An unusual vitamin E constituent (alpha-tocomonoenol) provides enhanced antioxidant protection in marine organisms adapted to cold-water environments

Abstract

A new vitamin E constituent having an unusual methylene unsaturation at the isoprenoid-chain terminus of alpha-tocopherol (alpha-Toc) was isolated from chum salmon eggs and was found to have identical antioxidant activity as does alpha-Toc in methanol or liposomal suspension at 37 degrees C. Here we report that this marine-derived tocopherol (MDT) is broadly distributed with alpha-Toc in the tissue of marine fish, and that the MDT composition of total vitamin E is greater in the flesh of cold-water salmon (12-20%) than in that of tropical fish (< or =2.5%). Vitamin E analysis of cultured masu salmon maintained on a MDT-deplete diet showed substantially less MDT content than native masu salmon, suggesting a trophic origin of MDT. This contention is supported by the finding of MDT in marine plankton from the cold waters of Hokkaido. We found that MDT inhibited peroxidation of cholesterol-containing phosphatidylcholine liposomes to a greater extent than did alpha-Toc at 0 degrees C. Furthermore, the ratios of the rate constants for MDT and alpha-Toc to scavenge peroxyl radicals increased with decreasing rates of radical flux in liposomes and fish oil at 0 degrees C, indicating that the enhanced activity of MDT at low temperature is attributed to its greater rate of diffusion in viscous lipids. These results suggest that MDT production, or its trophic accumulation, may reduce lipid peroxidation in marine organisms functionally adapted to cold-water environments.

Figure 1

Chemical structures for the α forms of vitamin E.

Figure 2

RP-HPLC with electrochemical detection chromatogram for the separation of δ-tocopherol, MDT, α-tocomonoenol, γ-tocopherol, and α-Toc in a hexane extract of human plasma.

Scheme 1

Figure 3

Formation of soyPC hydroperoxide (PC-OOH) during 0.5 μM benzophenone-sensitized photooxidation of 5 mM soyPC multilamellar liposomes containing 5 mM cholesterol at 0°C with 5 μM MDT or α-Toc. Vertical bars indicate SD (n = 3). The average rate of LOO⋅ formation was calculated as 86.3 pM/s from the rate of MDT or α-Toc consumption. (Inset) Data scaled to show the control rate of oxidation without the addition of vitamin E antioxidants.

Figure 4

Dependence in the reactivities of MDT and α-Toc expressed as k′/k ratios on LOO⋅ flux during the benzophenone-sensitized photooxidation of 5 mM soyPC multilamellar liposomes containing 5 mM cholesterol, and of neat fish oil, at 0°C. Tocopherol oxidation rates decreased with decreasing concentrations of benzophenone; maximum concentrations were 5 μM and 0.65 μM for the oxidation of soyPC liposome and fish oil, respectively. The rate of LOO⋅ formation was calculated by the rate of the total vitamin E (MDT and α-Toc) consumption.