Transcriptional control of a stem cell factor nucleostemin in liver regeneration and aging

PLoS One. 2024 Sep 11;19(9):e0310219. doi: 10.1371/journal.pone.0310219. eCollection 2024.

Abstract

Nucleostemin (NS) plays a role in liver regeneration, and aging reduces its expression in the baseline and regenerating livers following 70% partial hepatectomy (PHx). Here we interrogate the mechanism controlling NS expression during liver regeneration and aging. The NS promoter was analyzed by TRANSFAC. Functional studies were performed using cell-based luciferase assay, endogenous NS expression in Hep3B cells, mouse livers with a gain-of-function mutation of C/EBPα (S193D), and mouse livers with C/EBPα knockdown. We found a CAAT box with four C/EBPα binding sites (-1216 to -735) and a GC box with consensus binding sites for c-Myc, E2F1, and p300-associated protein complex (-633 to -1). Age-related changes in NS expression correlated positively with the expression of c-Myc, E2F1, and p300, and negatively with that of C/EBPα and C/EBPβ. PHx upregulated NS expression at 1d, coinciding with an increase in E2F1 and a decrease in C/EBPα. C/EBPα bound to the consensus sequences found in the NS promoter in vitro and in vivo, inhibited its transactivational activity in a binding site-dependent manner, and decreased the expression of endogenous NS in Hep3B cells. In vivo activation of C/EBPα by the S193D mutation resulted in a 4th-day post-PHx reduction of NS, a feature shared by 16-m/o livers. Finally, C/EBPα knockdown increased its expression in aged (24-m/o) livers under both baseline and regeneration conditions. This study reports the C/EBPα suppression of NS expression in aged livers, providing a new perspective on the mechanistic orchestration of tissue homeostasis in aging.

MeSH terms

  • Aging* / genetics
  • Aging* / metabolism
  • Aging* / physiology
  • Animals
  • Binding Sites
  • CCAAT-Enhancer-Binding Protein-alpha / genetics
  • CCAAT-Enhancer-Binding Protein-alpha / metabolism
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Line, Tumor
  • E1A-Associated p300 Protein / metabolism
  • E2F1 Transcription Factor / genetics
  • E2F1 Transcription Factor / metabolism
  • GTP-Binding Proteins* / genetics
  • GTP-Binding Proteins* / metabolism
  • Gene Expression Regulation
  • Hepatectomy
  • Humans
  • Liver / metabolism
  • Liver Regeneration* / genetics
  • Liver Regeneration* / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • Promoter Regions, Genetic*
  • Proto-Oncogene Proteins c-myc* / genetics
  • Proto-Oncogene Proteins c-myc* / metabolism
  • RNA-Binding Proteins
  • Transcription, Genetic

Substances

  • Nuclear Proteins
  • GTP-Binding Proteins
  • Proto-Oncogene Proteins c-myc
  • CCAAT-Enhancer-Binding Protein-beta
  • E2F1 Transcription Factor
  • nucleostemin protein, mouse
  • E1A-Associated p300 Protein
  • CCAAT-Enhancer-Binding Protein-alpha
  • Carrier Proteins
  • E2f1 protein, mouse
  • Ep300 protein, mouse
  • RNA-Binding Proteins

Grants and funding

This work was supported by National Institute on Aging (NIA) Public Health Service (PHS) grant R21AG052006 and the Cancer Prevention Research Institute of Texas (CPRIT) Individual Investigator Research Award (RP200081) to RYT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.