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. 2019 Jan 4;93(2):e01216-18.
doi: 10.1128/JVI.01216-18. Print 2019 Jan 15.

Inhibition of Epstein-Barr Virus Replication in Human Papillomavirus-Immortalized Keratinocytes

Affiliations

Inhibition of Epstein-Barr Virus Replication in Human Papillomavirus-Immortalized Keratinocytes

J T Guidry et al. J Virol. .

Abstract

Epstein-Barr virus (EBV) is implicated in the pathogenesis of human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OSCC). EBV-associated cancers harbor a latent EBV infection characterized by a lack of viral replication and the expression of viral oncogenes. Cellular changes promoted by HPV are comparable to those shown to facilitate EBV latency, though whether HPV-positive cells support a latent EBV infection has not been demonstrated. Using a model of direct EBV infection into HPV16-immortalized tonsillar cells grown in organotypic raft culture, we showed robust EBV replication in HPV-negative rafts but little to no replication in HPV-immortalized rafts. The reduced EBV replication was independent of immortalization, as human telomerase-immortalized normal oral keratinocytes supported robust EBV replication. Furthermore, we observed reduced EBV lytic gene expression and increased expression of EBER1, a noncoding RNA highly expressed in latently infected cells, in the presence of HPV. The use of human foreskin keratinocyte rafts expressing the HPV16 E6 and/or E7 oncogene(s) (HPV E6 and E7 rafts) showed that E7 was sufficient to reduce EBV replication. EBV replication is dependent upon epithelial differentiation and the differentiation-dependent expression of the transcription factors KLF4 and PRDM1. While KLF4 and PRDM1 levels were unaltered, the expression levels of KLF4 transcriptional targets, including late differentiation markers, were reduced in HPV E6 and E7 rafts compared to their levels in parental rafts. However, the HPV E7-mediated block in EBV replication correlated with delayed expression of early differentiation markers. Overall, this study reveals an HPV16-mediated block in EBV replication, through E7, that may facilitate EBV latency and long-term persistence in the tumor context.IMPORTANCE Using a model examining the establishment of EBV infection in HPV-immortalized tissues, we showed an HPV-induced interruption of the normal EBV life cycle reminiscent of a latent EBV infection. Our data support the notion that a persistent EBV epithelial infection depends upon preexisting cellular alterations and suggest the ability of HPV to promote such changes. More importantly, these findings introduce a model for how EBV coinfection may influence HPV-positive (HPV-pos) OSCC pathogenesis. Latently EBV-infected epithelial cells, as well as other EBV-associated head-and-neck carcinomas, exhibit oncogenic phenotypes commonly seen in HPV-pos OSCC. Therefore, an HPV-induced shift in the EBV life cycle toward latency would not only facilitate EBV persistence but also provide additional viral oncogene expression, which can contribute to the rapid progression of HPV-pos OSCC. These findings provide a step toward defining a role for EBV as a cofactor in HPV-positive oropharyngeal tumors.

Keywords: EBV; Epstein-Barr virus; HPV; latency; organotypic; replication; viral replication.

