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RNASeq analysis of differentiated keratinocytes reveals a massive response to late events during human papillomavirus type 16 infection, including loss of epithelial barrier function.
The human papillomavirus (HPV) replication cycle is tightly linked to epithelial cell differentiation. To examine HPV-associated changes in the keratinocyte transcriptome, RNAs isolated from undifferentiated and differentiated cell populations of normal, spontaneously immortalised, keratinocytes (NIKS), and NIKS stably transfected with HPV16 episomal genomes (NIKS16), were compared using RNASeq. HPV16 infection altered expression of 2862 cellular genes. Next, to elucidate the role of keratinocyte gene expression in late events during the viral life cycle, RNASeq was carried out on triplicate differentiated populations of NIKS (uninfected) and NIKS16 (infected). Of the top 966 genes altered (>log = 1.8, 3.5-fold change) 670 genes were downregulated and 296 genes were up-regulated. HPV down-regulated many genes involved in epithelial barrier function that involves structural resistance to the environment and immunity to infectious agents. For example, HPV infection repressed expression of the differentiated keratinocyte-specific pattern recognition receptor TLR7, the Langerhans cell chemoattractant, CCL20, and proinflammatory cytokines, IL1A and IL1B. However, IRF1, IFNκ and viral restriction factors (IFIT1, 2, 3, 5, OASL, CD74, RTP4) were up-regulated. HPV infection abrogated gene expression associated with the physical epithelial barrier, including keratinocyte cytoskeleton, intercellular junctions and cell adhesion. qPCR and western blotting confirmed changes in expression of seven of the most significantly altered mRNAs. Expression of three genes showed statistically significant changes during cervical disease progression in clinical samples. Taken together, the data indicate that HPV infection manipulates the differentiating keratinocyte transcriptome to create an environment conducive to productive viral replication and egress. Human papillomavirus (HPV) genome amplification and capsid formation takes place in differentiated keratinocytes. The viral life cycle is intimately associated with host cell differentiation. Deep sequencing (RNASeq) of RNA from undifferentiated and differentiated uninfected and HPV16-positive keratinocytes showed that almost 3000 genes were differentially expressed in keratinocyte due to HPV16 infection. Strikingly, the epithelial barrier function of differentiated keratinocytes, comprising keratinocyte immune function and cellular structure, was found to be disrupted. These data provide new insights into virus-host interaction crucial for production of infectious virus and reveal that HPV infection remodels keratinocytes for completion of the virus replication cycle.
Authors : Klymenko T , Gu Q , Herbert I , Stevenson A , Iliev V , Watkins G , Pollock C , Bhatia R , Cuschieri K , Herzyk P , Gatherer D , Graham S V ,
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Pathways :
WP2272: Pathogenic Escherichia coli infection
WP1017: Type II interferon signaling (IFNG)
WP1040: Inflammatory Response Pathway
WP1113: Cytokines and Inflammatory Response
WP1136: Type II interferon signaling (IFNG)
WP1156: Inflammatory Response Pathway
WP1253: Type II interferon signaling (IFNG)
WP1289: Type II interferon signaling (IFNG)
