RNA-Sequencing Analysis of 5' Capped RNAs Identifies Many New Differentially Expressed Genes in Acute Hepatitis C Virus Infection
Abstract
:1. Introduction
2. Results
2.1. HCV JFH-1 Infection of Huh 7.5 Cells
2.2. RNA Sequencing (RNA-seq) Analysis of Annotated Gene Transcripts
Ensembl Gene ID | Gene Name | Description | Fold Change | FDR |
---|---|---|---|---|
ENSG00000174951 | FUT1 | Fucosyltransferase 1 | 20.51 | 104.09 |
ENSG00000130487 | KLHDC7B | Kelch domain containing 7 | 18.93 | 141.94 |
ENSG00000136826 | KLF4 | Kruppel-like factor 4 | 15.10 | 142.63 |
ENSG00000128591 | FLNC | Filamin C | 13.38 | 1160.20 |
ENSG00000148677 | ANKRD1 | Ankyrin repeat domain 1 | 12.06 | 351.26 |
ENSG00000205595 | AREG | Amphiregulin | 11.63 | 229.81 |
ENSG00000135842 | C1orf24 | Chromosome 1 open reading frame 24 (C1orf24) | 7.23 | 63.37 |
ENSG00000180535 | MIST1 | Xlass II bHLH protein MIST1 | 6.99 | 84.43 |
ENSG00000136383 | ALPK3 | Alpha-kinase 3 | 6.83 | 202.42 |
ENSG00000139269 | INHBE | Inhibin, beta E | 6.40 | 1324.33 |
ENSG00000107731 | UNC5B | Unc-5 homolog B (C. elegans) | 6.17 | 265.31 |
ENSG00000049323 | LTBP1 | Latent transforming growth factor beta binding protein 1 | 6.14 | 129.49 |
ENSG00000048052 | HDAC9 | Histone deacetylase 9 | 6.09 | 137.83 |
ENSG00000198205 | ZXDA | Zinc finger, X-linked, duplicated A | 6.02 | 47.22 |
ENSG00000111981 | ULBP1 | UL16 binding protein 1 | 6.01 | 37.66 |
ENSG00000130513 | GDF15 | Growth differentiation factor 15 | 5.90 | 958.30 |
ENSG00000122728 | TAF1L | TAF1-like RNA polymerase II, TATA box binding protein (TBP)-associated factor | 5.54 | 41.06 |
ENSG00000138670 | RASGEF1B | RasGEF domain family, member 1B | 5.41 | 39.54 |
ENSG00000176971 | LOC387758 | Similar to RIKEN cDNA 1110018M03 | 5.39 | 23.55 |
ENSG00000160999 | APS | Adaptor protein with pleckstrin homology and src homology 2 domains | 5.18 | 22.09 |
ENSG00000006327 | TNFRSF12A | Fucosyltransferase 1 | 5.13 | 286.27 |
ENSG00000184545 | DUSP8* | Dual specificity phosphatase 8 | 5.05 | 87.30 |
ENSG00000130766 | SESN2 | Sestrin 2 | 4.84 | 593.42 |
ENSG00000070669 | ASNS | Asparagine synthetase | 4.80 | 577.30 |
ENSG00000136997 | MYC | v-myc myelocytomatosis viral oncogene homolog | 4.71 | 991.67 |
ENSG00000168679 | SLC16A4 | Solute carrier family 16 (monocarboxylic acid transporters), member 4 | 4.65 | 24.23 |
ENSG00000099889 | ARVCF | Armadillo repeat gene deletes in velocardiofacial syndrome | 4.53 | 240.65 |
ENSG00000162772 | ATF3* | Activating transcription factor 3 | 4.47 | 695.61 |
ENSG00000106948 | AKNA | AT-hook transcription factor | 4.45 | 773.28 |
ENSG00000167861 | C17orf28 | Chromosome 17 open reading frame 28 | 4.43 | 142.87 |
ENSG00000138685 | FGF2 | Fibroblast growth factor 2 | 4.08 | 23.78 |
ENSG00000105327 | BBC3 | BCL2 binding component 3 | 4.06 | 230.60 |
ENSG00000111087 | GLI1 | Glioma-associated oncogene homolog 1 (zinc finger protein) | 4.02 | 41.66 |
