Comprehensive analysis of Translationally Controlled Tumor Protein (TCTP) provides insights for lineage-specific evolution and functional divergence

PLoS One. 2020 May 6;15(5):e0232029. doi: 10.1371/journal.pone.0232029. eCollection 2020.

Abstract

Background: Translationally controlled tumor protein (TCTP) is a conserved, multifunctional protein involved in numerous cellular processes in eukaryotes. Although the functions of TCTP have been investigated sporadically in animals, invertebrates, and plants, few lineage-specific activities of this molecule, have been reported. An exception is in Arabidopsis thaliana, in which TCTP (AtTCTP1) functions in stomatal closuer by regulating microtubule stability. Further, although the development of next-generation sequencing technologies has facilitated the analysis of many eukaryotic genomes in public databases, inter-kingdom comparative analyses using available genome information are comparatively scarce.

Methodology: To carry out inter-kingdom comparative analysis of TCTP, TCTP genes were identified from 377 species. Then phylogenetic analysis, prediction of protein structure, molecular docking simulation and molecular dynamics analysis were performed to investigate the evolution of TCTP genes and their binding proteins.

Results: A total of 533 TCTP genes were identified from 377 eukaryotic species, including protozoa, fungi, invertebrates, vertebrates, and plants. Phylogenetic and secondary structure analyses reveal lineage-specific evolution of TCTP, and inter-kingdom comparisons highlight the lineage-specific emergence of, or changes in, secondary structure elements in TCTP proteins from different kingdoms. Furthermore, secondary structure comparisons between TCTP proteins within each kingdom, combined with measurements of the degree of sequence conservation, suggest that TCTP genes have evolved to conserve protein secondary structures in a lineage-specific manner. Additional tertiary structure analysis of TCTP-binding proteins and their interacting partners and docking simulations between these proteins further imply that TCTP gene variation may influence the tertiary structures of TCTP-binding proteins in a lineage-specific manner.

Conclusions: Our analysis suggests that TCTP has undergone lineage-specific evolution and that structural changes in TCTP proteins may correlate with the tertiary structure of TCTP-binding proteins and their binding partners in a lineage-specific manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biomarkers, Tumor / chemistry
  • Biomarkers, Tumor / genetics*
  • Biomarkers, Tumor / physiology*
  • Conserved Sequence
  • Eukaryotic Cells / classification
  • Eukaryotic Cells / metabolism
  • Evolution, Molecular*
  • Fungi / classification
  • Fungi / genetics
  • Genetic Speciation*
  • Humans
  • Invertebrates / classification
  • Invertebrates / genetics
  • Mammals / classification
  • Mammals / genetics
  • Molecular Docking Simulation
  • Phylogeny
  • Plant Cells / classification
  • Plant Cells / metabolism
  • Prokaryotic Cells / classification
  • Prokaryotic Cells / metabolism
  • Protein Binding
  • Protein Structure, Secondary
  • Species Specificity
  • Tumor Protein, Translationally-Controlled 1

Substances

  • Biomarkers, Tumor
  • TPT1 protein, human
  • Tumor Protein, Translationally-Controlled 1

Grants and funding

This work was supported by the Korea Research Institute of Bioscience and Biotechnology (KRIBB) initiative program, the Korea Atomic Energy Research Institute (KAERI) initiative program, and Korea Forest Service of Korean government through R&D Program for Forestry Technology (Project No. 2014071H10-2022-AA04) to Y.-M.K. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.