EFFECTS OF THE ACTION OF ARTHROSPIRA PLATENSIS (NORDSTEDT) GOMONT PHYCOBILIPROTEINS IN PLANT TISSUES: ANTIOXIDANT ACTIVITY IN THE GLUCOSE OXIDASE TEST SYSTEM AND UNCOUPLING OF OXIDATION AND PHOSPHORYLATION IN MITOCHONDRIA
Keywords:
Arthrospira platensis, phycobiliproteins, C-phycocyanin, glucose oxidase, hydrogen peroxide, mitochondria, uncoupling of oxidation and phosphorylation
Abstract
Background. Cyanobacterium Arthrospira (Spirulina) platensis has a unique biochemical composition and is widely used in various fields, including medicine and agriculture. The main phycobiliproteins (PBPs) of spirulina – C-phycocyanin and allophycocyanin protect animal cells from oxidative stress and mitochondrial dysfunction. At the same time there is little information about the antioxidant properties of PBPs in a plant cell and their influence on the bioenergetic parameters of plant mitochondria.
Purpose. The aim of this study was to determine the effect of A. platensis PBPs extract on glucose oxidase activity and functioning of potato mitochondria.
Materials and methods. PBPs were isolated from the crude biomass of A. platensis (Nordstedt) Gomont (strain IBSS-31) using cold extraction and precipitation with acetone. The protein extract with a high proportion of C-phycocyanin was used at concentrations of 0,025 – 0,25 mg/ml. The antioxidant properties of PBPs were evaluated by the inhibition of the glucose oxidase activity of potato extracts with increased expression of the GOX gene. The oxidative and phosphorylating activity of mitochondria in the presence of PBPs was measured by the polarographic method. Statistical data processing was carried out using SigmaPlot v. 14.0.
Results. The glucose oxidase test revealed the antioxidant activity of the PBPs extract, which was pronounced at a concentration of 0,25 mg / ml. At the same concentration, the extract caused uncoupling of oxidation and phosphorylation in potato mitochondria during succinate oxidation, associated with an increase in the state 4 respiration rate and a decrease of the respiratory control coefficient.
Conclusion. Thus, phycobiliproteins of A. platensis in a concentration-dependent manner reduce the generation of hydrogen peroxide in the glucose oxidase test system and cause uncoupling of the oxidation and phosphorylation in the plant mitochondria.
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References
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2. Gevorgiz R.G., Nehoroshev M.V. Kolichestvennoe opredelenie massovoj doli S-fikocianina i allofikocianina v suhoj biomasse Spirulina (Arthrospira) platensis North. Geitl. Holodnaja jekstrakcija : uchebno-metodicheskoe posobie [Quantification of the mass fraction of C-phycocyanin and allophycocyanin in dry biomass of Spirulina (Arthrospira) platensis North. Geitl. Cold extraction]. RAN, In-t morskih biologicheskih issledovanij im. A.O. Kovalevskogo, Sevastopol‘, 2017, 21 p. https://repository.marine-research.org/handle/299011/46
3. Kedik S.A., Jarcev E.I., Sakaeva I.V., Zhavoronok E.S., Panov A.V. Biofarmacevticheskij zhurnal, 2011, vol. 3, no. 3, pp. 3-10. https://submit.biopharmj.ru/ojs238/index.php/biopharmj/article/view/84
4. Klimenko E.S., Kulinchenko M.V., Grebnev P.A., Ditrish A., Konstantinov Ju.M. Journal of Stress Physiology & Biochemistry, 2014, vol. 10, no. 4, pp. 78-84. https://doi.org/10.31255/978-5-94797-319-8-1276-1279
5. Pobezhimova T.P., Kolesnichenko A.V., Grabelnykh O.I. Metody izuchenija mitohondrij rastenij. Poljarografija i jelektroforez [Methods for studying plant mitochondria. Polarography and electrophoresis]. M.: OOO «NPK Promjekspobezopasnost‘», 2004, 98 p.
6. Savchin D.V., Panjush A.S., Kartel‘ N.A. Sb. nauch. tr., Institut genetiki i citologii NAN Belarusi [Collection of scientific papers Institute of Genetics and Cytology of the National Academy of Sciences of Belarus]. Minsk, 2011, vol. 12, pp. 49-55.
