Potential consequences of phototoxicity on cell function during live imaging of intestinal organoids

PLoS One. 2024 Nov 15;19(11):e0313213. doi: 10.1371/journal.pone.0313213. eCollection 2024.

Abstract

Live imaging visualizes the structure, dynamics, and function of cells and tissues to reveal the molecular mechanisms, and has contributed to the advancement of life science. In live imaging, it has been well known that there is a trade-off between higher-resolution analysis and cell damage caused by light illumination, i.e., phototoxicity. However, despite the risk of unknowingly distorting experimental results, phototoxicity is an unresolved issue in live imaging because overall consequences occurring inside cells due to phototoxicity remains unknown. Here, we determined the molecular process of phototoxicity-induced cell damage systematically under low- and high-dose light illumination conditions by analyzing differential gene expression using RNA-sequencing in a three-dimensional organoid of small intestinal epithelial cells, enteroid. The low-dose light illumination already induced various abnormalities in functional molecules involved in the response to reactive oxygen species generated by the excitation of fluorescent dyes, intracellular metabolism, mitosis, immune responses, etc., at mRNA expression level. Together with the behavior toward apoptosis caused by high-dose light illumination, the light dose-dependent progression of intracellular damage was revealed. About visible impairment of intestinal epithelial function, failures in both the structure-forming ability of enteroids and Paneth cell granule secretion were observed under high-dose light illumination, while the drug efflux was not disturbed despite abnormal drug efflux transporter mRNA expression. Based on the gene expression profiles, we comprehensively clarified phenomena in the cells at mRNA level that cannot be recognized both morphologically and functionally during live imaging, further providing a new insight into the risk of phototoxicity. This study warns from the aspect of mRNA expression that awareness of phototoxic artifacts is needed when analyzing cellular function and the mechanism in live imaging.

MeSH terms

  • Animals
  • Apoptosis / radiation effects
  • Humans
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / radiation effects
  • Light / adverse effects
  • Mice
  • Organoids* / metabolism
  • Organoids* / radiation effects
  • Reactive Oxygen Species / metabolism

Substances

  • Reactive Oxygen Species

Grants and funding

This study was supported by Grants from the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (KAKENHI, https://www.jsps.go.jp/english/e-grants/) Grant Number 21K15460 (to Y.Y.), 21H02891 (to T.A.), 22K19120 (to K.N.), and the Program on Open Innovation Platforms for Industry-academia Co-creation (COI-NEXT, https://www.jst.go.jp/pf/platform/index.html) from the Japan Science and Technology Agency, Grant Number JPMJPF2108 (to K.N.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.