Mir-1307-5p Are Useful for Predicting Outcome in Diffuse Large B-Cell Lymphoma

Blood ◽  
2021 ◽  
Vol 138 (Supplement 1) ◽  
pp. 2399-2399
Author(s):  
Aditi Sharma ◽  
Ashim Das ◽  
Amanjit Bal ◽  
Radhika Srinivasan ◽  
Pankaj Malhotra ◽  
...  
Keyword(s):  
Progression Free Survival ◽  
B Cell Lymphoma ◽  
Transcriptome Profiling ◽  
Roc Curves ◽  
Differentially Expressed ◽  
Free Survival ◽  
Large B Cell Lymphoma ◽  
Differentially Expressed Mirnas ◽  
Pre Treatment

Abstract Background: Diffuse large B-cell Lymphoma (DLBCL) is stratified histologically as GCB and ABC phenotypes based on Hans algorithm. Besides this categorization, there is a paucity of molecular markers useful for predicting response to CHOP/R-CHOP chemotherapy and outcome of DLBCL patients. We performed miRNA profiling to identify potential miRNAs for their ability to predict response to chemotherapy and outcome in DLBCL patients. Methods: A total of 41 cases of histologically and immunohistochemically confirmed DLBCL cases who received R-CHOP/CHOP were included in this study after IRB approval. The follow up ranged from 7 to 2273 days with a mean of, 874 days. Cases in sustained complete remission for ≥ 1095 days were identified as "responders" whereas cases with partial response/stable disease or primary progressive disease were identified as"non-responders". In the first part of the study, miRNA transcriptome profiling was performed from lymph node tissue of 10 cases of DLBCL which included 3 responders and 7 non-responders (3 with refractory disease and 4 with relapse) for identification and selection of differentially expressed miRNAs. Total RNA was isolated from the biopsies, libraries constructed with ION TOTAL RNA-SEQ v2 and sequenced on S5 ION Torrent. The filtered reads were aligned to the reference genome hg19 using Bowtie. Differentially expressed miRNAs were identified by DESeq2. In the second part of the study, validation of the selected miRNAs was performed in a retrospective validation cohort of 41 cases including 17 responders and 24 non-responders by semi-quantitative qRT-PCR. ROC curves were obtained and best cut-off for the delta Ct values was selected for each of the miRNAs to distinguish the two cohorts of patients. In the third part of the study, an additional 38 cases of DLBCL were included prospectively as testing cohort, in whom mi-RNA were isolated from paired pre-treatment biopsy and plasma samples were evaluated for the expression of the selected miRNAs for prediction of response to treatment and outcome. Results: miRNA transcriptome profiling revealed a total of 30 differentially expressed miRNAs among DLBCL responders vs non-responders and the data was submitted to GEO database (GSE179760). The top 4 significantly downregulated miRNAs in non-responders selected for validation included miR-193b-5p, miR-671-5p, miR-1307-5p and miR-326 as shown in the volcano plot and heatmap in Fig.1. In-silico prediction for the interacting genes of the selected miRNAs revealed genes involved in lymphoma progression and chemoresistance . Validation by qRT-PCR revealed significant down-regulation of miR-1307-5p, miR-671-5p and miR-193b-5p in the non-responders compared to responders (Fig.2). There was no significant association of miRNA expression with disease stage, nodal or extranodal origin and the presence of B symptoms. However, the downregulation of miR-671-5p was found to be associated with the presence of B-symptoms. Downregulation of miR-193b-5p, miR-671-5p, miR-1307-5p expression showed a significant association with progression free survival as shown in Fig.3 (Spearman's correlation plot and Kaplan-Meier survival curves). In the prospective cohort of 38 DLBCL patients, all 3 miRNAs were expressed in cell free plasma and tissue but only miRNA-193b-5p showed correlation between them. Using the cut-off Ct values obtained from ROC curves of tissue miRNA levels in the validation cohort , 16/38 patients were predicted to be non-responders. The preliminary data showed that 8 of these 16 cases were correctly predicted (6 died of disease, 2 showed partial response). The remaining cases are still under follow-up. The treatment response could not be predicted on the corresponding plasma levels. Conclusion: Downregulation of miRNA-671-5p, miR-193b-5p and miR-1307-5p in pre-treatment biopsy samples is associated with poor outcome and shorter progression free survival and poor treatment response leading to refractory/relapse DLBCL, which needs confirmation in larger studies. Figure 1 Figure 1. Disclosures No relevant conflicts of interest to declare.

