Arthrospira platensis: antioxidant, hypoglycemic and hypolipidemic effects in vitro and in vivo (brief review)

Abstract

The cyanobacterium Arthrospira platensis biomass is a promising food source of biologically active substances with pharmacological activity.

The aim of this research was a brief review and analysis of experimental in vitro and in vivo studies of the antioxidant, hypoglycemic and hypolipidemic properties of A. platensis biomass, phycocyanins, and their chromophore – phycocyanobilin.

Material and methods. For the main search of the literature, the PubMed Internet resource was used, the key component of which is the Medline article database, covering about 75% of the world’s medical publications. In addition, Scopus and Web of Science databases were used. Search depth – 20 years. Search keywords: Arthrospira platensis, phycobiliprotein, C-phycocyanin, allophycocyanin, hypoglycemic effect, hypolipidemic effect, antioxidant activity, in vitro and in vivo studies.

Results. A brief description of the composition of the cyanobacterium Arthrospira platensis biomass, methods of its cultivation, phycocyanins extraction methods is presented. The results of experimental studies indicate the presence of pronounced antioxidant properties of A. platensis biomass, mainly due to phycocyanins in its composition. The hypoglycemic and hypolipidemic effects of A. platensis biomass and extracted phycocyanins intake have been established in vivo when modeling carbohydrate and/or lipid metabolism disorders. The results of in vitro and in vivo studies indicate the presence of pronounced antioxidant properties of phycocyanins. Hypoglycemic effects are shown in particular in experiments on rats with hyperlipidemia and alloxan diabetes fed a diet enriched with A. platensis biomass and on KKAy mice, treated with C-phycocyanin extract.

Conclusion. The analysis of the results of in vitro and in vivo studies of the antioxidant, hypoglycemic and hypolipidemic properties of A. platensis biomass and extracts with a high content of phycocyanins, presented in a brief review, suggests that their use in the diet of people with impaired carbohydrate and lipid metabolism is promising. Accordingly, from the standpoint of evidence-based medicine, clinical studies on the use of spirulina biomass and/or its extracts with a high content of phycocyanins as part of specialized foods intended for the prevention and/or dietary correction of carbohydrate and lipid metabolism disorders should be preceded by additional experimental physical-chemical, physiological and biochemical research.

Keywords:Arthrospira platensis; phycobillyprotein; C-phycocyanin; allophycocyanin; hypoglycemic; hypolipidemic; antioxidants

Funding. The research was supported by the state project FGMF-2022-0002.

Conflict of interest. Authors declare no conflict of interest.

Contribution. Analysis of publications, the Introduction and Conclusion sections writing – Mazo V.K.; gathering of literature data, general edition – Sidorova Yu.S.; analysis of publications, the Results section writing – Biryulina N.A.

For citation: Mazo V.K., Biryulina N.A., Sidorova Yu.S. Arthrospira platensis: antioxidant, hypoglycemic and hypolipidemic effects in vitro and in vivo (brief review). Voprosy pitaniia [Problems of Nutrition]. 2022; 91 (4): 19–25. DOI: https://doi.org/10.33029/0042-8833-2022-91-4-19-25 (in Russian)

References

1. Grosshagauer S., Kraemer K., Somoza V. The true value of Spirulina. J Agric Food Chem. 2020; 68 (14): 4109–15. DOI: https://doi.org/10.1021/acs.jafc.9b08251

2. Wollina U., Voicu C., Gianfaldoni S., Lotti T., França K., Tchernev G. Arthrospira platensis – potential in dermatology and beyond. Open Access Maced J Med Sci. 2018; 6 (1): 176–80. DOI: https://doi.org/10.3889/oamjms.2018.033

3. Pagels F., Guedes A.C., Amaro H.M., Kijjoa A., Vasconcelos V. Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol Adv. 2019; 37 (3): 422–43. DOI: https://doi.org/10.1016/j.biotechadv.2019.02.010

4. El Baky H.H.A., El Baroty G.S., Mostafa E.M. Optimization growth of Spirulina (Arthrospira) platensis in photobioreactor under varied nitrogen concentration for maximized biomass, carotenoids and lipid contents. Recent Pat Food Nutr Agric. 2020; 11 (1): 40–8. DOI: https://doi.org/10.2174/2212798410666181227125229

5. Petrukhina D.I. Assessment of the possibility of increasing biomass and synthesis products in the genera Spirulina and Arthrospira (Cyanophyta) after cryopreservation. Trudy Karel’skogo nauchnogo tsentra RAN [Proceedings of the Karelian Scientific Center of the Russian Academy of Sciences]. 2019; (6): 74–84. (in Russian)

