Paracrine Placental Growth Factor Signaling in Response to Ionizing Radiation Is p53-Dependent and Contributes to Radioresistance

Mol Cancer Res. 2021 Jun;19(6):1051-1062. doi: 10.1158/1541-7786.MCR-20-0403. Epub 2021 Feb 22.

Abstract

Placental growth factor (PlGF) is a pro-angiogenic, N-glycosylated growth factor, which is secreted under pathologic situations. Here, we investigated the regulation of PlGF in response to ionizing radiation (IR) and its role for tumor angiogenesis and radiosensitivity. Secretion and expression of PlGF was induced in multiple tumor cell lines (medulloblastoma, colon and lung adenocarcinoma) in response to irradiation in a dose- and time-dependent manner. Early upregulation of PlGF expression and secretion in response to irradiation was primarily observed in p53 wild-type tumor cells, whereas tumor cells with mutated p53 only showed a minimal or delayed response. Mechanistic investigations with genetic and pharmacologic targeting of p53 corroborated regulation of PlGF by the tumor suppressor p53 in response to irradiation under normoxic and hypoxic conditions, but with so far unresolved mechanisms relevant for its minimal and delayed expression in tumor cells with a p53-mutated genetic background. Probing a paracrine role of IR-induced PlGF secretion in vitro, migration of endothelial cells was specifically increased towards irradiated PlGF wild type but not towards irradiated PlGF-knockout (PIGF-ko) medulloblastoma cells. Tumors derived from these PlGF-ko cells displayed a reduced growth rate, but similar tumor vasculature formation as in their wild-type counterparts. Interestingly though, high-dose irradiation strongly reduced microvessel density with a concomitant high rate of complete tumor regression only in the PlGF-ko tumors. IMPLICATIONS: Our study shows a strong paracrine vasculature-protective role of PlGF as part of a p53-regulated IR-induced resistance mechanism and suggest PlGF as a promising target for a combined treatment modality with RT.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Animals
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Cell Movement / radiation effects
  • Gene Expression Regulation, Neoplastic / radiation effects*
  • Gene Knockout Techniques
  • HCT116 Cells
  • Humans
  • Mice
  • Mice, Nude
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / radiotherapy
  • Paracrine Communication / genetics
  • Paracrine Communication / radiation effects*
  • Placenta Growth Factor / genetics*
  • Placenta Growth Factor / metabolism
  • Radiation Tolerance / genetics*
  • Radiation, Ionizing*
  • Tumor Suppressor Protein p53 / genetics*
  • Tumor Suppressor Protein p53 / metabolism
  • Xenograft Model Antitumor Assays / methods

Substances

  • Tumor Suppressor Protein p53
  • Placenta Growth Factor