Full-text resources of PSJD and other databases are now available in the new Library of Science.
Visit https://bibliotekanauki.pl

PL EN


Preferences help
enabled [disable] Abstract
Number of results
2016 | 63 | 4 | 789-798

Article title

RNA-Seq-based analysis of differential gene expression associated with hepatitis C virus infection in a cell culture

Content

Title variants

Languages of publication

EN

Abstracts

EN
Hepatitis C virus (HCV) infection is one of the major causes of chronic liver diseases. Unfortunately, the mechanisms of HCV infection-induced liver injury and host-virus interactions are still not well recognized. To better understand these processes we determined the changes in the host gene expression that occur during HCV infection of Huh-7.5 cells. As a result, we identified genes that may contribute to the immune and metabolic cellular responses to infection. Pathway enrichment analysis indicated that HCV induced an increased expression of genes involved in mitogen-activated protein kinases signaling, adipocytokine signaling, cell cycle and nitrogen metabolism. In addition, the enrichment analyses of processes and molecular functions revealed that the up-regulated genes were mainly implicated in the negative regulation of phosphorylation. Construction of the pathway-gene-process network enabled exploration of a much more complex landscape of molecular interactions. Consequently, several essential processes altered by HCV infection were identified: negative regulation of cell cycle, response to endoplasmic reticulum stress, response to reactive oxygen species, toll-like receptor signaling and pattern recognition receptor signaling. The analyses of genes whose expression was decreased upon HCV infection showed that the latter were engaged in the metabolism of lipids and amino acids. Moreover, we observed disturbance in the cellular antiviral defense. Altogether, our results demonstrated that HCV infection elicits host response that includes a very wide range of cellular mechanisms. Our findings significantly broaden the understanding of complex processes that accompany HCV infection. Consequently, they may be used for developing new host-oriented therapeutic strategies.

Keywords

EN

Year

Volume

63

Issue

4

Pages

789-798

Physical description

Dates

published
2016
received
2016-06-01
revised
2016-06-24
accepted
2016-07-13
(unknown)
2016-10-25

Contributors

  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
author
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Computing Science, Poznan University of Technology, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Computing Science, Poznan University of Technology, Poznań, Poland
  • Institut Pasteur, Unité Hepacivirus et Immunité Innée, CNRS, URA 3015, Département de Virologie, Paris, France
  • Institut Pasteur, Unité Hepacivirus et Immunité Innée, CNRS, URA 3015, Département de Virologie, Paris, France
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Computing Science, Poznan University of Technology, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Chemical Technology and Engineering, Poznan University of Technology, Poznań, Poland

