The role of nuclear organization in trans-splicing based expression of heat shock protein 90 in Giardia lamblia

PLoS Negl Trop Dis. 2021 Sep 24;15(9):e0009810. doi: 10.1371/journal.pntd.0009810. eCollection 2021 Sep.

Abstract

Hsp90 gene of G. lamblia has a split nature comprising two ORFs separated by 777 kb on chromosome 5. The ORFs of the split gene on chromosome 5 undergo transcription to generate independent pre-mRNAs that join by a unique trans-splicing reaction that remains partially understood. The canonical cis-acting nucleotide elements such as 5'SS-GU, 3'SS-AG, polypyrimidine tract and branch point adenine are present in the independent pre-mRNAs and therefore trans-splicing of Hsp90 must be assisted by spliceosomes in vivo. Using an approach of RNA-protein pull down, we show that an RNA helicase selectively interacts with HspN pre-mRNA. Our experiments involving high resolution chromosome conformation capture technology as well as DNA FISH show that the trans-spliced genes of Giardia are in three-dimensional spatial proximity in the nucleus. Altogether our study provides a glimpse into the in vivo mechanisms involving protein factors as well as chromatin structure to facilitate the unique inter-molecular post-transcriptional stitching of split genes in G. lamblia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Giardia lamblia / genetics*
  • Giardia lamblia / metabolism*
  • HSP90 Heat-Shock Proteins / genetics*
  • HSP90 Heat-Shock Proteins / metabolism*
  • Humans
  • Open Reading Frames
  • RNA Precursors / genetics
  • RNA Precursors / metabolism
  • RNA Splicing
  • Spliceosomes / genetics
  • Spliceosomes / metabolism
  • Trans-Splicing*

Substances

  • HSP90 Heat-Shock Proteins
  • RNA Precursors

Grants and funding

This research was supported by Department of Biotechnology (Grant No.- DBTO-0403) and DBT-IISc Partnership grant to S.G., R.M and U.T.; V.I. and S.T. acknowledge GATE fellowship from IISc; S.V. acknowledges financial support from CCMB; S.M. was supported by scholarship from IISc. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.