Butyrate enhances the efficacy of radiotherapy via FOXO3A in colorectal cancer patient‑derived organoids

Int J Oncol. 2020 Dec;57(6):1307-1318. doi: 10.3892/ijo.2020.5132. Epub 2020 Oct 13.

Abstract

Enhancing the radioresponsiveness of colorectal cancer (CRC) is essential for local control and prognosis. However, consequent damage to surrounding healthy cells can lead to treatment failure. We hypothesized that short‑chain fatty acids (SCFAs) could act as radiosensitizers for cancer cells, allowing the administration of a lower and safer dose of radiation. To test this hypothesis, the responses of three‑dimensional‑cultured organoids, derived from CRC patients, to radiotherapy, as well as the effects of combined radiotherapy with the SCFAs butyrate, propionate and acetate as candidate radiosensitizers, were evaluated via reverse transcription‑quantitative polymerase chain reaction, immunohistochemistry and organoid viability assay. Of the three SCFAs tested, only butyrate suppressed the proliferation of the organoids. Moreover, butyrate significantly enhanced radiation‑induced cell death and enhanced treatment effects compared with administration of radiation alone. The radiation‑butyrate combination reduced the proportion of Ki‑67 (proliferation marker)‑positive cells and decreased the number of S phase cells via FOXO3A. Meanwhile, 3/8 CRC organoids were found to be non‑responsive to butyrate with lower expression levels of FOXO3A compared with the responsive cases. Notably, butyrate did not increase radiation‑induced cell death and improved regeneration capacity after irradiation in normal organoids. These results suggest that butyrate could enhance the efficacy of radiotherapy while protecting the normal mucosa, thus highlighting a potential strategy for minimizing the associated toxicity of radiotherapy.

Keywords: butyrate; colorectal cancer; FOXO3A; patient-derived organoid; radiosensitizer.

MeSH terms

  • Aged
  • Aged, 80 and over
  • Butyric Acid / administration & dosage*
  • Cell Culture Techniques
  • Chemoradiotherapy, Adjuvant / methods*
  • Colectomy
  • Colon / cytology
  • Colon / drug effects
  • Colon / pathology
  • Colon / radiation effects
  • Colonic Neoplasms / pathology
  • Colonic Neoplasms / therapy*
  • Colonoscopy
  • Female
  • Forkhead Box Protein O3 / metabolism*
  • Humans
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / pathology
  • Intestinal Mucosa / radiation effects
  • Male
  • Middle Aged
  • Organoids
  • Proctectomy
  • Rectal Neoplasms / pathology
  • Rectal Neoplasms / therapy*
  • Rectum / cytology
  • Rectum / drug effects
  • Rectum / pathology
  • Rectum / radiation effects

Substances

  • FOXO3 protein, human
  • Forkhead Box Protein O3
  • Butyric Acid