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Fomenko S. E., Kushnerova N. F., Sprygin V. G., Drugova E. S., Lesnikova L. N., Merzlyakov V. Yu. Assessment of antioxidant activity of seaweed extracts from the Sea of Japan in vitro and in vivo. Marine Biological Journal, 2023, vol. 8, no. 2, pp. 91-103. https://doi.org/10.21072/mbj.2023.08.2.06

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Abstract

Seaweeds are a source of important biologically active substances: lipids, amino acids, phenolic compounds, polycarbohydrates, etc. Polyphenolic compounds are one of the perspective groups of constituents of marine origin with high antioxidant activity; those play a key role in the life of marine macrophytes, allowing them to quickly respond to external stress and to perform protective functions. At the same time, the multicomponent composition of the phenolic fraction of the seaweed extract provides a wide spectrum of its pharmacological activity, inter alia a regulatory effect on numerous homeostasis disorders occurring during pathological processes in humans and animals. Wherein, the available opportunities for the practical use of seaweed extracts have not yet been depleted, and this is of undoubted interest for modern science. The aim of the work was to carry out a comparative assessment of the antioxidant activity of hydroalcoholic extracts isolated from the thalli of three classes of algae [brown (Sargassum pallidum), green (Ulva lactuca), and red (Ahnfeltia fastigiata var. tobuchiensis)] and to analyze their effect on indices of the endogenous antioxidant system of liver and blood in mice under experimental stress. Seaweeds were sampled in summer in the coastal waters of the Peter the Great Bay (the Sea of Japan). Sampled seaweeds were dried at a temperature of about +50 °C, grinded in a laboratory mill to particles 0.5–1 mm in size, and extracted with 70% ethanol via repercolation. In the extract of the brown alga S. pallidum, the highest content of polyphenols was recorded – (218.2 ± 20.3) mg-Eq GA·g−1 dry weight. In the extract of the green alga U. lactuca, the value was (16.2 ± 1.8) mg-Eq GA·g−1 dry weight; in the extract of the red alga A. fastigiata var. tobuchiensis, (9.1 ± 1.6) mg-Eq GA·g−1 dry weight. Accordingly, the antiradical activity of S. pallidum extract towards the cation radical ABTS+ and the alkyl peroxyl radical was significantly higher than that of U. lactuca and A. fastigiata var. tobuchiensis extracts. The effect of these seaweed extracts on the antioxidant defense indices of liver and plasma in mice under acute stress was studied experimentally. Weight indicators (weight of animals and weight coefficients of their internal organs) and biochemical indices (level of antiradical activity, malondialdehyde and reduced glutathione content, and activity of antioxidant enzymes) were established. The experiment was carried out on white outbred male mice (weight of 20–30 g). To model conditions of acute stress, mice were fixed vertically by the dorsal neck crease for 24 h. Alcohol-free seaweed extracts were injected into mice stomachs as an aqueous suspension (a dose of 100 mg of total polyphenols per kg of body weight) through a tube twice: right before vertical fixation and in 6 h. Into stomachs of the animals of the control and the “stress” groups, distilled water was injected in a volume equal to that of the injected extracts. In this model, all the attributes of stress manifested themselves: adrenal hypertrophy, involution of the thymus and spleen, and ulceration of the gastric and intestinal mucosa. Moreover, disturbances of the antioxidant defense system were recorded: a decrease of antioxidant enzymes activity in blood plasma, a drop in reduced glutathione content in liver, and an increase of the malondialdehyde level. Under the effect of the extracts, in all the groups of animals under stress, a tendency to stabilization of the studied antioxidant defense indices was observed. Interestingly, the values in mice receiving U. lactuca and A. fastigiata var. tobuchiensis extracts were inferior to those in the group of animals receiving S. pallidum extract. In the latter group of mice, there were no significant differences from the control values in terms of antioxidant defense indices. This is due to the fact the main components of the polyphenolic fractions of green and red algae are monomeric flavonoids, while brown algae contain high molecular weight phlorotannins. The latter ones are characterized by higher antioxidant activity than low molecular weight polyphenolic fractions of green and red algae.

