miR-34a is a tumor suppressor in zebrafish and its expression levels impact metabolism, hematopoiesis and DNA damage

PLoS Genet. 2024 May 28;20(5):e1011290. doi: 10.1371/journal.pgen.1011290. eCollection 2024 May.

Abstract

Li-Fraumeni syndrome is caused by inherited TP53 tumor suppressor gene mutations. MicroRNA miR-34a is a p53 target and modifier gene. Interestingly, miR-34 triple-null mice exhibit normal p53 responses and no overt cancer development, but the lack of miR-34 promotes tumorigenesis in cancer-susceptible backgrounds. miR-34 genes are highly conserved and syntenic between zebrafish and humans. Zebrafish miR-34a and miR-34b/c have similar expression timing in development, but miR-34a is more abundant. DNA damage by camptothecin led to p53-dependent induction of miR-34 genes, while miR-34a mutants were adult-viable and had normal DNA damage-induced apoptosis. Nevertheless, miR-34a-/- compound mutants with a gain-of-function tp53R217H/ R217H or tp53-/- mutants were more cancer-prone than tp53 mutants alone, confirming the tumor-suppressive function of miR-34a. Through transcriptomic comparisons at 28 hours post-fertilization (hpf), we characterized DNA damage-induced transcription, and at 8, 28 and 72 hpf we determined potential miR-34a-regulated genes. At 72 hpf, loss of miR-34a enhanced erythrocyte levels and up-regulated myb-positive hematopoietic stem cells. Overexpression of miR-34a suppressed its reporter mRNA, but not p53 target induction, and sensitized injected embryos to camptothecin but not to γ-irradiation.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Camptothecin / pharmacology
  • DNA Damage*
  • Gene Expression Regulation, Developmental
  • Genes, Tumor Suppressor
  • Hematopoiesis* / genetics
  • Humans
  • Li-Fraumeni Syndrome / genetics
  • Mice
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Tumor Suppressor Protein p53* / genetics
  • Tumor Suppressor Protein p53* / metabolism
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / genetics

Substances

  • Camptothecin
  • MicroRNAs
  • tp53 protein, zebrafish
  • Tumor Suppressor Protein p53
  • Zebrafish Proteins
  • MIRN34 microRNA, zebrafish

Grants and funding

This research was funded by the Canadian Institutes of Health Research (CIHR) (Grant number PJT-166081). KK was supported by the Ontario Graduate Scholarship (2022) and CIHR Canada Graduate Scholarship – Doctoral (2023). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.