7. Savchin D.V., Veresova T.N., Mezhnina O.A., Panjush A.S., Vjacheslavova A.O., Goldenkova-Pavlova I.V. Vesci NAN Belarusi. Ser. Bijal. Navuk, 2015, no. 1, pp. 50-55. https://vestibio.belnauka.by/jour/article/view/99
8. Stadnichuk I.N., Tropin I.V. Phycobiliproteins: structure, functions and biotechnological applications. Applied Biochemistry and Microbiology, 2017, vol. 53. no. 1, pp. 1-10. https://doi.org/10.7868/S0555109917010184
9. Bashandy S.A.E., El Awdan S.A., Ebaid H., Alhazza I.M. Antioxidant potential of Spirulina platensis mitigates oxidative stress and reprotoxicity induced by sodium arsenite in male rats. Oxid. Med.Cell. Longev., 2016, vol. 2016, id 7174351. https://doi.org/10.1155/2016/7174351
10. Bhat V.B., Madyastha K.M. C-phycocyanin: a potent peroxyl radical scavenger in vivo and in vitro. Biochem. Biophys. Res. Commun., 2000, vol. 275, pp. 20-25. https://doi.org/10.1006/bbrc.2000.3270
11. de Souza T.D., Prietto L., de Souza M. M., Furlong E.B. Profile, antioxidant potential, and applicability of phenolic compounds extracted from Spirulina platensis. African Journal of Biotechnology, 2015, vol. 41, pp. 2903-2909. https://doi.org/10.5897/AJB2015.14926
12. Demine S., Renard P., Arnould T. Mitochondrial uncoupling: a key controller of biological processes in physiology and diseases. Cells, 2019, vol. 8, no. 795. https://doi.org/10.3390/cells8080795
13. Ertani A., Nardi S., Francioso O., Sanchez-Cortes S., Di Foggia M., Schiavon M. Effects of two protein hydrolysates obtained from chickpea (Cicer arietinum L.) and Spirulina platensis on Zea mays (L.) plants. Front. Plant Sci., 2019, vol. 10, no. 954. https://doi.org/10.3389/fpls.2019.00954
14. Farooq S.M., Boppana N.B., Asokan D., Sekaran S.D., Shankar E.M., Li C., Gopal K., Bakar S.A., Karthik H.S., Ebrahim A.S. C-Phycocyanin confers protection against oxalate-mediated oxidative stress and mitochondrial dysfunctions in MDCK cells. PLoS One, 2014, vol. 4, pp. e93056. https://doi.org/10.1371/journal.pone.0093056
15. Fernández-Rojas B., Medina-Campos O.N., Hernández-Pando R., Negrette-Guzmán M., Huerta-Yepez S., Pedraza-Chaverri J. C-phycocyanin prevents cisplatin-induced nephrotoxicity through inhibition of oxidative stress. Food & function, 2014, vol. 5, no. 480. https://doi.org/10.1039/c3fo60501a
16. Godlewska K., Michalak I., Pacyga P., Baśladyńska S., Chojnacka K. Potential applications of cyanobacteria: Spirulina platensis filtrate and homogenates in agriculture. World Journal Microbiol. Biotechnol., 2019, vol. 35, no. 80. https://doi.org/10.1007/s11274-019-2653-6
17. Grabelnych O.I., Borovik O.A., Lyubushkina I.V., Gamburg K.Z., Fedyaeva A.V., Fedoseeva I.V., Stepanov A.V., Rikhvanov E.G., Sauchyn D.V., Urbanovich O.Yu., Borovskii G.B. Biological effects of potato plants transformation with glucose oxidase gene and their resistance to hyperthermia. Journal of Stress Physiology & Biochemistry, 2017, vol. 13, no. 1, pp. 5-14. http://www.jspb.ru/issues/2017/N1/JSPB_2017_1_05-14.pdf
18. Hongsthong A., Bunnag B. Overview of Spirulina: biotechnological, biochemical and molecular biological aspects. Chapter 2 In: Handbook on Cyanobacteria. Eds: P.M. Gault, H.J. Marler. Nova Science Publishers Inc., 2009, pp. 51-103.