ENSG00000065911 | MTHFD2 | Methylenetetrahydrofolate dehydrogenase (NADP+ dependent) 2, | 4.00 | 693.07 |
ENSG00000115520 | COQ10B | Coenzyme Q10 homolog B (S. cerevisiae) | 3.96 | 22.43 |
ENSG00000105499 | PLA2G4C* | Phospholipase A2, group IVC (cytosolic, calcium-independent) | 3.92 | 44.14 |
ENSG00000065600 | TMEM206 | Transmembrane protein 206 | 3.90 | 57.11 |
ENSG00000108551 | RASD1 | RAS, dexamethasone-induced 1 | 3.89 | 70.16 |
ENSG00000152137 | HSPB8 | Heat shock 22kDa protein 8 | 3.87 | 64.97 |
ENSG00000112182 | BACH2 | BTB and CNC homology 1, basic leucine zipper transcription factor 2 | 3.83 | 76.67 |
ENSG00000157765 | SLC34A2 | Homo sapiens cDNA FLJ90534 fis, highly similar to Homo sapiens sodium dependent phosphate transporter isoform NaPi-3b mRNA | 3.80 | 41.45 |
ENSG00000163393 | SLC22A15 | Solute carrier family 22 (organic cation transporter), member 15 | 3.77 | 104.50 |
ENSG00000168003 | SLC3A2 | Solute carrier family 3 (activators of dibasic and neutral amino acid transport), member 2 | 3.77 | 1977.88 |
ENSG00000164949 | GEM | GTP binding protein overexpressed in skeletal muscle (GEM) | 3.71 | 51.70 |
ENSG00000107281 | NPDC1 | Neural proliferation, differentiation and control, 1 | 3.68 | 38.82 |
ENSG00000154025 | SLC5A10 | Solute carrier family 5 (sodium/glucose cotransporter), member 10 | 3.67 | 50.35 |
ENSG00000196517 | SLC6A9 | Solute carrier family 6 (neurotransmitter transporter, glycine), member 9 | 3.65 | 153.70 |
ENSG00000166173 | LARP6 | La ribonuleoprotein domain family, member 6 | 3.62 | 146.96 |
ENSG00000184371 | CSF1 | Colony stimulating factor 1 (macrophage) | 3.58 | 132.33 |
ENSG00000120129 | DUSP1 | Dual specificity phosphatase 1 (DUSP1) | 3.53 | 446.22 |
Ensembl Gene ID | Gene Name | Description | Fold Change | FDR | Time Point |
---|---|---|---|---|---|
ENSG00000196475 | GK2 | Glycerol kinase 2 | −17.49 | −22.37 | 72 h |
ENSG00000164588 | HCN1 | Hyperpolarization activated cyclic nucleotide-gated potassium channel 1 | −15.64 | −23.39 | 6 h |
ENSG00000101438 | SLC32A1 | Solute carrier family 32 (GABA vesicular transporter), member 1 | −9.34 | −68.18 | 72 h |
ENSG00000178695 | KCTD12 | Potassium channel tetramerisation domain containing 12 | −8.10 | −41.92 | 6 h |
ENSG00000182687 | GALR2 | Galanin receptor 2 | −6.23 | −17.14 | 6 h |
ENSG00000120738 | EGR1 | Early growth response 1 | −5.33 | −259.33 | 6 h |
ENSG00000170989 | EDG1 | Endothelial differentiation, sphingolipid G-protein-coupled receptor, 1 | −4.20 | −21.82 | 72 h |
ENSG00000186074 | NKIR | NK inhibitory receptor precursor | −4.10 | −17.18 | 72 h |
ENSG00000153266 | ZNF312 | Zinc finger protein 312 | −3.91 | −116.99 | 6 h |
ENSG00000143595 | AQP10 | Aquaporin 10 | −3.32 | −97.38 | 72 h |
ENSG00000153266 | ZNF312 | Zinc finger protein 312 | −3.01 | −71.64 | 72 h |