References

  • Anders S, Pyl PT, Huber W (2015) HTSeq - a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169. https://doi.org/10.1093/bioinformatics/btu638.
  • Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93: 1019-1137. https://doi.org/10.1152/physrev.00028.2012.
  • Baoying W (2014) Big Data Analytics in Bioinformatics and Healthcare. IGI Global.
  • Benedicto I, Molina-Jiménez F, Moreno-Otero R, López-Cabrera M, Majano PL (2011) Interplay among cellular polarization, lipoprotein metabolism and hepatitis C virus entry. World J Gastroenterol WJG 17: 2683-2690. https://doi.org/10.3748/wjg.v17.i22.2683.
  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300
  • Bianco A, Reghellin V, Donnici L, Fenu S, Alvarez R, Baruffa C, Peri F, Pagani M, Abrignani S, Neddermann P, De Francesco R (2012) Metabolism of Phosphatidylinositol 4-Kinase IIIα-Dependent PI4P Is Subverted by HCV and Is Targeted by a 4-Anilino Quinazoline with Antiviral Activity. PLoS Pathog 8: e1002576. https://doi.org/10.1371/journal.ppat.1002576.
  • Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ (2010) Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis c virus. J Virol 84: 5404-5414. https://doi.org/10.1128/JVI.02529-09.
  • Carnero E, Fortes P (2016) HCV infection, IFN response and the coding and non-coding host cell genome. Virus Res 212: 85-102. https://doi.org/10.1016/j.virusres.2015.10.001.
  • Cerutti A, Maillard P, Minisini R, Vidalain PO, Roohvand F, Pecheur EI, Pirisi M, Budkowska A (2011) Identification of a Functional, CRM-1-Dependent Nuclear Export Signal in Hepatitis C Virus Core Protein. PLOS ONE 6: e25854. https://doi.org/10.1371/journal.pone.0025854.
  • Chan SW (2014) The unfolded protein response in virus infections. Front Microbiol 5: 518. https://doi.org/10.3389/fmicb.2014.00518.
  • Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR, Ma'ayan A (2013) Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14: 128. https://doi.org/10.1186/1471-2105-14-128.
  • Domingo E, Sheldon J, Perales C (2012) Viral Quasispecies Evolution. Microbiol Mol Biol Rev 76: 159-216. https://doi.org/10.1128/MMBR.05023-11.
  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8: 175-185.
  • Farci P (2011) New insights into the HCV quasispecies and compartmentalization. Semin Liver Dis 31: 356-374. https://doi.org/10.1055/s-0031-1297925.
  • Figlerowicz M, Jackowiak P, Formanowicz P, Kędziora P, Alejska M, Malinowska N, Błażewicz J, Figlerowicz M (2010) Hepatitis C virus quasispecies in chronically infected children subjected to interferon-ribavirin therapy. Arch Virol 155: 1977-1987. https://doi.org/10.1007/s00705-010-0789-7.
  • Galbraith JW, Franco RA, Donnelly JP, Rodgers JB, Morgan JM, Viles AF, Overton ET, Saag MS, Wang HE (2015) Unrecognized chronic hepatitis C virus infection among baby boomers in the emergency department. Hepatology 61: 776-782. https://doi.org/10.1002/hep.27410.
  • Gene Ontology Consortium (2015) Gene Ontology Consortium: going forward. Nucleic Acids Res 43: D1049-1056. https://doi.org/10.1093/nar/gku1179.
  • Ghany MG, Strader DB, Thomas DL, Seeff LB (2009) Diagnosis, management, and treatment of hepatitis C: An update. Hepatology 49: 1335-1374. https://doi.org/10.1002/hep.22759.
  • Gokhale NS, Vazquez C, Horner SM (2014) Hepatitis C virus. Strategies to evade antiviral responses. Future Virol 9: 1061-1075. https://doi.org/10.2217/fvl.14.89.
  • Grünvogel O, Esser-Nobis K, Reustle A, Schult P, Müller B, Metz P, Trippler M, Windisch MP, Frese M, Binder M, Fackler O, Bartenschlager R, Ruggieri A, Lohmann V (2015) DDX60L is an interferon-stimulated gene product restricting hepatitis C virus replication in cell culture. J Virol 89: 10548-10568. https://doi.org/10.1128/JVI.01297-15.
  • Howell J, Angus P, Gow P, Visvanathan K (2013) Toll-like receptors in hepatitis C infection: Implications for pathogenesis and treatment. J Gastroenterol Hepatol 28: 766-776. https://doi.org/10.1111/jgh.12170.
  • Ishida H, Kato T, Takehana K, Tatsumi T, Hosui A, Nawa T, Kodama T, Shimizu S, Hikita H, Hiramatsu N, Kanto T, Hayashi N, Takehara T (2013) Valine, the branched-chain amino acid, suppresses hepatitis C virus RNA replication but promotes infectious particle formation. Biochem Biophys Res Commun 437: 127-133. https://doi.org/10.1016/j.bbrc.2013.06.051.
