Photodynamic treatment increases the lifespan and oxidative stress resistance of Caenorhabditis elegans

ElsevierVolume 221, 20 August 2024, Pages 98-110Free Radical Biology and MedicineAuthor links open overlay panel, , , , , , , , , Highlights•

A Photodynamic reaction with hypericin and orange light generates ROS in C. elegans.

Mild PDTr increases the lifespan and resistance to oxidative stress in C. elegans.

PDTr-induced oxidative stress resistance depends on NRF2, FOXO, AMPK, and p38 MAPK.

PDTr induces NRF2 and FOXO nuclear translocation and ctl-1, gst-4, and sod-3 expression.

Abstract

Photodynamic therapy is a noninvasive treatment in which specific photosensitizers and light are used to produce high amounts of reactive oxygen species (ROS), which can be employed for targeted tissue destruction in cancer treatment or antimicrobial therapy. However, it remains unknown whether lower amounts of ROS produced by mild photodynamic therapy increase lifespan and stress resistance at the organism level. Here, we introduce a novel photodynamic treatment (PDTr) that uses 20 μM hypericin, a photosensitizer that originates from Hypericum perforatum, and orange light (590 nm, 5.4 W/m2, 1 min) to induce intracellular ROS formation (ROS), thereby resulting in lifespan extension and improved stress resistance in C. elegans. The PDTr-induced increase in longevity was abrogated by N-acetyl cysteine, suggesting the hormetic response was driven by prooxidative mechanisms. PDTr activated the translocation of SKN-1/NRF-2 and DAF-16/FOXO, leading to elevated expression of downstream oxidative stress-responsive genes, including ctl-1, gst-4, and sod-3. In summary, our findings suggest a novel PDTr method that extends the lifespan of C. elegans under both normal and oxidative stress conditions through the activation of SKN-1 and DAF-16 via the involvement of many antioxidant genes.

Keywords

Hypericin

Photodynamic treatment

Lifespan

Hormesis

Caenorhabditis elegans

AbbreviationsAMPK

AMP-activated protein kinase

EGCG

epigallocatechin gallate

MAPK

mitogen-activated protein kinase

NGM

nematode growth medium

NMR

nuclear magnetic resonance

PDTr

photodynamic treatment

ROS

reactive oxygen species

TTL

transistor-transistor logic

© 2024 The Authors. Published by Elsevier Inc.

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