6. Abdel-Daim M.M., Abuzead S.M., Halawa S.M. Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats. PLoS One. 2013; 8: e72991. DOI: https://doi.org/10.1371/journal.pone.0072991

7. Abdelkhalek N.K., Ghazy E.W., Abdel-Daim M.M. Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environ Sci Pollut Res Int. 2015; 22: 3023–31. DOI: https://doi.org/10.1007/s11356-014-3578-0

8. Abdel-Daim M.M., Farouk S.M., Madkour F.F., Azab S.S. Anti-inflammatory and immunomodulatory effects of Spirulina platensis in comparison to Dunaliella salina in acetic acid-induced rat experimental colitis. Immunopharmacol Immunotoxicol. 2015; 37 (2): 126–39. DOI: https://doi.org/10.3109/08923973.2014.998368

9. El-Tantawy W.H. Antioxidant effects of Spirulina supplement against lead acetate-induced hepatic injury in rats. J Tradit Complement Med. 2015; 6 (4): 327–31. DOI: https://doi.org/10.1016/j.jtcme.2015.02.001

10. Rajbanshi S.L.A., Patel D.S., Pandanaboina C.S. Hepato-protective effects of blue-green alga Spirulina platensis on diclofenac-induced liver injury in rats. Mal J Nutr. 2016; 22 (2): 289–99.

11. Elshazly M.O., Abd El-Rahman S.S., Morgan A.M., Ali M.E. The remedial efficacy of Spirulina platensis versus chromium-induced nephrotoxicity in male Sprague-Dawley rats. PLoS One. 2015; 10 (6): e0126780.

12. Abdel-Daim M.M., Shaaban Ali M., Madkour F.F., Elgendy H. Oral Spirulina platensis attenuates hyperglycemia and exhibits antinociceptive effect in streptozotocin-induced diabetic neuropathy rat model. J Pain Res. 2020; 13: 2289–96. DOI: https://doi.org/10.2147/JPR.S267347

13. Sadek K.M., Lebda M.A., Nasr S.M., Shoukry M. Spirulina platensis prevents hyperglycemia in rats by modulating gluconeogenesis and apoptosis via modification of oxidative stress and MAPK-pathways. Biomed Pharmacother. 2017; 92: 1085–94. DOI: https://doi.org/10.1016/j.biopha.2017.06.023

14. Muthuraman P., Senthilkumar R., Srikumar K. Alterations in beta-islets of Langerhans in alloxan-induced diabetic rats by marine Spirulina platensis. J Enzyme Inhib Med Chem. 2009; 24 (6): 1253–6. DOI: https://doi.org/10.3109/14756360902827240

15. Nawrocka D., Kornicka K., Smieszek A., Marycz K. Spirulina platensis improves mitochondrial function impaired by elevated oxidative stress in adipose-derived mesenchymal stromal cells (ASCs) and Intestinal Epithelial Cells (IECs), and Enhances Insulin Sensitivity in Equine Metabolic Syndrome (EMS) Horses. Mar Drugs. 2017; 15 (8): 237. DOI: https://doi.org/10.3390/md15080237

16. Cheong S.H., Kim M.Y., Sok D.E., Hwang S.Y., Kim J.H., Kim H.R., et al. Spirulina prevents atherosclerosis by reducing hypercholesterolemia in rabbits fed a high-cholesterol diet. J Nutr Sci Vitaminol. 2010; 56 (1): 34–40. DOI: https://doi.org/10.3177/jnsv.56.34

17. Nasirian F., Mesbahzadeh B., Maleki S.A., Mogharnasi M., Kor N.M. The effects of oral supplementation of Spirulina platensis microalgae on hematological parameters in streptozotocin-induced diabetic rats. Am J Transl Res. 2017; 9 (12): 5238–44.

18. Strasky Z., Zemankova L., Nemeckova I., Rathouska J., Wong R.J., Muchova L., et al. Spirulina platensis and phycocyanobilin activate atheroprotective heme oxygenase-1: a possible implication for atherogenesis. Food Funct. 2013; 4 (11): 1586–94. DOI: https://doi.org/10.1039/c3fo60230c

19. Han L.K., Li D.X., Xiang L., Gong X.J., Kondo Y., Suzuki I., et al. Isolation of pancreatic lipase activity-inhibitory component of Spirulina platensis and it reduce postprandial triacylglycerolemia. Yakugaku Zasshi. 2006; 126 (1): 43–9. DOI: https://doi.org/10.1248/yakushi.126.43

20. Ku C.S., Yang Y., Park Y., Lee J. Health benefits of blue-green algae: prevention of cardiovascular disease and nonalcoholic fatty liver disease. J Med Food. 2013; 16 (2): 103–11. DOI: https://doi.org/10.1089/jmf.2012.2468

21. llter I., Akyıl S., Demirel Z., Koç M., Conk-Dalay M., Kaymak-Ertekin F. Optimization of phycocyanin extraction from Spirulina platensis using different techniques. J Food Compos Anal. 2018; 70: 78–88.