Authors

S. E. Fomenko

leading researcher, PhD

https://orcid.org/0000-0002-0261-0190

https://elibrary.ru/author_items.asp?id=109637

N. F. Kushnerova

head of the laboratory, D. Sc.

https://orcid.org/0000-0002-6476-0039

https://elibrary.ru/author_items.asp?id=109633

V. G. Sprygin

leading researcher, PhD

https://orcid.org/0000-0001-7400-909X

https://elibrary.ru/author_items.asp?id=109634

E. S. Drugova

researcher, PhD

https://orcid.org/0000-0002-7472-5958

https://elibrary.ru/author_items.asp?id=551142

L. N. Lesnikova

researcher, PhD

https://orcid.org/0000-0003-4187-230X

https://elibrary.ru/author_items.asp?id=551105

V. Yu. Merzlyakov

researcher

https://orcid.org/0000-0002-9536-3247

https://elibrary.ru/author_items.asp?id=551122

References

Боголицын К. Г., Дружинина А. С., Овчинников Д. В., Каплицин П. А., Шульгина Е. В., Паршина А. Э. Полифенолы бурых водорослей // Химия растительного сырья. 2018. № 3. С. 5–21. [Bogolitsyn K. G., Druzhinina A. S., Ovchinnikov D. V., Kaplitsyn P. A., Shulgin E. V., Parshina A. E. Polyphenols of brown algae. Khimiya rastitel’nogo syr’ya, 2018, no. 3, pp. 5–21. (in Russ.)]. https://doi.org/10.14258/jcprm.2018031898

Венгеровский А. И., Маркова И. В., Саратиков А. С. Доклиническое изучение гепатозащитных средств // Ведомости фармакологического комитета. 1999. № 2. С. 9–12. [Vengerovsky A. I., Markova I. V., Saratikov A. S. Doklinicheskoe izuchenie gepatozashchitnykh sredstv. Vedomosti farmakologicheskogo komiteta, 1999, no. 2, pp. 9–12. (in Russ.)]

Имбс Т. И., Звягинцева Т. Н. Флоротаннины – полифенольные метаболиты бурых водорослей // Биология моря. 2018. Т. 44, № 4. С. 217–227. [Imbs T. I., Zvyagintseva T. N. Phlorotannins are polyphenolic metabolites of brown algae. Biologiya morya, 2018, vol. 44, no. 4, pp. 217–227. (in Russ.)]. https://doi.org/10.1134/S0134347518040010

Кушнерова Н. Ф., Спрыгин В. Г., Фоменко С. Е., Рахманин Ю. А. Влияние стресса на состояние липидного и углеводного обмена печени, профилактика // Гигиена и санитария. 2005. № 5. С. 17–21. [Kushnerova N. F., Sprygin V. G., Fomenko S. Ye., Rakhmanin Yu. A. Impact of stress on hepatic lipid and carbohydrate metabolism, prevention. Gigiena i sanitariya, 2005, no. 5, pp. 17–21. (in Russ.)]

Кушнерова Н. Ф., Фоменко С. Е., Спрыгин В. Г., Момот Т. В. Влияние липидного комплекса экстракта из морской красной водоросли Ahnfeltia tobuchiensis (Kanno et Matsubara) Makienko на биохимические показатели плазмы крови и мембран эритроцитов при экспериментальном стрессе // Биология моря. 2020. Т. 46, № 4. С. 269–276. [Kushnerova N. F., Fomenko S. E., Sprygin V. G., Momot T. V. The effects of the lipid complex of extract from the marine red alga Ahnfeltia tobuchiensis (Kanno et Matsubara) Makienko on the biochemical parameters of blood plasma and erythrocyte membranes during experimental stress exposure. Biologiya morya, 2020, vol. 46, no. 4, pp. 269–276. (in Russ.)]. https://doi.org/10.31857/S0134347520040051

Спрыгин В. Г., Кушнерова Н. Ф., Фоменко С. Е., Сизова Л. А., Момот Т. В. Гепатопротекторные свойства экстракта из бурой водоросли Saccharina japonica // Биология моря. 2013. Т. 39, № 1. С. 50–54. [Sprygin V. G., Kushnerova N. F., Fomenko S. E., Sizova L. A., Momot T. V. The hepatoprotective properties of an extract from the brown alga Saccharina japonica. Biologiya morya, 2013, vol. 39, no. 1, pp. 50–54. (in Russ.)]

