G2-quadruplex in the 3'UTR of IE180 regulates Pseudorabies virus replication by enhancing gene expression

RNA Biol. 2020 Jun;17(6):816-827. doi: 10.1080/15476286.2020.1731664. Epub 2020 Mar 12.

Abstract

RNA secondary structure elements in the mRNA 3'-untranslated regions (3'UTR) play important roles in post-transcriptional regulation. RNA structure elements in the viral RNA provide valuable model for studying diverse regulation mechanisms. Herpesvirus genomes are double-stranded DNA with GC-rich sequences, which can be transcribed into abundant GC-rich RNAs. It is valuable to explore the structures and function of those GC-rich RNAs. We identified a G2-quadruplex-forming sequence named PQS18-1 in the 3'UTR of the unique immediate early gene of Pseudorabies virus (PRV), an important member of Alphaherpesvirinae subfamily. The RNA PQS18-1 was folded into parallel G-quadruplex structure, enhancing gene expression. Both non-G-quadruplex mutant and G3-quadruplex mutant in the 3'UTR showed lower gene expression level than the wildtype G2-quadruplex. TMPyP4 destroyed PQS18-1 G2-quadruplex and suppressed gene expression, accordingly reducing PRV replication by one titre in the PK15 cells at 24 h post infection. Our findings indicated that the RNA G2-quadruplex in 3'UTR was essential for high expression of IE180 gene, and it could be a specific post-transcription regulation element in response to small molecules or other macromolecules. This study discovers a novel RNA G2-quadruplex in the 3'UTR of an immediate early gene of alphaherpesvirus and provides a new nucleic acid target for anti-virus drug design.

Keywords: Alphaherpesvirinae; 3ʹ-untranslated region; G-quadruplex; immediate early gene; post-transcription regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions*
  • Animals
  • Base Sequence
  • G-Quadruplexes*
  • Gene Expression Regulation, Viral*
  • Herpesvirus 1, Suid / genetics*
  • Immediate-Early Proteins / genetics*
  • Pseudorabies / virology*
  • Virus Replication / genetics*

Substances

  • 3' Untranslated Regions
  • Immediate-Early Proteins

Grants and funding

This work was supported by the National Natural Science Foundation of China under Grant number 31672558, 21732002, 31701791, 21502060 and 31770191; the Huazhong Agricultural University Scientific & Technological Self-innovation Foundation under Grant 2015RC013, 2662017PY113 and 2662015PY208; the Open fund of The State Key Laboratory of Bio-organic and Natural Products Chemistry, Chinese Academy of Sciences under Grant SKLBNPC16343; the Hubei Provincial Natural Science Foundation of China under Grant 2017CFB233; and the Fundamental Research Funds for the Central Universities under Grant 2662015QD046. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.