22. Evaluation of Certain Food Additives: Eighty-Sixth Report of the Joint FAO/WHO Expert Committee on Food Additives. Geneva: World Health Organization and Food and Agriculture Organization of the United Nations, 2019 (WHO Technical Report Series; No. 1014). Licence: CC BY-NC-SA 3.0 IGO.

23. Paramonov L.E. Estimation of chlorophyll content by absorption spectra of native Spirulina platensis cells. Voprosy sovremennoi al’gologii [Problems of Modern Algology]. 2020; (1): 25–33. (in Russian)

24. Lafarga T., Fernández-Sevilla J.M., González-López C., Acién-Fernández F.G. Spirulina for the food and functional food industries. Food Res Int. 2020; 137: 109356. DOI: https://doi.org/10.1016/j.foodres.2020.109356

25. Martelli F., Alinovi M., Bernini V., Gatti M., Bancalari E. Arthrospira platensis as natural fermentation booster for milk and soy fermented beverages // Foods. 2020. Vol. 9, N 3. P. 350. DOI: https://doi.org/10.3390/foods9030350

26. Dumay J., Morancais M. Chapter 9 – Proteins and pigments. In: J. Fleurence, I. Levine (eds). Seaweed in Health and Disease Prevention. San Diego: Academic Press, 2016: 275–318. ISBN 9780128027721. DOI: https://doi.org/10.1016/B978-0-12-802772-1.00009-9

27. Liu Q., Huang Y., Zhang R., Cai T., Cai Y. Medical application of Spirulina platensis derived C-phycocyanin. Evid Based Complement Alternat Med. 2016; 2016: 7803846. DOI: https://doi.org/10.1155/2016/7803846

28. Cherdkiatikul T., Suwanwong Y. Production of the α and β subunits of Spirulina allophycocyanin and C-phycocyanin in Escherichia coli: a comparative study of their antioxidant activities. J Biomol Screen. 2014; 19 (6): 959–65. DOI: https://doi.org/10.1177/1087057113520565

29. McCarty M.F., Iloki-Assanga S. Co-administration of phycocyanobilin and/or phase 2-inducer nutraceuticals for prevention of opiate tolerance. Curr Pharm Des. 2018; 24 (20): 2250–4. DOI: https://doi.org/10.2174/1381612824666180723162730

30. Ou Y., Lin L., Yang X., Pan Q., Cheng X. Antidiabetic potential of phycocyanin: effects on KKAy mice. Pharm Biol. 2013; 51 (5): 539–44. DOI: https://doi.org/10.3109/13880209.2012.747545

31. Nagaoka S., Shimizu K., Kaneko H., Shibayama F., Morikawa K., Kanamaru Y., et al. A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats. J Nutr. 2005; 135 (10): 2425–30. DOI: https://doi.org/10.1093/jn/135.10.2425

32. Lanone S., Bloc S., Foresti R., Almolki A., Taillé C., Callebert J., et al. Bilirubin decreases nos2 expression via inhibition of NAD(P)H oxidase: implications for protection against endotoxic shock in rats. FASEB J. 2005; 19 (13): 1890–2. DOI: https://doi.org/10.1096/fj.04-2368fje

33. Datla S.R., Dusting G.J., Mori T.A., Taylor C.J., Croft K.D., Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension. 2007; 50 (4): 636–42. DOI: https://doi.org/10.1161/HYPERTENSIONAHA.107.092296

34. McCarty M.F., Kerna N.A. Spirulina rising: microalgae, phyconutrients, and oxidative stress. EC Microbiol. 2021; 17 (7): 121–8. DOI: https://doi.org/10.31080/ecmi.2021.17.011

35. McCarty M.F., DiNicolantonio J.J. Nutraceuticals have potential for boosting the type 1 interferon response to RNA viruses including influenza and coronavirus. Prog Cardiovasc Dis. 2020; 63 (3): 383–5. DOI: https://doi.org/10.1016/j.pcad.2020.02.007

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CHIEF EDITOR
CHIEF EDITOR
Viktor A. Tutelyan
Full Member of the Russian Academy of Sciences, Doctor of Medical Sciences, Professor, Scientific Director of the Federal Research Centre of Nutrition, Biotechnology and Food Safety (Moscow, Russia)

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