Hepatitis B Virus DNA Polymerase Restrains Viral Replication Through the CREB1/HOXA Distal Transcript Antisense RNA Homeobox A13 Axis

Hepatology. 2021 Feb;73(2):503-519. doi: 10.1002/hep.31284.

Abstract

Background and aims: Long noncoding RNAs (lncRNAs) have been associated with infection and hepatitis B virus (HBV)-related diseases, though the underlying mechanisms remain unclear.

Approach and results: We obtained HBV-HCC lncRNA profiles by deep sequencing and found HOXA distal transcript antisense RNA (HOTTIP) to be significantly up-regulated. RT-qPCR indicated that HOTTIP is highly expressed in HBV-positive hepatoma tissue and induced by HBV in vitro. Virological experiments showed that HOTTIP significantly suppresses the generation of hepatitis B viral surface antigen, hepatitis B viral e antigen and HBV replication. Homeobox A13 (HOXA13), a downstream factor of HOTTIP, was found to bind to HBV enhancer I and X promotor to repress the production of HBV pregenome RNA (pgRNA) and total RNA as well as HBV replication, suggesting that HOXA13 mediates HOTTIP-induced suppression of HBV replication. More interestingly, HBV DNA polymerase (DNA pol) binds to and stabilizes cAMP-responsive element-binding protein 1 (CREB1) mRNA to facilitate translation of the protein, which, in turn, binds to the regulatory element of HOTTIP to promote its expression.

Conclusions: Our findings demonstrate that HBV DNA pol attenuates HBV replication through activation of the CREB1-HOTTIP-HOXA13 axis. These findings shed light on the mechanism by which HBV restrains replication to contribute to persistent infection.

Publication types

  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Carcinoma, Hepatocellular / genetics*
  • Carcinoma, Hepatocellular / pathology
  • Carcinoma, Hepatocellular / virology
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • DNA-Directed DNA Polymerase / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Hep G2 Cells
  • Hepatitis B virus / enzymology
  • Hepatitis B virus / genetics
  • Hepatitis B, Chronic / genetics*
  • Hepatitis B, Chronic / pathology
  • Hepatitis B, Chronic / virology
  • Homeodomain Proteins / metabolism
  • Host Microbial Interactions / genetics
  • Humans
  • Liver / pathology
  • Liver Neoplasms / genetics*
  • Liver Neoplasms / pathology
  • Liver Neoplasms / virology
  • Male
  • Middle Aged
  • Promoter Regions, Genetic / genetics
  • Protein Stability
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism
  • Viral Proteins / metabolism*
  • Virus Replication / genetics
  • Young Adult

Substances

  • CREB1 protein, human
  • Cyclic AMP Response Element-Binding Protein
  • Homeodomain Proteins
  • RNA, Long Noncoding
  • Viral Proteins
  • homeobox protein HOXA13
  • long noncoding RNA HOTTIP, human
  • DNA-Directed DNA Polymerase