PMCID
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Samples were mounted on glass slides and analyzed by epifluorescence (Olympus IX81 S1F-3, cellM software) and confocal (spinning-disc PerkinElmer UltraView VoX, Velocity software) microscopes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For quantification of phenotype frequencies, at least 100 transfected cells were counted.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Pseudotyped viruses were generated in HEK293T cells as described .
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Briefly, the plasmid driving the expression of the shRNA transgene was transfected into cells using Lipofectamine 2000 (Invitrogen) together with other lentiviral packaging plasmids coding for Gag, Pol Tat Rev, and the VSV-G envelope.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Transfections were done in a 10cm format, and the supernatant containing the virus was harvested 72 hours post-transfection, filtered through a 0.45 μm filter spun at 2000 rpm for 5 min to remove cells debrides and stored at -80°C.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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2x10 Jurkat T cells were transduced with the pseudotyped particles for transduction.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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16 hours later, the medium containing lentiviral particles was changed.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Following transduction, cells were cultured in a medium supplemented with 2 μg/ml of puromycin to eliminate non-transduced cells that did not express shRNA.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Upon the death of all the control cells, the medium was changed, and surviving cells were propagated for future experiments.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For transducing CD4 primary cells, we used HIVGKO (a gift from Eric Verdin), which codes for a codon-optimized GFP reporter under the control of the HIV-1 promoter and in the context of expression of all viral proteins and a mKO2 reporter under the control of the constitutive promoter EF1α .
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For knockdown (KD) of CYTOR expression, J-Lat 6.3 cells were transduced with lentiviruses that drive the expression of shRNA that specifically targets CYTOR.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were next selected on puromycin, and polyclonal stable cells were monitored for CYTOR expression by RT-qPCR.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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To achieve CYTOR over-expression, cells were transduced with a lentivirus that drives the expression of CYTOR—exons 1, 4 and 5, the most abundantly expressed form in humans.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Following antibiotic selection, resistant J-Lat 6.3 T cells were subjected to RT-qPCR to confirm CYTOR over-expression or knockdown.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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CYTOR RNA levels were normalized to the gapdh gene.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Although we are aware that GAPDH expression is elevated following TCR stimulation, we did analyze several cellular genes in search of a better marker, but concluded that, e.g., genes for actin polymerization machinery are all affected more strongly by T cell activation than gapdh .
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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We therefore used gapdh for normalization.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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To obtain CYTOR knockdown in stimulated primary CD4+ T cells, cells were isolated from health donors (n = 3) and stimulated with anti-CD3/CD28 beads (1:1 ratio of beads to cell number).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were cultured on stimulation media (RPMI+IL2), and on day 3 post isolation and stimulation, cells were subjected to transduction with lentivirus expressing shRNA against CYTOR.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The following day cells were transduced with HIVGKO and 48 hour later were analyzed by FACS for HIV-GFP and mKO2 expression.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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To monitor the effects of CYTOR in promoting HIV latency, we followed the kinetics of entry of stimulated Jurkat 2D10 T cells that express a cassette of the HIV provirus, expressing 2dGFP reporter.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells where CYTOR is depleted or over-expressed and control cells that express scramble shRNA were activated with P/I and then sorted by FACS to isolate those that express GFP.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were then grown, during which their HIV GFP expression was followed by FACS.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Control cells expressing scramble shRNA or cells where CYTOR expression was depleted (KD) were cross-linked with 1% formaldehyde for 10 minutes and then washed with PBS and reverse cross-linked with glycine (125mM; 5 minutes).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were then lysed for 10 minutes on ice in 130μl sonication buffer (20 mM Tris pH-7.8, 2 mM EDTA, 0,5% SDS, 0.5 mM phenylmethylsulfonyl fluoride (PMSF), and 1% protease inhibitor cocktail), and the nuclear pellets were collected.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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DNA was fragmented by sonication at the following settings: amplitude 20% for 30 cycles at 10 seconds on/10 seconds off.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Samples were centrifuged (15 minutes, 14,000 rpm, 4°C).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The soluble chromatin fraction (25 μg) was collected and immunoprecipitated (IP) overnight at 4°C on a rotating wheel in IP buffer (0.5% Triton X-100, 2 mM EDTA, 20 mM Tris pH-7.8, 150 mM NaCl and 10% glycerol) with 2.5 μg of one of the indicated antibodies.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The next day, the IP material was incubated with 25 μl dynabeads protein G for two hours to ensure the binding of the antibody to the magnetic beads.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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DNA was eluted with freshly prepared elution solution (1% SDS and 0.1 M NaHCO3) and heated at 65°C overnight to reverse-crosslink the samples.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Precipitated DNA fragments were then extracted using a ChIP DNA clean and concentrator kit (ZYMO Research), and HIV DNA levels were quantified by qPCR with the primers specifically located on the NFκB region at the HIV-LTR promoter.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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All signals were normalized relative to input DNA.