Abstract
The effect of a lipid extract isolated from the marine green algae Codium fragile (Suringar) Hariot on the liver and blood biochemical indicators in mice under the impact of acute stress (vertical fixation by the dorsal neck fold) was studied. The pharmacological effect of the C. fragile lipid extract was manifested in the restoration of lipid and carbohydrate metabolism, as well as in the normalization of the indicators of the endogenous antioxidant defense system under the effect of stress. The biological activity of the lipid extract of C. fragile is, probably, due to the action of its constituent polyunsaturated fatty acids of the ω-3 and ω-6 families. The lipid extract of C. fragile was not inferior to the reference Omega-3 preparation in restoring the body’s metabolic reactions caused by the impact of the stress; however, it showed higher antioxidant activity.
Similar content being viewed by others
REFERENCES
Ahn, J., Kim, M.J., Yoo, A., Ahn, J., Ha, T., Jung, C.H., Seo, H.D., and Jang, Y.J., Identifying codium fragile extract components and their effects on muscle weight and exercise endurance, Food Chem., 2021, vol. 353, p. 129463. https://doi.org/10.1016/j.foodchem.2021.129463
Amenta, J.S., A rapid chemical method for quantification of lipids separated by thin-layer chromatography, J. Lipid Res., 1964, vol. 5, pp. 270–272. https://doi.org/10.1016/S0022-2275(20)40251-2
Bligh, E.G. and Dyer, W.J., A rapid method of total lipid extraction and purification, Can. J. Biochem. Phys., 1959, vol. 37, no. 8, pp. 911–917. https://doi.org/10.1139/o59-099
Burk, R.F., Lawrence, R.A., and Lane, J.M., Liver necrosis and lipid peroxidation in the rat as the result of paraquat and diquat administration. effect of selenium deficiency, J. Clin. Invest., 1980, vol. 65, no. 5, pp. 1024–1031. https://doi.org/10.1172/JCI109754
Carreau, J.P. and Dubacq, J.P., Adaptation of a macro-scale method to the micro-scale for fatty acid methyl transesterification of biological lipid extracts, J. Chromatogr., 1978, vol. 151, no. 3, pp. 384–390. https://doi.org/10.1016/S0021-9673(00)88356-9
Chapman, V.J. and Chapman, D.J., Seaweeds and Their Uses, New York, NY, USA: Chapman and Hall, 1980, 3rd ed. https://doi.org/10.1007/978-94-009-5806-7
Christie, W.W., Equivalent chain-lengths of methyl ester derivatives of fatty acids on gas chromatography: a reappraisal, J. Chromatogr., 1988, vol. 447, pp. 305–314. https://doi.org/10.1016/0021-9673(88)90040-4
Chrousos, G.P., Stress and disorders of the stress system, Nat. Rev. Endocrinol., 2009, no. 5, pp. 374–381. https://doi.org/10.1038/nrendo.2009.106
European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (ETS No. 123), Strasbourg, 1986. http://conventions.coe.int.
Folch, J., Less, M., and Sloane-Stanley, G.H., A simple method for the isolation and purification of total lipids from animal tissues, J. Biol. Chem., 1957, vol. 226, no. 1, pp. 497–509. https://doi.org/10.1016/S0021-9258(18)64849-5
Fomenko, S.E., Kushnerova, N.F., Sprygin, V.G., and Momot, T.V., Disturbance of metabolic processes in the liver of rats under the influence of stress, Tikhookean. Med. Zh., 2013, no. 2, pp. 67–70.
Fomenko, S.E., Kushnerova, N.F., Sprygin, V.G., and Momot, T.V., The antioxidant and stress-protective properties of an extract from the green alga Ulva lactuca Linnaeus, 1753, Russ. J. Mar. Biol., 2016, vol. 42, no. 6, pp. 509–514. https://doi.org/10.1134/S1063074016060031
Van Gent, C.M., Roseleur, O.J., and Van Der Bijl, P., The detection of cerebrosides on thin-layer chromatograms with an anthrone spray reagent, J. Chromatogr., 1973, vol. 85, no. 1, pp. 174–176. https://doi.org/10.1016/S0021-9673(01)91884-9
Goecke, F., Hernandez, V., Bittner, M., Gonzalez, M., Becerra, J., and Silva, M., Fatty acid composition of three species of Codium (Bryopsidales, Chlorophyta) in Chile, Rev. Biol. Mar. Oceanogr., 2010, vol. 45, no. 2, pp. 325–330. https://doi.org/10.4067/S0718-19572010000200014
Gurskaya, A.I., Otvalko, E.A., Yatskovskaya, N.M., and Chirkin, A.A., Biochemical criteria of acute and chronic stress during immobilization of rats, Vestn. VDU, 2017, vol. 98, no. 1, pp. 61–65.
