PIR promotes tumorigenesis of breast cancer by upregulating cell cycle activator E2F1

Cell Cycle. 2019 Nov;18(21):2914-2927. doi: 10.1080/15384101.2019.1662259. Epub 2019 Sep 10.

Abstract

Pirin (PIR) protein belongs to the superfamily of cupin and is highly conserved between eukaryotic and prokaryotic organisms. It has been reported that PIR is upregulated in various tumors and involved in tumorigenesis. However, its biological functions particularly in promoting tumorigenesis are, to date, poorly characterized. Here we report that knockdown of PIR in MCF7 and MDA-MB-231 cell lines causes a dramatic decrease in cell proliferation and xenograft tumor growth in mice. Mechanistically, the cell cycle activator E2F1 and its target genes cdk4, cdk6, cycE, cycD and DDR1 are remarkably downregulated in PIR depleted cells, leading to G1/S phase arrest. Luciferase reporter assay and chromatin immunoprecipitation assay indicate that PIR can activate E2F1 transcription by binding to its promoter region. Consistent with the observation in PIR knockdown cells, PIR inhibitors markedly inhibit the proliferation of both cell lines. Furthermore, knockdown of PIR significantly decreases the abilities of MCF7 cells for mobility and invasion in vitro and their metastasis in mice, which may be attributed to the decrease of DDR1. In conclusion, PIR stimulates tumorigenesis and progression by activating E2F1 and its target genes. Our finding thus suggests PIR as a potential druggable target for the therapy of cancers with high expression level of PIR.

Keywords: tumorigenesis.

MeSH terms

  • Animals
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / pathology*
  • Dioxygenases / genetics
  • Dioxygenases / metabolism*
  • E2F1 Transcription Factor / metabolism*
  • Female
  • G1 Phase Cell Cycle Checkpoints / genetics
  • Gene Expression Regulation, Neoplastic / genetics*
  • HEK293 Cells
  • Humans
  • MCF-7 Cells
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Neoplasm Transplantation
  • Promoter Regions, Genetic / genetics
  • Transcriptional Activation / genetics
  • Transplantation, Heterologous

Substances

  • E2F1 Transcription Factor
  • E2F1 protein, human
  • Dioxygenases
  • PIR protein, human

Grants and funding

This work was supported by the National Natural Science Foundation of China [91857102, U1705287, 31571473 and 31701252]; State Key Laboratory of Cellular Stress Biology, Xiamen University [SKLCSB2018KF007 and SKLCSB2019KF005].