WP1350: Type II interferon signaling (IFNG)
WP1438: Influenza A virus infection
WP1527: stress response
WP1530: miRNA regulation of DNA Damage Response
WP1579: DNA damage response
WP1584: Type II diabetes mellitus
WP1845: MAPK targets/ Nuclear events mediated by MAP kinases
WP1903: Response to elevated platelet cytosolic Ca2+
WP1939: Unfolded Protein Response
WP2087: miRNA regulation of DNA Damage Response
WP2107: pathways in human cancer
WP2113: Type III interferon signaling
WP2152: BDNF
WP222: Cytokines and Inflammatory Response (BioCarta)
WP271: Cytokines and Inflammatory Response (BioCarta)
WP40: Inflammatory Response Pathway
WP453: Inflammatory Response Pathway
Related Genes :
[Ascl1 Ash1 Mash-1 Mash1] Achaete-scute homolog 1 (ASH-1) (mASH-1) (mASH1)
[FAS2 CPAR2_807400] Fatty acid synthase subunit alpha (EC 2.3.1.86) [Includes: Acyl carrier; 3-oxoacyl-[acyl-carrier-protein] reductase (EC 1.1.1.100) (Beta-ketoacyl reductase); 3-oxoacyl-[acyl-carrier-protein] synthase (EC 2.3.1.41) (Beta-ketoacyl synthase)]
[gliT AFUA_6G09740] Thioredoxin reductase gliT (EC 1.8.1.-) (Gliotoxin biosynthesis protein T)
[Pou3f2 Brn-2 Brn2 Otf7] POU domain, class 3, transcription factor 2 (Brain-specific homeobox/POU domain protein 2) (Brain-2) (Brn-2) (Nervous system-specific octamer-binding transcription factor N-Oct-3) (Octamer-binding protein 7) (Oct-7) (Octamer-binding transcription factor 7) (OTF-7)
[Myt1l Kiaa1106 Nzf1 Png1] Myelin transcription factor 1-like protein (MyT1-L) (MyT1L) (Neural zinc finger factor 1) (NZF-1) (Postmitotic neural gene 1 protein) (Zinc finger protein Png-1)
[TI39_contig844g00043] Pentafunctional AROM polypeptide [Includes: 3-dehydroquinate dehydratase (3-dehydroquinase) (EC 4.2.1.10); 3-dehydroquinate synthase (DHQS) (EC 4.2.3.4); Shikimate kinase (SK) (EC 2.7.1.71); 3-phosphoshikimate 1-carboxyvinyltransferase (EC 2.5.1.19) (5-enolpyruvylshikimate-3-phosphate synthase) (EPSP synthase) (EPSPS); Shikimate dehydrogenase (EC 1.1.1.25)]
[BAX GW7_13624] Apoptosis regulator BAX (Apoptosis regulator BAX isoform alpha)
[SIX1 GW7_21074] Homeobox protein SIX1
[PDGFRA GW7_00400] Platelet-derived growth factor receptor alpha (PDGF-R-alpha) (PDGFR-alpha) (EC 2.7.10.1) (Alpha platelet-derived growth factor receptor) (Alpha-type platelet-derived growth factor receptor)
[GW7_13838] Cellular tumor antigen p53
[PTK2B GW7_07620] Protein tyrosine kinase 2 beta (Protein-tyrosine kinase 2-beta isoform a)
[PARK7 GW7_09141] Protein DJ-1
[CAV3 GW7_19497] Caveolin
[GW7_18161] Apolipoprotein E
[LEP GW7_16808] Leptin (Obesity factor)
[CD36 GW7_06118] Platelet glycoprotein 4
[STAT5B] Signal transducer and activator of transcription
[DLL1] Delta-like protein
[CDK5] Cyclin-dependent kinase 5 isoform 1
[TRAF6 GW7_01379] TNF receptor-associated factor 6
[RPS3 GW7_02079] 40S ribosomal protein S3 (40S ribosomal protein S3 isoform 1)
[SMAD3] Mothers against decapentaplegic homolog (MAD homolog) (Mothers against DPP homolog) (SMAD family member)
[PAX6] Paired box protein Pax-6 isoform a
[ACVR1 GW7_12831] Serine/threonine-protein kinase receptor (EC 2.7.11.30)
[GREM1 GW7_17375] Gremlin
[ANXA1 GW7_17325] Annexin
[PTPN11] Tyrosine-protein phosphatase non-receptor type (EC 3.1.3.48)
[ZC3H12A] Ribonuclease ZC3H12A
[AKT1] Non-specific serine/threonine protein kinase (EC 2.7.11.1)
[FOXP3] Forkhead box protein P3 isoform b
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