Comparative analysis of the LARP1 C-terminal DM15 region through Coelomate evolution

PLoS One. 2024 Aug 27;19(8):e0308574. doi: 10.1371/journal.pone.0308574. eCollection 2024.

Abstract

TOR (target of rapamycin), a ubiquitous protein kinase central to cellular homeostasis maintenance, fundamentally regulates ribosome biogenesis in part by its target La-related protein 1 (LARP1). Among other target transcripts, LARP1 specifically binds TOP (terminal oligopyrimidine) mRNAs encoding all 80 ribosomal proteins in a TOR-dependent manner through its C-terminal region containing the DM15 module. Though the functional implications of the LARP1 interaction with target mRNAs is controversial, it is clear that the TOP-LARP1-TOR axis is critical to cellular health in humans. Its existence and role in evolutionarily divergent animals remain less understood. We focused our work on expanding our knowledge of the first arm of the axis: the connection between LARP1-DM15 and the 5' TOP motif. We show that the overall DM15 architecture observed in humans is conserved in fruit fly and zebrafish. Both adopt familiar curved arrangements of HEAT-like repeats that bind 5' TOP mRNAs on the same conserved surface, although molecular dynamics simulations suggest that the N-terminal fold of the fruit fly DM15 is predicted to be unstable and unfold. We demonstrate that each ortholog interacts with TOP sequences with varying affinities. Importantly, we determine that the ability of the DM15 region to bind some TOP sequences but not others might amount to the context of the RNA structure, rather than the ability of the module to recognize some sequences but not others. We propose that TOP mRNAs may retain similar secondary structures to regulate LARP1 DM15 recognition.

Publication types

  • Comparative Study

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Autoantigens* / chemistry
  • Autoantigens* / genetics
  • Autoantigens* / metabolism
  • Evolution, Molecular*
  • Humans
  • Molecular Dynamics Simulation
  • Protein Binding
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Ribonucleoproteins* / chemistry
  • Ribonucleoproteins* / genetics
  • Ribonucleoproteins* / metabolism
  • SS-B Antigen*
  • Zebrafish / genetics

Substances

  • Ribonucleoproteins
  • SS-B Antigen
  • Autoantigens
  • RNA, Messenger

Grants and funding

This work was supported by grants R01GM116889 and R35GM145257 from the National Institute of General Medical Sciences (https://www.nigms.nih.gov) and RSG-17-197-01-RMC from the American Cancer Society (www.cancer.org) to A.J.B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.