Some chemotherapeutics-treated colon cancer cells display a specific phenotype being a combination of stem-like and senescent cell features

Cancer Biol Ther. 2018 Jan 2;19(1):63-75. doi: 10.1080/15384047.2017.1385675. Epub 2017 Dec 22.

Abstract

Colorectal cancer (CRC) is the second leading cause of death among cancer patients in the Northern countries. CRC can reappear a long time after treatment. Recent clinical studies demonstrated that, in response to chemotherapy, cancer cells may undergo stress-induced premature senescence (SIPS), which typically results in growth arrest. Nonetheless, these senescent cells were reported to divide in an atypical manner and thus contribute to cancer re-growth. Therefore, we examined if SIPS escape may follow treatment with chemotherapeutics used clinically: 5-fluorouracil (5-FU), oxaliplatin (OXA) and irinotecan (IRINO). To mimic the therapeutic regimes we exposed human colon cancer HCT116 and SW480 cells to repeated cycles of drug treatment. The cells treated with 5-FU or IRINO exhibited several hallmarks of SIPS: growth arrest, increased size and granularity, polyploidization, augmented activity of the SA-β-galactosidase, accumulation of P21 and CYCLIN D1 proteins, and the senescence-associated secretory phenotype. Moreover, re-population of the cancer cell cultures was delayed upon treatment with the senescence-inducing agents. At the same time, we detected a subpopulation of senescent colon cancer cells with features of stemness: elevated NANOG expression, exclusion of Hoechst 33342 (typical for side population) and increased CD24 expression. Additionally, rare, polyploid cells exhibited blastocyst-like morphology and produced progeny. In parallel, majority of chemotherapeutics-treated cells underwent mesenchymal to epithelial transition, as the percentage of CD44-positve cells was reduced, and levels of E-cadherin (epithelial marker) were elevated. Our study demonstrates that a subpopulation of chemotherapeutics-treated colon cancer cells display a specific phenotype being a combination of stem-like and senescent cell features. This may contribute to their resistance to chemotherapy and their ability to re-grow cancer after completion of therapeutic intervention.

Keywords: 5-fluoruracil; angiogenesis; cancer Biology; cancer stem cells; cell Cycle control; chemotherapy; colon cancer; doxorubicin; irinotecan; molecular Therapy; oxaliplatin; senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Cellular Senescence / drug effects*
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / pathology
  • Cyclin D1 / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • Epithelial-Mesenchymal Transition / drug effects*
  • Fluorouracil / pharmacology
  • Fluorouracil / therapeutic use
  • HCT116 Cells
  • Humans
  • Hyaluronan Receptors / metabolism
  • Irinotecan / pharmacology
  • Irinotecan / therapeutic use
  • Neoplastic Stem Cells / drug effects*
  • Neoplastic Stem Cells / pathology
  • Oxaliplatin / pharmacology
  • Oxaliplatin / therapeutic use

Substances

  • Antineoplastic Agents
  • CCND1 protein, human
  • CD44 protein, human
  • Hyaluronan Receptors
  • Oxaliplatin
  • Cyclin D1
  • Irinotecan
  • Fluorouracil

Grants and funding

The Foundation for Polish Science co-financed by the European Union under the European Social Fund (IP2012 062172); the Ministry of Science and Higher Education (IP2012 062172); the Ministry of Science and Higher Education (438/2012); Polish National Center of Science (2012/05/E/ST2/02180); Polish National Center of Science (2013/09/B/NZ3/01389); EU FP7 Project BIO-IMAGINE: BIO-IMAGing in research INnovation and Education (264173).