Спрыгин В. Г., Кушнерова Н. Ф., Фоменко С. Е., Другова Е. С., Лесникова Л. Н., Мерзляков В. Ю., Момот Т. В. Влияние экстракта из морской бурой водоросли Sargassum pallidum (Turner) C. Agardh, 1820 на метаболические реакции печени при экспериментальном токсическом гепатите // Биология моря. 2017. Т. 43, № 6. С. 444–449. [Sprygin V. G., Kushnerova N. F., Fomenko S. E., Drugova E. S., Lesnikova L. N., Merzlyakov V. Y., Momot T. V. The influence of an extract from the marine brown alga Sargassum pallidum on the metabolic reactions in the liver under experimental toxic hepatitis. Biologiya morya, 2017, vol. 43, no. 6, pp. 444–449. (in Russ.)]

Фоменко С. Е., Кушнерова Н. Ф., Спрыгин В. Г., Другова Е. С., Лесникова Л. Н., Мерзляков В. Ю. Липидный состав и мембранопротекторное действие экстракта из морской зелёной водоросли Ulva lactuca (L.) // Химия растительного сырья. 2019. № 3. С. 41–51. [Fomenko S. E., Kushnerova N. F., Sprygin V. G., Drugova E. S., Lesnikova L. N., Merzlyakov V. Yu. Lipid composition and membranoprotective action of extract from marine green algae Ulva lactuca (L.). Khimiya rastitel’nogo syr’ya, 2019, no. 3, pp. 41–51. (in Russ.)]. https://doi.org/10.14258/jcprm.2019035116

Agregán R., Munekata P. E. S., Franco D., Carballo J., Barba F. J., Lorenzo J. M. Antioxidant potential of extracts obtained from macro- (Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcata) and micro-algae (Chlorella vulgaris and Spirulina platensis) assisted by ultrasound. Medicines, 2018, vol. 5, iss. 2, art. no. 33 (9 p.). https://doi.org/10.3390/medicines5020033

Alagan V. T., Valsala R. N., Rajesh K. D. Bioactive chemical constituent analysis, in vitro antioxidant and antimicrobial activity of whole plant methanol extracts of Ulva lactuca Linn. British Journal of Pharmaceutical Research, 2017, vol. 15, no. 1, pp. 1–14. https://doi.org/10.9734/BJPR/2017/31818

Bartosz G., Janaszewska A., Ertel D., Bartosz M. Simple determination of peroxyl radical-trapping capacity. Biochemistry and Molecular Biology International, 1998, vol. 46, iss. 3, pp. 519–528. https://doi.org/10.1080/15216549800204042

Buege J. A., Aust S. D. Microsomal lipid peroxidation. In: Biomembranes. Part C, Biological Oxidants, Microsomal, Cytochrome P-450, and Other Hemoprotein Systems / F. Sidney, P. Lester (Eds). New York : Academic Press, 1978, pp. 302–310. (Methods in Enzymology ; vol. 52). https://doi.org/10.1016/s0076-6879(78)52032-6

Burk R. F., Lawrence R. A., Lane J. M. Liver necrosis and lipid peroxidation in the rat as the result of paraquat and diquat administration: Effect of selenium deficiency. The Journal of Clinical Investigation, 1980, vol. 65, iss. 5, pp. 1024–1031. https://doi.org/10.1172/JCI109754

Chrousos G. P. Stress and disorders of the stress system. Nature Reviews Endocrinology, 2009, no. 5, pp. 374–381. https://doi.org/10.1038/nrendo.2009.106

Cotas J., Leandro A., Monteiro P., Pacheco D., Figueirinha A., Gonçalves A. M. M., da Silva G. J., Pereira L. Seaweed phenolics: From extraction to applications. Marine Drugs, 2020, vol. 18, iss. 8, pp. 384–431. https://doi.org/10.3390/md18080384

de Quirós A. R.-B., Lage-Yusty M. A., López-Hernández J. Determination of phenolic compounds in macroalgae for human consumption. Food Chemistry, 2010, vol. 121, iss. 2, pp. 634–638. https://doi.org/10.1016/j.foodchem.2009.12.078

Ellman G. L. Tissue sulfhydryl group. Archives of Biochemistry and Biophysics, 1959, vol. 82, iss. 1, pp. 70–77. https://doi.org/10.1016/0003-9861(59)90090-6

European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes. Strasbourg : Council of Europe, 1986, 11 p. (European Treaty Series ; no. 123). URL: https://rm.coe.int/168007a67b [accessed: 28.12.2021].