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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ChIP assays were also performed with an anti-rabbit or mouse IgG as negative control.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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3x10 cells were cross-linked with freshly made 1% formaldehyde in PBS for 10 minutes at room temperature while shaking.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Crosslinking was quenched with 125 μM glycine for 5 minutes at room temperature.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were centrifuged at 1200 rpm for 5 minutes at 4°C and washed twice with PBS on ice.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The pellet was re-suspended in 300 μl of sonication buffer (50mM Tris 7.0, 10mM EDTA, 1% SDS, DTT, PMSF, protease inhibitors (Roche), and RNase inhibitor (NEB).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were then incubated on ice for 10 minutes and sonicated in Bioruptor at high settings of 3 rounds each of 10 cycles 40 seconds ON/40 seconds OFF.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Water was changed to ice-cold between the rounds.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Sociated samples were centrifuged at max speed for 10 minutes at 4°C, and then chromatin material was kept at -80°C.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For IP, chromatin was diluted in twice the volume of hybridization buffer (500 mM, NaCl, 1% SDS, 100 mM Tris pH-8, 10 mM EDTA, 15% Formamide, protease inhibitors (Roche) and RNase inhibitor (NEB).2 μg of biotinylated RNA was added to 0.5 ml diluted chromatin and mixed by end-to-end rotation at 37°C for 4 hours.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Streptavidin-magnetic beads were washed three times in sonication buffer, blocked with 500 ng/μl yeast total RNA and 1 mg/ml BSA for 1 hour at room temperature before resuspended in their original volume.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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40 μl of beads were added, and the reaction was incubated for 30 minutes at 37°C.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Beads were captured by a magnet and washed five times with the wash buffer (2x SSC, 0.5% SDS, supplemented with fresh DTT and PMSF).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Beads were resuspended in 3-times of the original volume with the DNA elution buffer (50 mM NaHCO3, 1% SDS, 200 mM NaCl), and DNA was eluted with a cocktail of 100 μg/ml RNaseA (Sigma) and 0.1 U/μl RNase H (Epicenter).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Chromatin was reverse-cross-by treatment with 0.2 U/μl proteinase K at 65°C for 45 minutes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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DNA was then extracted with an equal volume of phenol:chloroform: isoamyl alcohol(Invitrogen) and precipitated with ethanol at -80°C overnight.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For probe in-vitro transcription of linear RNA synthesis, 1 μg of RNA was transcribed and biotinylated using AmpliScribe-T7-Flashbiotin-RNA transcription kit (Epicentre) according to the manufacturer’s instructions.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Eluted DNA was analyzed by qPCR with primers specific to the HIV promoter.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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10 Jurkat J-Lat 6.3 cells were washed twice with PBS and resuspended in 800 μl of RNA-IP buffer (0.5% NP-40, 20 mM HEPES pH 7.8, 100 mM KCl, 0.2 mM EDTA supplemented with RNase inhibitor (NEB) and protease inhibitor (Sigma).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Cells were cross-linked, and cell lysate was incubated on ice for 10 minutes before isolating nuclei through centrifugation at 2500g for 15 minutes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The supernatant was collected and resuspended in freshly prepared RIP buffer.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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ChIP material was then sonicated, and the pelleted nuclear membrane and debris were removed by centrifugation at 13,000 rpm for 10 minutes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Isolated ChIP material was incubated with 2.5 μg of indicated antibodies overnight at 4°C.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Then, 20 μl of pre-blocked BSA protein A beads were added and incubated for an additional 2 hours at 4°C.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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50 μl of cell lysate was collected as input samples.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Beads were washed 4 times with washing buffer (0.5% NP-40, 20 mM HEPES pH 7.8, 100 mM KCl, 0.2 mM EDTA supplemented with RNase inhibitor (NEB) and protease inhibitor (Sigma) to remove unbound material.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The pellet was resuspended in 100 μl of the lysis buffer and extracted using a TRIZOL reagent (Sigma).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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RNA was reverse transcribed using qPCRBIO kit (PCPbiosystems), and qPCR was performed using indicated primers against CYTOR or 7SK ncRNA.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The amplification of 7SL RNA served as a control RNA that is not associated with P-TEFb.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Input RNA was extracted and reverse-transcribed the same way.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Dilutions of input were used for standard curve and calculations.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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10 Jurkat cells were washed twice with PBS and resuspended in 800 μl of RNA-pull-down buffer (0.5% NP-40, 20 mM HEPES pH 7.8, 100 mM KCl, 0.2 mM EDTA supplemented with RNase inhibitor (NEB) and protease inhibitor (Sigma).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Lysates were incubated with an in-vitro transcribed biotinylated CYTOR anti-sense probe (synthesized by IDT), and reactions were pulled down with streptavidin beads.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Beads were resuspended in 3 times of their original volume of DNase buffer (100 mM NaCl and 0.1% NP-40), and protein was eluted with a cocktail of 100 μg/ml RNaseA (Sigma) and 0.1 U/μl RNaseH (Epicenter) and 100 U/ml DNase I (Invitrogen) at 37°C for 30 minutes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Eluted proteins were subjected to western blotting with indicated antibodies.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Non-specific IgG served as control.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Biotinylated scrambled RNA was used as a control for RNA-IP.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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7SK RNA confirmed association with P-TEFb.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Input is 5% of the total cell lysate .
