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Regulation of photosensation by hydrogen peroxide and antioxidants in C. elegans.

ABSTRACT: The eyeless C. elegans exhibits robust phototaxis behavior in response to short-wavelength light, particularly UV light. C. elegans senses light through LITE-1, a unique photoreceptor protein that belongs to the invertebrate taste receptor family. However, it remains unclear how LITE-1 is regulated. Here, we performed a forward genetic screen for genes that when mutated suppress LITE-1 function. One group of lite-1 suppressors are the genes required for producing the two primary antioxidants thioredoxin and glutathione, suggesting that oxidization of LITE-1 inhibits its function. Indeed, the oxidant hydrogen peroxide (H2O2) suppresses phototaxis behavior and inhibits the photoresponse in photoreceptor neurons, whereas other sensory behaviors are relatively less vulnerable to H2O2. Conversely, antioxidants can rescue the phenotype of lite-1 suppressor mutants and promote the photoresponse. As UV light illumination generates H2O2, we propose that upon light activation of LITE-1, light-produced H2O2 then deactivates LITE-1 to terminate the photoresponse, while antioxidants may promote LITE-1's recovery from its inactive state. Our studies provide a potential mechanism by which H2O2 and antioxidants act synergistically to regulate photosensation in C. elegans.

SUBMITTER: Zhang W

PROVIDER: S-EPMC7755287 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Regulation of photosensation by hydrogen peroxide and antioxidants in C. elegans.

Zhang Wenyuan W He Feiteng F Ronan Elizabeth A EA Liu Hongkang H Gong Jianke J Liu Jianfeng J Xu X Z Shawn XZS

PLoS genetics 20201210 12

The eyeless C. elegans exhibits robust phototaxis behavior in response to short-wavelength light, particularly UV light. C. elegans senses light through LITE-1, a unique photoreceptor protein that belongs to the invertebrate taste receptor family. However, it remains unclear how LITE-1 is regulated. Here, we performed a forward genetic screen for genes that when mutated suppress LITE-1 function. One group of lite-1 suppressors are the genes required for producing the two primary antioxidants thi ...[more]

PMID: 33301443

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Project description:The regulatory mechanisms by which hydrogen peroxide (H2O2) modulates the activity of transcription factors in bacteria (OxyR and PerR), lower eukaryotes (Yap1, Maf1, Hsf1 and Msn2/4) and mammalian cells (AP-1, NRF2, CREB, HSF1, HIF-1, TP53, NF-κB, NOTCH, SP1 and SCREB-1) are reviewed. The complexity of regulatory networks increases throughout the phylogenetic tree, reaching a high level of complexity in mammalians. Multiple H2O2 sensors and pathways are triggered converging in the regulation of transcription factors at several levels: (1) synthesis of the transcription factor by upregulating transcription or increasing both mRNA stability and translation; (ii) stability of the transcription factor by decreasing its association with the ubiquitin E3 ligase complex or by inhibiting this complex; (iii) cytoplasm-nuclear traffic by exposing/masking nuclear localization signals, or by releasing the transcription factor from partners or from membrane anchors; and (iv) DNA binding and nuclear transactivation by modulating transcription factor affinity towards DNA, co-activators or repressors, and by targeting specific regions of chromatin to activate individual genes. We also discuss how H2O2 biological specificity results from diverse thiol protein sensors, with different reactivity of their sulfhydryl groups towards H2O2, being activated by different concentrations and times of exposure to H2O2. The specific regulation of local H2O2 concentrations is also crucial and results from H2O2 localized production and removal controlled by signals. Finally, we formulate equations to extract from typical experiments quantitative data concerning H2O2 reactivity with sensor molecules. Rate constants of 140 M(-1) s(-1) and ≥1.3 × 10(3) M(-1) s(-1) were estimated, respectively, for the reaction of H2O2 with KEAP1 and with an unknown target that mediates NRF2 protein synthesis. In conclusion, the multitude of H2O2 targets and mechanisms provides an opportunity for highly specific effects on gene regulation that depend on the cell type and on signals received from the cellular microenvironment.

Project description:The aim of this study was to gain insight into the compartment-specific roles of ascorbate and glutathione in leaf senescence in Arabidopsis thaliana. The subcellular distribution of ascorbate, glutathione, and hydrogen peroxide (H2O2) was analyzed by transmission electron microscopy and correlated with the activity of antioxidative enzymes in wildtype plants and the ascorbate- and glutathione-deficient mutants vtc2-1 and pad2-1, respectively. Both mutants showed earlier and stronger senescence than the wildtype indicating the importance of a functioning ascorbate and glutathione cycle in the induction and regulation of senescence. Glutathione levels dropped drastically and up to 93 % in all cell compartments of wildtype plants and the vtc2-1 mutant within the first day of dark-induced senescence while ascorbate contents remained unchanged until the very end. Glutathione contents in mitochondria of pad2-1 mutants decreased more slowly over the first 7 days than compared to the other plants indicating an important role of glutathione in mitochondria in this mutant during senescence. The strongest decrease (84 %) of glutathione contents in wildtype plants at this time point was found in mitochondria indicating an important role of mitochondria for the induction of senescence and cell death events. Due to the general decrease of the antioxidative capacity, a strong accumulation of H2O2 was observed in cell walls, plastids, and the cytosol in all plants. Activities of glutathione reductase, dehydroascorbate reductase and catalase were strongly reduced while ascorbate peroxidase and monodehydroascorbate reductase were increased. The initial rapid drop of glutathione levels seemed to be the trigger for senescence, while ascorbate appeared to be the key factor in regulating senescence through controlling H2O2 levels by the oxidation of reduced ascorbate to monodehydroascorbate and the subsequent reduction to ascorbate by monodehydroascorbate reductase.

Dataset Information

Regulation of photosensation by hydrogen peroxide and antioxidants in C. elegans.

Publications

Regulation of photosensation by hydrogen peroxide and antioxidants in C. elegans.

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