Ferreres F., Lopes G., Gil-Izquierdo A., Andrade P. B., Sousa C., Mouga T., Valentão P. Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESI-MSn: Approaches to hyaluronidase inhibitory capacity and antioxidant properties. Marine Drugs, 2012, vol. 10, iss. 12, pp. 2766–2781. https://doi.org/10.3390/md10122766

Goldberg D. M., Spoone R. J. Assay of glutathione reductase. In: Methods of Enzymatic Analysis. Vol. 3: Enzymes 1. Oxidoreductases, transferases. 3rd edition / H. U. Bergmeyer (Ed.). Weinheim : Verlag Chemie, 1983, pp. 258–265.

Manach C., Scalbert A., Morand C., Rémésy C., Jiménez L. Polyphenols: Food sources and bioavailability. The American Journal of Clinical Nutrition, 2004, vol. 79, iss. 5, pp. 727–747. https://doi.org/10.1093/ajcn/79.5.727

Michalak I., Chojnacka K. Algae as production systems of bioactive compounds. Engineering in Life Sciences, 2015, vol. 15, iss. 2, pp. 160–176. https://doi.org/10.1002/elsc.201400191

Paoletti F., Aldinucci D., Mocali A., Caparrini A. A sensitive spectrophotometric method for the determination of superoxide-dismutase activity in tissue extracts. Analytical Biochemistry, 1986, vol. 154, iss. 2, pp. 536–541. https://doi.org/10.1016/0003-2697(86)90026-6

Parys S., Rosenbaum A., Kehraus S., Reher G., Glombitza K.-W., König G. M. Evaluation of quantitative methods for the determination of polyphenols in algal extracts. Journal of Natural Products, 2007, vol. 70, iss. 12, pp. 1865–1870. https://doi.org/10.1021/np070302f

Pradhan B., Patra S., Behera C., Nayak R., Jit B. P., Ragusa A., Jena M. Preliminary investigation of the antioxidant, anti-diabetic, and anti-inflammatory activity of Enteromorpha intestinalis extracts. Molecules, 2021, vol. 26, iss. 4, pp. 1171–1187. https://doi.org/10.3390/molecules26041171

Ragan M. A., Glombitza K. W. Phlorotannins, brown algal polyphenols. In: Progress in Phycological Research. Bristol : Biopress Ltd, 1986, vol. 4, pp. 129–241.

Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 1999, vol. 26, iss. 9–10, pp. 1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3

Şahın E., Gümüşlü S. Stress-dependent induction of protein oxidation, lipid peroxidation and anti-oxidants in peripheral tissues of rats: Comparison of three stress models (immobilization, cold and immobilization–cold). Clinical and Experimental Pharmacology and Physiology, 2007, vol. 34, iss. 5–6, pp. 425–431. https://doi.org/10.1111/j.1440-1681.2007.04584.x

Shibata T., Kawaguchi S., Hama Y., Inagaki M., Yamaguchi K., Nakamura T. Local and chemical distribution of phlorotannins in brown algae. Journal of Applied Phycology, 2004, vol. 16, pp. 291–296. https://doi.org/10.1023/B:JAPH.0000047781.24993.0a

Skriptsova A. V., Zhigadlova G. G. A revision of the red algal genus Ahnfeltia on the Russian coast of the North Pacific. Phycologia, 2022, vol. 61, iss. 4, pp. 396–402. https://doi.org/10.1080/00318884.2022.2061154

Wang T., Jónsdóttir R., Liu H., Gu L., Kristinsson H. G., Raghavan S., Ólafsdóttir G. Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. Journal of Agricultural and Food Chemistry, 2012, vol. 60, iss. 23, pp. 5874–5883. https://doi.org/10.1021/jf3003653

Zhong B., Robinson N. A., Warner R. D., Barrow C. J., Dunshea F. R., Suleria H. A. R. LC-ESI-QTOF-MS/MS characterization of seaweed phenolics and their antioxidant potential. Marine Drugs, 2020, vol. 18, iss. 6, pp. 331–352. https://doi.org/10.3390/md18060331

Funding

This work was carried out within the framework of the state research assignment of V. I. Il’ichev Pacific Oceanological Institute FEB RAS “Ecological and biogeochemical processes in marine ecosystems: The role of natural and anthropogenic factors” (0211-2021-0014, registration number 121-21500052-9).

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