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The cytosolic extracts were prepared by resuspending 3x10 cells in 500μl of Buffer A (10 mM KCl, 10 mM MgCl2, 10 mM HEPES, 1 mM EDTA, 1 mM DTT, 0.1% PMSF, and EDTA-free complete protease inhibitor cocktail (Roche) with 0.5% NP-40 for 10 minutes on ice.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The nuclei were spun down at 5,000 g for 5 minutes, and the supernatant was saved as the cytosolic extract (CE).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The nuclei were washed once with 200 μl of Buffer A with 0.5% NP-40 and re-pelleted.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The nuclei were resuspended in 100 μl of Buffer B (450 mM NaCl, 1.5 mM MgCl2, 20 mM HEPES, 0.5 mM EDTA, 1 mM DTT, 0.1% PMSF, and EDTA-free complete protease inhibitor cocktail (Roche) and incubated on ice for 60 minutes.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The lysates were clarified by centrifugation at 20,000g for 10 minutes to prepare nuclear extract (NE).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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RNA from nuclear or cytoplasmic was extracted with Trizol, and RNA was reverse transcribed using a qPCRBIO kit (PCPbiosystems), and qPCR was performed using indicated primers against CYTOR or 7SK ncRNA.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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CYTOR and 7SK RNA levels were normalized to 7SL RNA in each of the fractions and conditions.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For identifying ncRNAs that are differentially expressed upon T cell stimulation in cells that carry active HIV (GFP+) versus latent HIV (GFP-), J-Lat 6.3 cells were stimulated with P/I and sorted based on their GFP expression (n = 4).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For analysis of transcriptome upon CYTOR depletion cells, primary CD4+ T cells were stimulated with CD3/CD28 beads and then subjected to CYTOR KD by transducing cells with lentivirus that drive the expression of shRNA that target CYTOR (n = 3).
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PMC11075828
|
Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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CYTOR overexpression was obtained by transducing stimulated cells with lentivirus that drive CYTOR expression.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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RNA was purified utilizing the RNeasy Mini kit (QIAGEN) according to the manufacturer’s instructions.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The integrity of the isolated RNA was tested using the Agilent High Sensitivity RNA Kit and Tapestation 4200 at the Genome Technology Center at the Faculty of Medicine Bar-Ilan University.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Total RNA was used for mRNA enrichment by using the NEBNext mRNA polyA Isolation Module (NEB; E7490L), and libraries for Illumina sequencing were performed using the NEBNext Ultra II RNA kit (NEB; E7770L).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Quantification of the library was performed using dsDNA HS Assay Kit and Qubit 2.0 (Molecular Probes, Life Technologies), and qualification was done using the Agilent D1000 Tapestation Kit and Tapestation 4200.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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150 nM of each library was pooled together and was diluted to 4nM according to NextSeq manufacturer’s instructions.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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1.6 pM was loaded onto the Flow Cell with 1% PhiX library control.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Libraries were sequenced on an Illumina NextSeq 500 instrument, 75 cycles of single-read sequencing.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For analysis: Quality Control was conducted by evaluating the quality of the FASTQ files using ’Fastqc’ (v0.12.1).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Subsequently, the samples underwent quality trimming via the ’Fastp’ software (v0.23.3).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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To identify potential contaminations, ’fastq-screen’ software was applied.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Read alignment involved aligning the reads to the Human GRCh38 genome (Ensembl release 110) using ’STAR’ software (v2.7.10b).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Read assignments to coding regions were determined using the ’SubRead’ package (’FeatureCounts’ v2.0.6).
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Finally, BAM files were sorted using ‘samtools’.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Differential expression analysis was conducted in DAVID.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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PCA was performed to evaluate data dispersion, revealing a batch effect among samples collected on different dates.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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A correction was implemented in the DESeq2 model to minimize this batch effect.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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Finally, the indicated groups were compared (without including the control in the model), identifying 90 DEGs.
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PMC11075828
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Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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The selected cutoff values were an adjusted p-value <0.05 and a fold-change > 2.
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PMC11075828
|
Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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For enrichment analysis, the DAVID program was employed to identify enriched pathways and terms associated with the selected genes .
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PMC11075828
|
Direct and indirect effects of CYTOR lncRNA regulate HIV gene expression.
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These quality control and data analysis steps ensure the reliability and accuracy of the RNA-seq analysis.
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