  • Jackowiak P, Figlerowicz M, Kurzynska-Kokorniak A, Figlerowicz M (2011) Mechanisms involved in the development of chronic hepatitis C as potential targets of antiviral therapy. Curr Pharm Biotechnol 12: 1774-1780.
  • Jackowiak P, Kowala-Piaskowska A, Figlerowicz M, Alejska M, Malinowska N, Figlerowicz M (2012) Evolution of hepatitis C virus hypervariable region 1 in chronically infected children. Virus Res 167: 380-384. https://doi.org/10.1016/j.virusres.2012.05.005.
  • Jackowiak P, Kuls K, Budzko L, Mania A, Figlerowicz M, Figlerowicz M (2014) Phylogeny and molecular evolution of the hepatitis C virus. Infect Genet Evol 21: 67-82. https://doi.org/10.1016/j.meegid.2013.10.021.
  • Jongeneel CV, Iseli C, Stevenson BJ, Riggins GJ, Lal A, Mackay A, Harris RA, O'Hare MJ, Neville AM, Simpson AJ, Strausberg RL (2003) Comprehensive sampling of gene expression in human cell lines with massively parallel signature sequencing. Proc Natl Acad Sci U S A 100: 4702-4705. https://doi.org/10.1073/pnas.0831040100.
  • Kurzynska-Kokorniak A, Koralewska N, Pokornowska M, Urbanowicz A, Tworak A, Mickiewicz A, Figlerowicz M (2015) The many faces of Dicer: the complexity of the mechanisms regulating Dicer gene expression and enzyme activities. Nucleic Acids Res 43: 4365-4380. https://doi.org/10.1093/nar/gkv328.
  • Larrat S, Vallet S, David-Tchouda S, Caporossi A, Margier J, Ramière C, Scholtes C, Haïm-Boukobza S, Roque-Afonso AM, Besse B, André-Garnier E, Mohamed S, Halfon P, Pivert A, LeGuillou-Guillemette H, Abravanel F, Guivarch M, Mackiewicz V, Lada O, Mourez T, Plantier JC, Baazia Y, Alain S, Hantz S, Thibault V, Gaudy-Graffin C, Bouvet D, Mirand A, Henquell C, Gozlan J, Lagathu G, Pronier C, Velay A, Schvoerer E, Trimoulet P, Fleury H, Bouvier-Alias M, Brochot E, Duverlie G, Maylin S, Gouriou S, Pawlotsky JM, Morand P (2015) Naturally occurring resistance-associated variants of hepatitis C virus protease inhibitors in poor responders to pegylated interferon-ribavirin. J Clin Microbiol 53: 2195-2202. https://doi.org/10.1128/JCM.03633-14.
  • Ledergerber C, Dessimoz C (2011) Base-calling for next-generation sequencing platforms. Brief Bioinform 12: 489-497. https://doi.org/10.1093/bib/bbq077.
  • Liang TJ, Ghany MG (2013) Current and future therapies for hepatitis C virus infection. N Engl J Med 368: 1907-1917. https://doi.org/10.1056/NEJMra1213651.
  • Lindenbach BD, Evans MJ, Syder AJ, Wölk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626. https://doi.org/10.1126/science.1114016.
  • Maillard P, Walic M, Meuleman P, Roohvand F, Huby T, Goff WL, Leroux-Roels G, Pécheur EI, Budkowska A (2011) Lipoprotein lipase inhibits hepatitis C virus (HCV) infection by blocking virus cell entry. PLOS ONE 6: e26637. https://doi.org/10.1371/journal.pone.0026637.
  • Malumbres M, Harlow E, Hunt T, Hunter T, Lahti JM, Manning G, Morgan DO, Tsai LH, Wolgemuth DJ (2009) Cyclin-dependent kinases: a family portrait. Nat Cell Biol 11: 1275-1276. https://doi.org/10.1038/ncb1109-1275.
  • Marinov GK, Williams BA, McCue K, Schroth GP, Gertz J, Myers RM, Wold BJ (2014) From single-cell to cell-pool transcriptomes: Stochasticity in gene expression and RNA splicing. Genome Res 24: 496-510. https://doi.org/10.1101/gr.161034.113.
  • Marukian S, Andrus L, Sheahan TP, Jones CT, Charles ED, Ploss A, Rice CM, Dustin LB (2011) Hepatitis C virus induces interferon-λ and interferon-stimulated genes in primary liver cultures. Hepatology 54: 1913-1923. https://doi.org/10.1002/hep.24580.
  • Mee CJ, Farquhar MJ, Harris HJ, Ramma W, Ahmed A, Maurel P, Bicknell R, Balfe P, McKeating JA (2010) Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor dependent manner. Gastroenterology 138: 1134-1142. https://doi.org/10.1053/j.gastro.2009.11.047.
  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. https://doi.org/10.1038/nmeth.1226.
  • Oshiumi H, Miyashita M, Okamoto M, Morioka Y, Okabe M, Matsumoto M, Seya T (2015) DDX60 Is involved in RIG-I-dependent and independent antiviral responses, and its function is attenuated by virus-induced EGFR activation. Cell Rep 11: 1193-1207. https://doi.org/10.1016/j.celrep.2015.04.047.