scholarly journals Global Transcriptome Profiling Identifies a Key Mir-185-PAK6 Axis That Promotes Survival of Leukemic Stem Cells and Drug-Insensitive Blasts in BCR-ABL+ Human Leukemia

Blood ◽  
2018 ◽  
Vol 132 (Supplement 1) ◽  
pp. 931-931
Author(s):  
Andrew Wu ◽  
Lin Hanyang ◽  
Katharina Rothe ◽  
Min Chen ◽  
Jens Ruschmann ◽  
...  
Keyword(s):  
Expression Profiles ◽  
Transcriptome Profiling ◽  
Differentially Expressed ◽  
Leukemic Stem Cells ◽  
Cd34 Cells ◽  
Differentially Expressed Mirnas ◽  
Resistant Cells

Abstract Chronic myeloid leukemia (CML) stem/progenitor cells and BCR-ABL+ acute lymphoblastic leukemia (ALL) blast cells are insensitive to tyrosine kinase inhibitor (TKI) monotherapies. These cells rapidly generate therapy-resistant clones in vitro and in vivo and are often responsible for disease relapse. Therefore, identification of predictive biomarkers and novel treatments that target key molecular events active in leukemic stem cells (LSCs) are needed. MicroRNAs (miRNAs) are small molecules that regulate the gene expression network and are highly deregulated in many cancers. Through global transcriptome profiling, we have recently identified 66 differentially expressed miRNAs in pre-treatment CD34+ stem/progenitor cells from CML patients (n=6) compared to healthy bone marrow (NBM) controls (n=3, adjusted P<0.05); 26 differentially expressed miRNAs were identified between subsequent IM-nonresponders and IM-responders (P<0.05). 21 differentially expressed miRNAs were successfully validated in additional IM-responders (n=11), IM-nonresponders (n=11) and NBM (n=11). Interestingly, miR-185 was discovered to be one of the most highly deregulated miRNAs, with significant reduction in CD34+ cells from IM-nonresponders compared to IM-responders (p=0.0006). This significant change was further demonstrated in CD34+ cells from CML patients (n=60) before and after 3-month TKI nilotinib treatment in a clinical trial (p<0.05). We further demonstrated that miR-185 functions as a tumor suppressor; its restored expression by lentiviral transduction in CD34+ IM-nonresponder cells significantly impaired survival of these cells and sensitized them to TKI treatment in vitro. Restored miR-185 expression in BCR-ABL+ ALL blasts led to a profound decrease in leukemia burden and significantly enhanced survival compared to controls in vivo (median survival 65 vs. 47 days, P=0.0005). Strikingly, mice injected with miR-185-transduced cells and treated with dasatinib (DA) survived much longer than recipients of control cells treated with DA (median survival 83 vs. 60 days, P=0.0018). Moreover, restoration of miR-185 expression combined with DA treatment greatly reduced in vivo long-term regenerative activity of LSCs from IM-nonresponders as compared to control cells treated with DA in NRG mice (<0.2% vs. 5% GFP+ patient cells in the BM, 25 weeks post-transplantation). We observed not only a marked reduction in GFP+CD34+ cells, but also a near elimination of GFP+CD34+CD38- LSCs that were transduced with miR-185 and treated with DA compared to control cells treated with DA, indicating that restored miR-185 expression combined with DA preferentially prevents the growth of patient-derived long-term leukemia-initiating cells in vivo. Several miRNA target genes were further identified by integrating miRNA expression profiles with gene expression profiles from the same patient samples using strand-specific RNA-seq. Based on three out of six prediction algorithms (mirBase, TargetScan, miRanda, tarBase, mirTarget2, and PicTar), PAK6, a serine/threonine-protein kinase, was found to be highly expressed in CD34+ IM-nonresponder cells compared to IM-responders (p<0.003), which correlated with reduced expression of miR-185 in these cells (p=0.0002). PAK6 was confirmed as a target gene of miR-185 by a luciferase reporter assay. Western blot analysis showed that restored miR-185 expression caused a marked decrease in protein levels of PAK6 in miR-185-transduced cells and suppression of PAK6 reduced viability of these cells. These results indicate that PAK6 is a critical target of miR-185, and that loss of miR-185 expression in CML may lead to up-regulation of PAK6, which in turn contributes to disease progression and drug resistance. Indeed, the use of a pre-clinically validated pan PAK inhibitor (PF-3758309) significantly inhibited the growth of IM-resistant cells and CD34+ IM-nonresponder cells and these effects could be enhanced by TKIs (p<0.05). Mechanistically, we observed that p-ERK and p-AKT were significantly reduced in PAK6 knockdown or miR185-restored IM-resistant cells in response to IM treatment. Thus, we infer that downregulation of PAK6 may sensitize TKI-resistant cells to TKI therapy through inhibition of the RAS/MAPK pathway. Taken together, PAK6, a novel target of miR-185, emerges as an attractive druggable target for combination therapy of TKI-resistant patients. Disclosures No relevant conflicts of interest to declare.