19. Ježek P., Holendová B., Garlid K.D., Jabůrek M. Mitochondrial uncoupling proteins: subtle regulators of cellular redox signaling. Antioxidants & Redox Signaling, 2018, vol. 29, no. 7. https://doi.org/10.1089/ars.2017.7225
20. Konícková R., Vanková K., Vaníková J., Vánová K., Muchová L., Subhanová I., Zadinová M., Zelenka J., Dvorák A., Kolár M., Strnad H., Rimpelová S., Ruml T., Wong R. J., Vítek L. Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Annals of Hepatology, 2014, vol. 13, no. 2, pp. 273-283. https://doi.org/10.1016/S1665-2681(19)30891-9
21. Koru E. Earth Food Spirulina (Arthrospira): Production and quality standards. Food Additive, 2012. pp. 191-202. https://doi.org/10.5772/31848
22. Li Y-J., Han Z., Ge L., Zhou C.-J., Zhao Y-F., Wang D-H., Ren J.G, Niu X-X., Liang C-G. C-phycocyanin protects against low fertility by inhibiting reactive oxygen species in aging mice. Oncotarget, 2016, vol. 7, no. 14, pp. 17393-17409. https://doi.org/10.18632/oncotarget.8165
23. Liu Q., Huang Y., Zhang R., Cai T., Cai Y. Medical application of Spirulina platensis derived c-phycocyanin. Evid. Based Complement. Alternat. Med., 2016, vol. 2016, id 7803846. https://doi.org/10.1155/2016/7803846
24. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem., 1951, vol. 193, pp. 265-275.
25. Neuburger M., Journet E.P., Bligny R., Carde J.P., Douce R. Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch. Biochem. Biophys., 1982, vol. 217, no. 1, pp. 312-323. https://doi.org/10.1016/0003-9861(82)90507-0
26. Niu Y.-J., Zhou W., Guo J., Nie Z.-W., Shin K.-T., Kim N.-H., Lv W.-F., Cui X.-S. C-phycocyanin protects against mitochondrial dysfunction and oxidative stress in parthenogenetic porcine embryos. Scientific reports, 2017, vol. 7, article number: 16992. https://doi.org/10.1038/s41598-017-17287-0
27. Romay C., Gonzalez R. Phycocyanin is an antioxidant protector of human erythrocytes against lysis by peroxyl radicals. J. Pharm. Pharmacol., 2000, vol. 52, pp. 367-368. https://doi.org/10.1211/0022357001774093
28. Romay C., Gonzalez R., Ledon N., Remirez D., Rimbau V. C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr. Protein. Pept. Sci., 2003, vol. 4, pp. 207-216. https://doi.org/10.2174/1389203033487216
29. Thaakur S., Sravanthi R. Neuroprotective effect of Spirulina in cerebral ischemia-reperfusion injury in rats. J. Neural Transm. 2010, vol. 117, pp. 1083-1091. https://doi.org/10.1007/s00702-010-0440-5
30. Wu Q., Liu L., Miron A., Klímová B., Wan D., Kuča K. The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch. Toxicol., 2016, vol. 90, pp. 1817-1840. https://doi.org/10.1007/s00204-016-1744-5
31. Zheng J., Inoguchi T., Sasaki S., Maeda Y., McCarty M.F., Fujii M., Ikeda N., Kobayashi K., Sonoda N., Takayanagi R. Phycocyanin and phycocyanobilin from Spirulina platensis protect against diabetic nephropathy by inhibiting oxidative stress. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2013, vol. 304, pp. R110-R120. https://doi.org/10.1152/ajpregu.00648.2011
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Published
2021-04-29
How to Cite
Stepanov, A., Aksenova, A., Polyakova, E., Fedoseeva, I., Grabelnykh, O., & Gevorgiz, R. (2021). EFFECTS OF THE ACTION OF ARTHROSPIRA PLATENSIS (NORDSTEDT) GOMONT PHYCOBILIPROTEINS IN PLANT TISSUES: ANTIOXIDANT ACTIVITY IN THE GLUCOSE OXIDASE TEST SYSTEM AND UNCOUPLING OF OXIDATION AND PHOSPHORYLATION IN MITOCHONDRIA. Siberian Journal of Life Sciences and Agriculture, 13(2), 202-224. https://doi.org/10.12731/2658-6649-2021-13-2-202-224
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Biological Sciences
Copyright (c) 2021 Alexey V. Stepanov, Alisa A. Aksenova, Elizaveta A. Polyakova, Irina V. Fedoseeva, Olga I. Grabelnykh, Ruslan G. Gevorgiz
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