Therapy-Induced Senescent/Polyploid Cancer Cells Undergo Atypical Divisions Associated with Altered Expression of Meiosis, Spermatogenesis and EMT Genes

Int J Mol Sci. 2022 Jul 27;23(15):8288. doi: 10.3390/ijms23158288.

Abstract

Upon anticancer treatment, cancer cells can undergo cellular senescence, i.e., the temporal arrest of cell division, accompanied by polyploidization and subsequent amitotic divisions, giving rise to mitotically dividing progeny. In this study, we sought to further characterize the cells undergoing senescence/polyploidization and their propensity for atypical divisions. We used p53-wild type MCF-7 cells treated with irinotecan (IRI), which we have previously shown undergo senescence/polyploidization. The propensity of cells to divide was measured by a BrdU incorporation assay, Ki67 protein level (cell cycle marker) and a time-lapse technique. Advanced electron microscopy-based cell visualization and bioinformatics for gene transcription analysis were also used. We found that after IRI-treatment of MCF-7 cells, the DNA replication and Ki67 level decreased temporally. Eventually, polyploid cells divided by budding. With the use of transmission electron microscopy, we showed the presence of mononuclear small cells inside senescent/polyploid ones. A comparison of the transcriptome of senescent cells at day three with day eight (when cells just start to escape senescence) revealed an altered expression of gene sets related to meiotic cell cycles, spermatogenesis and epithelial-mesenchymal transition. Although chemotherapy (DNA damage)-induced senescence is indispensable for temporary proliferation arrest of cancer cells, this response can be followed by their polyploidization and reprogramming, leading to more fit offspring.

Keywords: SBEM scans; cancer; cell senescence; chemotherapy; polyploidization; senescence escape; soma-to-germline transition.

MeSH terms

  • Cellular Senescence* / genetics
  • Epithelial-Mesenchymal Transition
  • Humans
  • Irinotecan
  • Ki-67 Antigen / genetics
  • Male
  • Meiosis
  • Neoplasms* / drug therapy
  • Neoplasms* / genetics
  • Polyploidy
  • Spermatogenesis / genetics

Substances

  • Ki-67 Antigen
  • Irinotecan