Harris, W.S., Miller, M., Tighe, A.P., Davidson, M.H., and Schaefer, E.J., Omega-3 fatty acids and coronary heart disease risk: clinical and mechanistic perspectives, Atherosclerosis, 2008, vol. 197, pp. 12–24. https://doi.org/10.1016/j.atherosclerosis.2007.11.008
Hulbert, A.I., Turner, N., Storlien, L.H., and Else, P.L., Dietary fats and membrane function: implications for metabolism and disease, Biol. Rev. Camb. Philos. Soc., 2005, vol. 80, no. 1, pp. 155–169. https://doi.org/10.1017/s1464793104006578
Jump, D.B., Depner, C.M., Tripathy, S., and Lytle, K.A., Potential for dietary omega-3 fatty acids to prevent nonalcoholic fatty liver disease and reduce the risk of primary liver cancer, Adv. Nutr., 2015, vol. 6, no. 6, pp. 694–702. https://doi.org/10.3945/an.115.009423
Karpishchenko, A.I., Alipov, A.N., and Alekseev, V.V., Meditsinskie laboratornye tekhnologii. Rukovodstvo po klinicheskoi laboratornoi diagnostike (Medical Laboratory Technologies. Manual of Clinical Laboratory Diagnostics), GEOTAR-Media, 2013, vol. 2.
Khan, S.A. and Makki, A., Dietary changes with omega-3 fatty acids improves the blood lipid profile of Wistar albino rats with hypercholesterolaemia, Int. J. Med. Res. Health Sci., 2017, vol. 6, no. 3, pp. 34–40.
Khotimchenko, S.V., Lipidy morskikh vodoroslei-makrofitov i trav. Struktura, raspredelenie, analiz (Lipids from Macrophyte Seaweeds and Herbs: Structure, Distribution, and Analysis), Vladivostok: Dal’nauka, 2003.
Khotimchenko, S., Vaskovsky, V., and Titlyanova, T., Fatty acids of marine algae from the pacific coast of North California, Bot. Mar., 2002, vol. 45, pp. 17–22. https://doi.org/10.1515/BOT.2002.003
Kim, J., Choi, J.H., Oh, T., Ahn, B., and Unno, T., Codium fragile ameliorates high-fat diet-induced metabolism by modulating the gut microbiota in mice, Nutrient, 2020, vol. 12, p. 1848. https://doi.org/10.3390/nu12061848
Komal, F., Khan, M.K., Imran, M., Ahmad, M.H., Anwar, H., Ashfaq, U.A., Ahmad, N., Masroor, A., Ahmad, R.S., Nadeem, M., and Nisa, M.U., Impact of different omega-3 fatty acid sources on lipid, hormonal, blood glucose, weight gain and histopathological damages profile in PCOS rat model, J. Transl. Med., 2020, vol. 18, pp. 349–360. https://doi.org/10.1186/s12967-020-02519-1
Kushnerova, N.F., Sprygin, V.G., Fomenko, S.E., and Rakhmanin, Yu.A., The influence of stress on the state of lipid and carbohydrate metabolism of the liver, prevention, Gig. Sanit., 2005, no. 5, pp. 17–21.
Kushnerova, N.F., Fomenko, S.E., Sprygin, V.G., and 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, Russ. J. Mar. Biol., 2020, vol. 46, no. 4, pp. 277–283. https://doi.org/10.1134/S1063074020040057
Lee, C., Park, G.H., Ahn, E.M., Kim, B.A., Park, C.I., and Jang, J.H., Protective effect of Codium fragile against UVB-induced pro-inflammatory and oxidative damages in HaC-aT cells and BALB/c mice, Fitoterapia, 2013, vol. 86, pp. 54–63. https://doi.org/10.1016/j.fitote.2013.01.020
Nieto, N., Fernandez, M.I., Torres, M.I., Ríos, A., and Suarez, M.D., Dietary monounsaturated n-3 and n-6 long-chain polyunsaturated fatty acids affect cellular antioxidant defense system in rats with experimental ulcerative colitis induced by trinitrobenzene sulfonic acid, Gil. Dig. Dis. Sci., 1998, vol. 43, no. 12, pp. 2678–2687. https://doi.org/10.1023/a:1026655311878
Novgorodtseva, T.P., Karaman, Yu.K., Bival’kevich, N.V., and Zhukova, N.V., The use of a biologically active food supplement based on lipids from marine hydrobionts in an experiment on rats, Vopr. Pitan., 2010, vol. 79, no. 2, pp. 24–27.