scholarly journals Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition

2020 ◽  
Author(s):  
Luis Enrique Cabrera Quio ◽  
Alexander Schleiffer ◽  
Karl Mechtler ◽  
Andrea Pauli
Keyword(s):  
Regulation Of Gene Expression ◽  
Physiological Role ◽  
Transcriptome Profiling ◽  
Time Frame ◽  
Rna Degradation ◽  
Developmental Transitions ◽  
Mrna Targets ◽  
Go Enrichment ◽  
Normal Adults

AbstractPost-transcriptional mechanisms are crucial for the regulation of gene expression. These mechanisms are particularly important during rapid developmental transitions such as the oocyte-to-embryo transition, which is characterized by dramatic changes to the developmental program in the absence of nuclear transcription. Under these conditions, changes to the RNA content are solely dependent on RNA degradation. Although several mechanisms that promote RNA decay during embryogenesis have been identified, it remains unclear which cellular machineries contribute to remodeling the maternal transcriptome during the oocyte-to-embryo transition. Here, we focused on the auxiliary 3’-to-5’ degradation factor Ski7 in zebrafish as its mRNA peaks during this time frame. Homozygous ski7 mutant fish were viable and developed into morphologically normal adults, yet they had decreased fertility. Consistent with the idea that Ski7 participates in remodeling the transcriptome during the oocyte-to-embryo transition, transcriptome profiling identified stage-specific mRNA targets of Ski7. Genes upregulated in ski7 mutants were generally lowly expressed in wild type, suggesting that Ski7 maintains low transcript levels for this subset of genes. GO enrichment analyses of genes mis-regulated in ski7 mutants implicated Ski7 in the regulation of redox processes. This was confirmed experimentally by an increased resistance of ski7 mutant embryos to reductive stress. Overall, our results provide first insights into the physiological role of vertebrate Ski7 as an important post-transcriptional regulator during the oocyte-to-embryo transition.

scholarly journals miRNA Expression Profile and Effect of Wenxin Granule in Rats with Ligation-Induced Myocardial Infarction

