Singlet molecular oxygen-quenching activity of carotenoids: relevance to protection of the skin from photoaging

Abstract

Carotenoids are known to be potent quenchers of singlet molecular oxygen [O(2) ((1)Δ(g))]. Solar light-induced photooxidative stress causes skin photoaging by accelerating the generation of reactive oxygen species via photodynamic actions in which O(2) ((1)Δ(g)) can be generated by energy transfer from excited sensitizers. Thus, dietary carotenoids seem to participate in the prevention of photooxidative stress by accumulating as antioxidants in the skin. An in vivo study using hairless mice clarified that a O(2) ((1)Δ(g)) oxygenation-specific peroxidation product of cholesterol, cholesterol 5α-hydroperoxide, accumulates in skin lipids due to ultraviolet-A exposure. Matrix metalloproteinase-9, a metalloproteinase family enzyme responsible for the formation of wrinkles and sagging, was enhanced in the skin of ultraviolet-A -irradiated hairless mice. The activation of metalloproteinase-9 and the accumulation of 5α-hydroperoxide, as well as formation of wrinkles and sagging, were lowered in mice fed a β-carotene diet. These results strongly suggest that dietary β-carotene prevents the expression of metalloproteinase-9 (at least in part), by inhibiting the photodynamic action involving the formation of 5α-hydroperoxide in the skin. Intake of β-Carotene therefore appears to be helpful in slowing down ultraviolet-A -induced photoaging in human skin by acting as a O(2) ((1)Δ(g)) quencher.

Keywords: carotenoids; cholesterol hydroperoxide; matrix metalloproteinase; photoaging; singlet molecular oxygen.

Fig. 1

O₂ (¹Δ_g)-generating reactions in biological systems. ¹O₂: O₂ (¹Δ_g).

Fig. 2

Major pathways of cholesterol oxidation in biological systems. ¹O₂: O₂ (¹Δ_g).

Fig. 3

Structures of primary oxidation n products of β-carotene with reactive oxygen species. ¹O₂: O₂ (¹Δ_g).

Fig. 4

Effect of ultraviolet-A (UVA) irradiation on the accumulation of primary oxidation products of β-carotene in the skin of hairless mice. A: HPLC chromatogram of β-carotene oxidation product standards and extracts from skin tissue. B: Comparison of the concentrations of primary oxidation products from mouse skin with and without UVA irradiation. Hos: HR-1 hairless mice (male, 8 weeks of age) were fed a diet containing β-carotene (50 mg/100 g diet) and α-tocopherol (5 mg/100 g diet) for 3 weeks. The mice covered with leather on half of their back received UVA light at 47 J/cm² on one occasion. Irradiated and non-irradiated areas were obtained after 12 h from the irradiation period, extracted with ethanol/hexane (1/1 vol) and analyzed using HPLC equipped with an ODS-80Ts column (4.6 × 250 mm) (Tosoh Company, Tokyo, Japan) and a mobile phase consisting of methanol/acetonitrile/dichloromethane/water (7/7/2/0.16 by vol.) at 450 nm.

Fig. 5

Proposed relationship between dietary β-carotene and peroxidation of cholesterol in ultraviolet-A (UVA)-induced skin photoaging. ¹O₂: O₂ (¹Δ_g), Chol 5α-OOH: Cholesterol 5α-hydroperoxide, Chol 7α/β-OOH: 7α/β-hydroperoxide, MMP: matrix metalloproteinase.