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Figures

FIG 1
FIG 1
Reduced EBV replication in HPV-immortalized rafts following EBV infection. (A) Schematic of EBV infection of HPV-immortalized human tonsillar epithelial (HPV-pos HTE) cells in raft culture. (B) HTE raft DNA harboring either episomal or integrated HPV was analyzed for exonuclease digestion resistance by qPCR. DNA from HPV-infected 293TT cells served as an episomal control. qPCR was used to detect HPV16 DNA (E6), mitochondrial DNA (Mito), and 18S ribosomal DNA. (C) EBV genome copy numbers per hCRP copy number in primary HTE (HPV-neg; n = 6) and HPV-pos HTE rafts harboring episomal (n = 3) or integrated (n = 6) HPV genomes were quantified by qPCR. Shown are the average values and standard errors of the means. *, P < 0.05 relative to the results for HPV-neg HTE rafts. (D) EBV genome copy numbers per hCRP copy number in NOK rafts were quantified by qPCR. Shown are the average values and standard errors of the means. *, P < 0.05 relative to the results for EBV. Rafts were infected in the presence or absence of acyclovir (ACV; 50 μg/ml).
FIG 2
FIG 2
EBV gene expression profile in HPV-immortalized rafts. Acyclovir-treated HPV-neg and HPV-pos HTE raft cultures were analyzed by RT-qPCR for mRNA levels of EBV genes. The BZLF1 expression level in HPV-neg rafts was arbitrarily set to 1. Shown are the average relative expression levels and standard errors of the means from a minimum of 3 rafts per group. *, P < 0.05 relative to the results for HPV-neg HTE rafts.
FIG 3
FIG 3
Delayed epithelial differentiation in HPV-immortalized rafts. (A, B) H&E staining (A) and involucrin (Inv) immunofluorescent (IF) staining (B) of HPV-neg and HPV-pos HTE rafts. (C) HPV-neg and HPV-pos rafts were analyzed by RT-qPCR for mRNA levels of KLF4, PRDM1, WNT5A and filaggrin (FLG). Shown are the average normalized expression levels and standard errors of the means from a minimum of three rafts per group. *, P < 0.05 relative to the results for HPV-neg HTE rafts. (D) IF staining of KLF4 in HPV-neg and HPV-pos rafts. (E) Amounts of KLF4-positive cells were quantified as the percentages of total cells. Shown are the average values and standard errors of the means. (A, B, D) Basal layers are delineated by dotted lines. Scale bars represent 50 μm.
FIG 4
FIG 4
Abrogated EBV replication in HPV16 E6E7-expressing rafts. (A, B) HPV oncogene expression confirmed by RT-qPCR in NOK (n = 1) (A) and HFK (n = 3) (B) cell lines expressing E6, E7, or both (E6E7). E6 expression levels in NOK E6E7 and HFK E6E7 were arbitrarily set to 1. (B) Shown are the average values and standard errors of the means. (C) NOK or HFK expressing E6E7 (n = 5) or carrying an empty vector (Vec; NOK [n = 7], HFK [n = 2]) were rafted, infected with EBV, and analyzed for EBV genome copy numbers per hCRP copy number by qPCR. *, P < 0.05 relative to the results for NOK Vec. (D) Parental HFK and HFK E6E7 rafts (n = 5) were analyzed for EBV genome copy numbers per hCRP copy number at 15 days postinfection (dpi). Shown are the average values and standard errors of the means. (E) HFK and HFK E6E7 rafts infected with cell-free EBV were analyzed for EBV genome copy numbers per hCRP copy number at 6 dpi. Shown are the average values and standard errors of the means from a minimum of 3 rafts per group. *, P < 0.05 relative to the results for parental HFK.
FIG 5
FIG 5
Loss of EBV early and late proteins in HPV16 E6E7-expressing rafts. (A to C) IF staining (A) and quantification of EBV Z (B) and EA-D (C) in HFK and HFK E6E7 rafts infected with EBV. Three independent rafts per group were analyzed. Signal-positive cells were quantified as the percentages of total cells. (B, C) Shown are the average values and standard errors of the means. **, P < 0.01 relative to the results for parental HFK. (A) Scale bars represent 50 μm. (D) IF staining of EBV gp350 in EBV-infected HFK and HFK E6E7 rafts. White arrows indicate cells exhibiting a prominent signal. Scale bar represents 15 μm. (A, D) Basal layers are delineated by dotted lines.
FIG 6
FIG 6
TGF-β1 effect on EBV replication in HFK E6E7 rafts. (A) Parental HFK (n = 6) and HFK E6E7 (n = 5) rafts and HFK E6E7 rafts treated with TGF-β1 (10 ng/ml; n = 5) were analyzed for MYC expression by RT-qPCR. MYC expression in HFK was arbitrarily set to 1. Shown are the average relative expression levels and standard errors of the means. *, P < 0.05; **, P < 0.01. (B) Rafts were infected with EBV and treated with TGF-β1 and acyclovir (ACV; 100 μg/ml) or vehicle (Veh). EBV genome copy numbers per hCRP copy number were quantified by qPCR. n.d., not done. Shown are the average values and standard errors of the means.
FIG 7
FIG 7
Decreased EBV replication in E7-expressing rafts. Parental HFK rafts (n = 8) and HFK rafts expressing E6 (n = 7), E7 (n = 6), or both (E6E7) (n = 10) were analyzed for EBV genome copy numbers per hCRP copy number in the presence of acyclovir (ACV; 100 μg/ml) or vehicle (Veh). Shown are the average values and standard errors of the means. *, P < 0.05 relative to the results for parental HFK.
FIG 8
FIG 8
Delayed differentiation in E7-expressing HFK rafts. (A to E) IF staining of involucrin (Inv) (A), cytokeratin 10 (K10) (B), filaggrin (Flg) (C), KLF4 (D), and PRDM1 (E) in parental HFK rafts and HFK rafts expressing E6 and/or E7. Basal layers are delineated by dotted lines. Scale bars represent 50 μm. (F) Percentages of KLF4- and PRDM1-positive cells were quantified as the percentages of total cells in rafts. Shown are the average values and standard errors of the means. (G) HFK and E6E7 rafts (n = 3) were analyzed by RT-qPCR for mRNA levels of KLF4 and PRDM1. KLF4 expression level in HFK was arbitrarily set to 1. (H) Rafts were analyzed by RT-qPCR for mRNA levels of FLG, LOR, and WNT5A. (G, H) Shown are the average relative expression levels and standard errors of the means from a minimum of three rafts per group. *, P < 0.05 relative to the results for parental HFK.

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