2017 ◽  
Vol 2017 ◽  
pp. 1-10 ◽  
Author(s):  
Aiming Wu ◽  
Lixia Lou ◽  
Jianying Zhai ◽  
Dongmei Zhang ◽  
Limin Chai ◽  
...  
Keyword(s):  
Myocardial Infarction ◽  
Expression Profile ◽  
Mirna Expression ◽  
Mirna Expression Profile ◽  
Differentially Expressed ◽  
Coronary Artery Ligation ◽  
Mrna Levels ◽  
Artery Ligation ◽  
Gene Level ◽  
Differentially Expressed Mirnas

Wenxin Granule (WXKL) is a traditional Chinese medicine used for treatment of myocardial infarction (MI) and arrhythmias. However, the genomic pathological mechanisms of MI and mechanisms of WXKL are largely unknown. This study aims to investigate a comprehensive miRNA expression profile, and the predicted correlation pathways to be targeted by differentially expressed miRNAs in MI, and mechanisms of WXKL from a gene level. MI rat model was established by a coronary artery ligation surgery. miRNA expression microarrays were performed and the data were deposited in Gene Expression Omnibus (GEO number GSE95855). And, pathway analysis was performed by using the DIANA-miRPath v3.0 online tool. The expressions of miR-1, miR-133, Cx43, and Cx45 were detected by quantitative real-time PCR. It was found that 35 differentially expressed miRNAs and 23 predicted pathways, including miR-1, miR-133, and gap junction pathway, are involved in the pathogenesis of MI. And, WXKL increased the expressions of miR-1 and miR-133, while also increased the mRNA levels of Cx43 and Cx45, and, especially, recovered the Cx43/Cx45 ratio near to normal level. The results suggest that regulatory effects on miR-1, miR-133, Cx43, and Cx45 might be a possible mechanism of WXKL in the treatment of MI at the gene level.

scholarly journals Effects of Castration on miRNA, lncRNA, and mRNA Profiles in Mice Thymus

Genes ◽  
2020 ◽  
Vol 11 (2) ◽  
pp. 147
Author(s):  
Bingxin Li ◽  
Kaizhao Zhang ◽  
Yaqiong Ye ◽  
Jingjing Xing ◽  
Yingying Wu ◽  
...  
Keyword(s):  
Gene Networks ◽  
Gonadal Hormones ◽  
Differentially Expressed ◽  
Thymic Epithelial Cells ◽  
Mrna Levels ◽  
Rna Seq ◽  
Thymic Development ◽  
Promoter Sequences ◽  
Differentially Expressed Mirnas ◽  
Non Coding Rnas

Thymic degeneration and regeneration are regulated by estrogen and androgen. Recent studies have found that long non-coding RNAs (lncRNAs) and microRNAs (miRNAs) are involved in organ development. In this study, RNA sequencing (RNA-seq) results showed that ovariectomy significantly affected 333 lncRNAs, 51 miRNAs, and 144 mRNAs levels (p < 0.05 and |log2fold change| > 1), and orchiectomy significantly affected 165 lncRNAs, 165 miRNAs, and 208 mRNA levels in the thymus. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that differentially expressed genes (DEGs) were closely related to cell development and immunity. Next, we constructed two lncRNA–miRNA–mRNA networks using Cytoscape based on the targeting relationship between differentially expressed miRNAs (DEMs) and DEGs and differentially expressed lncRNAs (DELs) analyzed by TargetScan and miRanda. Besides, we screened DEGs that were significantly enriched in GO and in ceRNA networks to verify their expression in thymocytes and thymic epithelial cells (TECs). In addition, we analyzed the promoter sequences of DEGs, and identified 25 causal transcription factors. Finally, we constructed transcription factor-miRNA-joint target gene networks. In conclusion, this study reveals the effects of estrogen and androgen on the expression of miRNAs, lncRNAs, and mRNAs in mice thymus, providing new insights into the regulation of thymic development by gonadal hormones and non-coding RNAs.

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