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. 2022 Apr 4;27(7):2332.
doi: 10.3390/molecules27072332.

Protective Effect of Djulis (Chenopodium formosanum) Extract against UV- and AGEs-Induced Skin Aging via Alleviating Oxidative Stress and Collagen Degradation

Jia-Ling Lyu  1   2   3 , Yi-Jung Liu  1   2   4 , Kuo-Ching Wen  2 , Chen-Yuan Chiu  5 , Yung-Hsiang Lin  6 , Hsiu-Mei Chiang  1   2
Affiliations

Protective Effect of Djulis (Chenopodium formosanum) Extract against UV- and AGEs-Induced Skin Aging via Alleviating Oxidative Stress and Collagen Degradation

Jia-Ling Lyu et al. Molecules. .

Abstract

Skin aging is a complex process involving photoaging and glycation stress, which share some fundamental pathways and have common mediators. They can cause skin damage and collagen degradation by inducing oxidative stress and the accumulation of reactive oxygen species (ROS). Chenopodium formosanum (CF), also known as Djulis, is a traditional cereal in Taiwan. This study investigated the protection mechanisms of CF extract against ultraviolet (UV) radiation and advanced glycation end products (AGEs)-induced stress. The results indicated that CF extract had strong antioxidant and free radical scavenging effects. It could reduce UV-induced intracellular ROS generation and initiate the antioxidant defense system by activating the nuclear factor erythroid 2-related factor 2 (Nrf2)/heme oxygenase-1 (HO-1) signaling pathway in human skin fibroblasts. CF extract modulated mitogen-activated protein kinase (MAPK) and transformed growth factor-beta (TGF-β) signaling pathways to alleviate oxidative stress-induced skin aging. Moreover, the results revealed that CF extract not only promoted collagen synthesis but also improved aging-induced collagen degradation. CF extract attenuated AGEs-induced ROS production and the upregulation of receptor for AGEs (RAGE). The overall results suggest that CF extract provides an effective anti-aging strategy by preventing skin damage from oxidative stress and collagen loss with potent antioxidant, anti-photoaging, and antiglycation activities.

Keywords: Chenopodium formosanum; Djulis; advanced glycation end products; glycation stress; reactive oxygen species; ultraviolet radiation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(a) DPPH free radical scavenging activity (%); (b) reducing capability (%); (c) superoxide anion radical scavenging activity (%); (d) hydrogen peroxide scavenging activity (%); (e) hydroxyl radical scavenging activity (%) and (f) ferrous ion chelating activity (%) of CF extract. Significant difference versus control group: *, p < 0.05; **, p < 0.01; ***, p < 0.001.
Figure 2
Figure 2
Cell viability (%) of human skin fibroblasts treated with (a) a series of concentrations of CF extract; (b) various UVB doses and (c) CF extract on UV radiation. Significant difference versus non-irradiated group: ###, p < 0.001. Significant difference versus UVB-irradiated group: *, p < 0.05; ***, p < 0.001.
Figure 3
Figure 3
The effects of CF extract on UVB-induced intracellular ROS generation in human skin fibroblasts (scale bar = 50 µm). Significant difference versus non-irradiated group: ###, p < 0.001. Significant difference versus UVB-irradiated group: **, p < 0.01.
Figure 4
Figure 4
The effects of CF extract on UVB-induced Nrf2, Keap1 and HO-1 expression in human skin fibroblasts. Significant difference versus non-irradiated group: ###, p < 0.001. Significant difference versus UVB-irradiated group: *, p < 0.05; ***, p < 0.001.
Figure 5
Figure 5
The effects of CF extract on UVB-induced nuclear translocation of Nrf2 in human skin fibroblasts (scale bar = 50 µm).
Figure 6
Figure 6
The effects of CF extract on UVB-induced MMP-1, -3, -9 and TIMP-1 expression in human skin fibroblasts. Significant difference versus non-irradiated group: ##, p < 0.01; ###, p < 0.001. Significant difference versus UVB-irradiated group: **, p < 0.01; ***, p < 0.001.
Figure 7
Figure 7
The effects of CF extract on UVB-induced expression of (a) AP-1 and (b) MAPK in human skin fibroblasts. Significant difference versus non-irradiated group: ###, p < 0.001. Significant difference versus UVB-irradiated group: *, p < 0.05; **, p < 0.01; ***, p < 0.001.
Figure 8
Figure 8
The effects of CF extract on UVB-inhibited TGF-β and Smad3 expression in human skin fibroblasts. Significant difference versus non-irradiated group: ###, p < 0.001. Significant difference versus UVB-irradiated group: **, p < 0.01; ***, p < 0.001.
Figure 9
Figure 9
The effects of CF extract on CML-treated intracellular ROS generation in human skin fibroblasts. Significant difference versus non-treated group: ###, p < 0.001. Significant difference versus CML-treated group: *, p < 0.05; **, p < 0.01.
Figure 10
Figure 10
The effects of CF extract on CML-treated RAGE expression in human skin fibroblasts. Significant difference versus non-treated group: ###, p < 0.001. Significant difference versus CML-treated group: *, p < 0.05; **, p < 0.01; ***, p < 0.001.
Figure 11
Figure 11
The effects of CF extract on (a) type I pro-collagen expression and (b) total collagen content in human skin fibroblasts. Significant difference versus non-treated group: *, p < 0.05; **, p < 0.01; ***, p < 0.001.
Figure 12
Figure 12
The effects of CF extract on total collagen content of (a) UVB-irradiated and (b) CML-treated groups. (c) Immunofluorescence staining of collagen in human skin fibroblasts (scale bar = 25 µm). Significant difference versus control group: ##, p < 0.01. Significant difference versus UVB-irradiated or CML-treated group: *, p < 0.05; **, p < 0.01; ***, p < 0.001.
Figure 13
Figure 13
Hypothetical model of CF-mediated defense pathways against UV and AGEs-induced oxidative stress and collagen degradation in Hs68 cells. (↑, up-regulation; ↓, down-regulation).
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