ENSG00000167183 | PRR15L | Proline rich 15-like | −2.95 | −39.58 | 72 h |
ENSG00000131470 | TBPIP | TBP-1 interacting protein (TBPIP) | −2.80 | −17.88 | 6 h |
ENSG00000134389 | CFHL5 | Complement factor H-related 5 | −2.72 | 0.37 | 48 h |
ENSG00000156475 | PPP2R2B | Protein phosphatase 2, regulatory subunit B (PR 52) | −2.65 | −26.85 | 72 h |
ENSG00000159261 | CLDN14 | Claudin 14 (CLDN14) | −2.58 | −26.90 | 72 h |
ENSG00000186910 | SERPINA11 | Serpin peptidase inhibitor, clade A (alpha-1 antiproteinase, antitrypsin) | −2.53 | −25.05 | 72 h |
ENSG00000182782 | GPR109A | G protein-coupled receptor 109A | −2.50 | −29.16 | 72 h |
ENSG00000182782 | GPR109B | G protein-coupled receptor 109B | −2.50 | −29.16 | 72 h |
ENSG00000197711 | HP | Haptoglobin | −2.42 | −291.19 | 72 h |
ENSG00000197711 | HPR | Haptoglobin-related protein | −2.42 | −291.19 | 72 h |
ENSG00000130427 | EPO | Erythropoietin | −2.39 | −44.50 | 72 h |
ENSG00000143224 | PPOX | Protoporphyrinogen oxidase | −2.37 | −15.81 | 6 h |
ENSG00000162344 | FGF19 | Fibroblast growth factor 19 | −2.31 | −40.79 | 6 h |
2.3. Changes in Kegg Pathways during Acute HCV Infection
KEGG Pathway name | Genes in Pathway | 6 h | 48 h | 72 h | |||
---|---|---|---|---|---|---|---|
DEGs (EGs) | p value | DEGs (EGs) | p value | DEGs (EGs) | p value | ||
MAPK signaling | 268 | 5 (168) | 0.003 | 13 (173) | 0.01 | 33 (177) | 0.0005 |
Cytokine-cytokine receptor interaction | 265 | 9 (90) | 0.005 | 19 (92) | 0.002 | ||
Antigen processing and presentation | 78 | 2 (36) | 0.02 | ||||
RIG-I-like receptor signaling | 71 | 12 (44) | 0.001 | ||||
Toll-like receptor signaling | 102 | 11 (58) | 0.03 | ||||
NOD-like receptor signaling | 59 | 9 (40) | 0.02 | ||||
Cytosolic DNA-sensing pathway | 56 | 7 (28) | 0.02 | ||||
Epithelial cell signaling in H. pylori infection | 68 | 11 (53) | 0.01 | ||||
Adipocytokine signaling | 68 | 7 (50) | 0.002 | 13 (48) | 0.0008 | ||
TGF-beta signaling | 85 | 6 (68) | 0.03 | 13 (55) | 0.02 | ||
Regulation of autophagy | 34 | 5 (18) | 0.03 | ||||
Apoptosis | 89 | 12 (68) | 0.04 | ||||
ECM-receptor interaction | 85 | 4 (37) | 0.04 | ||||
Jak-STAT signaling | 155 | 15 (77) | 0.01 | ||||
Hepatitis C | 135 | 20 (98) | 0.002 | ||||
mTOR signaling | 52 | 2 (41) | 0.02 | ||||
Hedgehog signaling | 56 | 5 (30) | 0.004 | ||||
Notch signaling | 47 | 9 (37) | 0.01 | ||||
Renal cell carcinoma | 70 | 2 (58) | 0.04 | ||||
Basal cell carcinoma | 55 | 4 (31) | 0.02 | ||||
Hematopoietic cell lineage | 88 | 4 (29) | 0.02 | ||||
Osteoclast differentiation | 128 | 7 (76) | 0.02 | 19 (76) | 0.0001 | ||
Insulin signaling | 138 | 19 (110) | 0.01 | ||||
Type II diabetes mellitus | 48 | 4 (27) | 0.01 | ||||
Aminoacyl tRNA biosynthesis | 63 | 13 (41) | 0.0001 | ||||
Ribosome biogenesis in eukaryotes | 81 | 12 (44) | 0.001 | ||||
Sphingolipid metabolism | 40 | 9 (33) | 0.005 | ||||
Glutathione metabolism | 50 | 2 (39) | 0.03 | ||||