  • Papic N, Maxwell CI, Delker DA, Liu S, Heale BS, Hagedorn CH (2012) RNA-sequencing analysis of 5' capped RNAs identifies many new differentially expressed genes in acute hepatitis C virus infection. Viruses 4: 581-612. https://doi.org/10.3390/v4040581.
  • Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123. https://doi.org/10.1093/nar/gkp596.
  • Rehermann B (2016) HCV in 2015: Advances in hepatitis C research and treatment. Nat Rev Gastroenterol Hepatol 13: 70-72. https://doi.org/10.1038/nrgastro.2015.227.
  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140. https://doi.org/10.1093/bioinformatics/btp616.
  • Roux PP, Blenis J (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344. https://doi.org/10.1128/MMBR.68.2.320-344.2004.
  • Safran M, Dalah I, Alexander J, Rosen N, Iny Stein T, Shmoish M, Nativ N, Bahir I, Doniger T, Krug H, Sirota-Madi A, Olender T, Golan Y, Stelzer G, Harel A, Lancet D (2010) GeneCards Version 3: the human gene integrator. Database (Oxford) 2010: baq020. https://doi.org/10.1093/database/baq020.
  • Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27: 863-864. https://doi.org/10.1093/bioinformatics/btr026.
  • Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM (2011) A diverse array of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485. https://doi.org/10.1038/nature09907.
  • Simmonds P (2013) The origin of hepatitis C virus. Curr Top Microbiol Immunol 369: 1-15. https://doi.org/10.1007/978-3-642-27340-7_1.
  • Sultan M, Dökel S, Amstislavskiy V, Wuttig D, Sültmann H, Lehrach H, Yaspo ML (2012) A simple strand-specific RNA-Seq library preparation protocol combining the Illumina TruSeq RNA and the dUTP methods. Biochem Biophys Res Commun 422: 643-646. https://doi.org/10.1016/j.bbrc.2012.05.043.
  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111. https://doi.org/10.1093/bioinformatics/btp120.
  • Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Kräusslich HG, Mizokami M, Bartenschlager R, Liang TJ (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796. https://doi.org/10.1038/nm1268.
  • Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081-1086. https://doi.org/10.1126/science.1209038.
  • Walters KA, Syder AJ, Lederer SL, Diamond DL, Paeper B, Rice CM, Katze MG (2009) Genomic analysis reveals a potential role for cell cycle perturbation in HCV-mediated apoptosis of cultured hepatocytes. PLoS Pathog 5: e1000269. https://doi.org/10.1371/journal.ppat.1000269.
  • Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, Benali S, Bourlière M (2014) Chronic hepatitis C: future treatment. Clin Pharmacol 6: 1-17. https://doi.org/10.2147/CPAA.S30338.
  • Wilson GK, Stamataki Z (2012) In Vitro systems for the study of hepatitis C virus infection. Int J Hepatol 2012: 292591. https://doi.org/10.1155/2012/292591.
  • Woodhouse SD, Narayan R, Latham S, Lee S, Antrobus R, Gangadharan B, Luo S, Schroth GP, Klenerman P, Zitzmann N (2010) Transcriptome sequencing, microarray, and proteomic analyses reveal cellular and metabolic impact of hepatitis C virus infection in vitro. Hepatology 52: 443-453. https://doi.org/10.1002/hep.23733.
  • Yuan YC, Wu X, Warden C (2013) Optimal Calculation of RNA-Seq Fold-Change Values. Int J Comput Bioinforma Silico Model 2: 285-292. Retrieved from. https://www.researchgate.net/publication/258629398_Optimal_Calculation_of_RNA-Seq_Fold-Change_Values
  • Zeisel MB, Lupberger J, Fofana I, Baumert TF (2013) Host-targeting agents for prevention and treatment of chronic hepatitis C - Perspectives and challenges. J Hepatol 58: 375-384. https://doi.org/10.1016/j.jhep.2012.09.022.
  • Zhang H (2016) Overview of Sequence Data Formats. Methods Mol Biol 1418: 3-17. https://doi.org/10.1007/978-1-4939-3578-9_1.
  • Zhao W, He X, Hoadley KA, Parker JS, Hayes DN, Perou CM (2014) Comparison of RNA-Seq by poly (A) capture, ribosomal RNA depletion, and DNA microarray for expression profiling. BMC Genomics 15: 419. https://doi.org/10.1186/1471-2164-15-419.

Document Type

Publication order reference

Identifiers

YADDA identifier

bwmeta1.element.bwnjournal-article-abpv63p789kz
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.