Ortiz, J., Uquiche, E., Robert, P., Romero, N., Quitral, V., and Llantén, C., Functional and nutritional value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis pyrifera, Eur. J. Lipid Sci. Technol., 2009, vol. 111, no. 4, pp. 320–327. https://doi.org/10.1002/ejlt.200800140
Patten, A.R., Brocardo, P.S., and Christie, B.R., Omega-3 supplementation can restore glutathione levels and prevent oxidative damage caused by prenatal ethanol exposure, J. Nutr. Biochem., 2013, vol. 24, no. 5, pp. 760–769. https://doi.org/10.1016/j.jnutbio.2012.04.003
Pereira, A.G., Fraga-Corral, M., Garcia-Oliveira, P., Lourenco Lopes, C., Carpena, M., Prieto, M.A., and Simal-Gandara, J., The use of invasive algae species as a source of secondary metabolites and biological activities: Spain as case-study, Mar. Drugs, 2021, vol. 19, pp. 178–198. https://doi.org/10.3390/md19040178
Ravussin, E., Adiponectin enhances insulin action by decreasing ectopic fat deposition, J. Pharmacogenomics, 2002, vol. 2, no. 1, pp. 4–7. https://doi.org/10.1038/sj.tpj.6500068
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., and Rice-Evans, C., Antioxidant activity applying an improved ABTS radical cation decolorization assay, Free Radical Biol. Med., 1999, vol. 26, nos. 9–10, pp. 1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3
Refaat, B., Abdelghany, A.H., Ahmad, J., Abdalla, O.M., Elshopakey, G.E., Idris, S., and El-Boshy, M., Vitamin D(3) enhances the effects of omega-3 oils against metabolic dysfunction-associated fatty liver disease in rat, Biofactors, 2022, vol. 48, no. 2, pp. 498–513. https://doi.org/10.1002/biof.1804
Richard, D., Kefi, K., Barbe, U., Bausero, P., and Visioli, F., Polyunsaturated fatty acids as antioxidants, Pharmacol. Res., 2008, vol. 57, no. 6, pp. 451–455. https://doi.org/10.1016/j.phrs.2008.05.002
Sahin, E. and Gumuëslu, 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), Clin. Exp. Pharmacol. Physiol., 2007, vol. 34, nos. 5–6, pp. 425–431. https://doi.org/10.1111/j.1440-1681.2007.04584.x
Sanchez-Machado, D., Lopez-Cervantes, J., Lopez-Hernandez, J., and Paseiro-Losada, P., Fatty acids, total lipid, protein and ash contents of processed edible seaweeds, Food Chem., 2004, vol. 85, pp. 439–444. https://doi.org/10.1016/j.foodchem.2003.08.001
Seo, H.-D., Lee, E., Ahn, J., Hahm, J.-H., Ha, T.-Y., Lee, D.-H., and Jung, C.H., Codium fragile reduces adipose tissue expansion and fatty liver incidence by downregulating adipo- and lipogenesis, J. Food Biochem., 2022, vol. 46, no. 12, p. e14395. https://doi.org/10.1111/jfbc.14395
Solin, A.V., Korozin, V.I., and Lyashev, Yu.D., The influence of regulatory peptides on stress-induced changes in lipid metabolism in experimental animals, Byull. Eksp. Biol. Med., 2013, vol. 155, no. 3, pp. 299–301.
Svetachev, V.I. and Vaskovsky, V., A simplified technique for thin-layer microchromatography of lipids, J. Chromatogr., 1972, vol. 6, pp. 376–378. https://doi.org/10.1016/s0021-9673(01)91245-2
Titlyanov, E.A. and Titlyanova, T.V., Morskie rasteniya stran Aziatsko-Tikhookeanskogo regiona, ikh ispol’zovanie i kul’tivirovanie (Marine Plants of the Countries of the Asia-Pacific Region, Their Use and Cultivation), Vladivostok: Dal’nauka, 2012.
Vascovsky, V.E., Kostetsky, E.Y., and Vasendin, I.M., Universal reagent for phospholipid analysis, J. Chromatogr., 1975, vol. 114, pp. 129–141. https://doi.org/10.1016/s0021-9673(00)85249-8
Vaskovsky, V.E. and Khotimchenko, S.V., HPTLC of polar lipids of algae and other plants, J. Chromatogr., 1982, vol. 5, pp. 635–636. https://doi.org/10.1002/jhrc.1240051113
Funding
This work was carried out within the framework of a State Assignment of the Ilyichev Pacific Oceanological Institute (Far Eastern Branch of the Russian Academy of Sciences) on the topic “Ecological and Biogeochemical Processes in Marine Ecosystems: The Role of Natural and Anthropogenic Factors,” project no. 0211-2021-0014, registration no. 121-21500052-9.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
The experiments with animals were conducted in compliance with the NIH Guidelines for the care and use of laboratory animals (http://oacu.od.nih.gov/regs/index.htm). Experimental protocols were approved by the Ethics Committee of Ilyichev Pacific Oceanological Institute (Protocol No. 21 of November 10, 2022).
CONFLICT OF INTEREST
The authors of this work declare that they have no conflicts of interest.
Additional information
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fomenko, S.E., Kushnerova, N.F., Sprygin, V.G. et al. The Effect of a Lipid Extract from the Marine Green Algae Codium fragile (Suringar) Hariot 1889 on Metabolic Reactions under Acute Stress. Biol Bull Russ Acad Sci 51, 260–270 (2024). https://doi.org/10.1134/S1062359023602690
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359023602690