Cyanoamino acid metabolism | 7 | 1 (4) | 0.02 | ||||
Ubiquinone and other terpenoid-quinone biosynthesis | 7 | 1 (5) | 0.03 | ||||
Taurine and hypotaurine metabolism | 10 | 1 (5) | 0.03 | ||||
Neurotophin signaling | 127 | 18 (94) | 0.006 | ||||
One carbon pool by folate | 18 | 5 (17) | 0.03 | ||||
Prion diseases | 36 | 2 (21) | 0.006 |
2.4. RNA Sequencing Analysis of 5' Capped RNA Identifies Upregulated Unannotated Pol II Transcripts
GENOME POSITION | ||||||||
---|---|---|---|---|---|---|---|---|
Chr | Start | Stop | Total BPs | HCV RPKM | MOCK RPKM | Fold Change | FDR | Time point |
8 | 47528429 | 47529270 | 841 | 7.74 | 0.93 | 7.52 | 113.0 | 72 h |
5 | 85865845 | 85866626 | 781 | 10.08 | 3.37 | 2.92 | 57.2 | 72 h |
4 | 1384494 | 1385183 | 689 | 6.10 | 2.27 | 2.59 | 21.4 | 72 h |
8 | 87354779 | 87355196 | 417 | 7.95 | 3.04 | 2.50 | 14.7 | 72 h |
16 | 31580193 | 31580636 | 443 | 10.55 | 4.19 | 2.44 | 21.4 | 72 h |
17 | 7967452 | 7968557 | 1105 | 6.15 | 2.62 | 2.33 | 101.1 | 48 h |
16 | 21513065 | 21513758 | 693 | 8.71 | 3.94 | 2.17 | 21.9 | 72 h |
15 | 64995200 | 64995463 | 263 | 31.29 | 15.07 | 2.07 | 95.1 | 48 h |
11 | 122489643 | 122489913 | 270 | 9.48 | 4.76 | 1.97 | 18.1 | 48 h |
14 | 65747331 | 65747885 | 554 | 11.64 | 6.17 | 1.86 | 15.4 | 72 h |
2.4. Effect of Gene Silencing of Selected Upregulated Genes on HCV JFH-1 Replication and Infectious Virus Production
3. Discussion
3.1. Acute HCV Infection Reprograms Gene Transcription of Infected Cells
3.2. Acute HCV Infection Related Kegg Pathways
3.3. HCV and Cellular Glycosylation Pathways
3.4. KLDC7B Gene Silencing Inhibits HCV Replication
4. Experimental Procedures
4.1. Cell Culture
4.2. Production of Infectious HCV
4.3. Infection of Cells with HCV JFH1
4.4. RNA Isolation
4.5. RNA Sequencing
4.6. Bioinformatics
4.7. Real-Time PCR (qPCR)
4.9. RNA Interference
4.10. Quantification of Infectious HCV Virions and HCV RNA
5. Conclusions
Acknowledgments
Funding
Conflict of Interest
References and Notes
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Papic, N.; Maxwell, C.I.; Delker, D.A.; Liu, S.; Heale, B.S.E.; Hagedorn, C.H. RNA-Sequencing Analysis of 5' Capped RNAs Identifies Many New Differentially Expressed Genes in Acute Hepatitis C Virus Infection. Viruses 2012, 4, 581-612. https://doi.org/10.3390/v4040581
Papic N, Maxwell CI, Delker DA, Liu S, Heale BSE, Hagedorn CH. RNA-Sequencing Analysis of 5' Capped RNAs Identifies Many New Differentially Expressed Genes in Acute Hepatitis C Virus Infection. Viruses. 2012; 4(4):581-612. https://doi.org/10.3390/v4040581
Chicago/Turabian StylePapic, Neven, Christopher I. Maxwell, Don A. Delker, Shuanghu Liu, Bret S. E. Heale, and Curt H. Hagedorn. 2012. "RNA-Sequencing Analysis of 5' Capped RNAs Identifies Many New Differentially Expressed Genes in Acute Hepatitis C Virus Infection" Viruses 4, no. 4: 581-612. https://doi.org/10.3390/v4040581