Antioxidant Interactions Between Citrus Fruit Carotenoids and Ascorbic Acid in New Models of Animal Cell Membranes

Overview

Journal Antioxidants (Basel)

Date 2023 Sep 28

PMID 37760036

Authors

Marcelo P Barros

Jaime Zacarias-Garcia

Florencia Rey

Lorenzo Zacarias

Maria J Rodrigo

Affiliations

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Abstract

The regular consumption of citrus fruits by humans has been associated with lower incidence of chronic-degenerative diseases, especially those mediated by free radicals. Most of the health-promoting properties of citrus fruits derive from their antioxidant content of carotenoids and ascorbic acid (ASC). In the current work we have investigated the scavenging (against hydroxyl radical) and quenching capacities (against singlet oxygen) of four different carotenoid extracts of citrus fruits in the presence or absence of ASC (μM range) in organic solvent, aqueous solution, micelles and in an innovative biomimicking liposomal system of animal cell membrane (AML). The fruits of four varieties of citrus were selected for their distinctive carotenoid composition (liquid chromatography characterization): 'Nadorcott' mandarin and the sweet oranges 'Valencia late', 'Ruby Valencia' and 'Pinalate' mutant. The quenching activity of citrus carotenoids strongly depended on the biological assemblage: freely diffusible in organic solvent, 'Ruby Valencia' carotenoids (containing lycopene) showed the highest quenching activity, whereas 'Nadorcott' mandarin extracts, rich in β-cryptoxanthin, prevailed in micellar systems. Interestingly, the addition of 10 μM ASC significantly increased the quenching activity of all citrus extracts in micelles: 'Valencia' orange (+53%), 'Pinalate' (+87%), 'Ruby' (4-fold higher) and 'Nadorcott' mandarins (+20%). Accurate C-BODIPY fluorescence assays showed solid scavenging activities of all citrus extracts against AML oxidation: 'Valencia' (-61%), 'Pinalate' (-58%) and 'Ruby' oranges (-29%), and 'Nadorcott' mandarins (-70%). Indeed, all four citrus extracts tested here have balanced antioxidant properties; extracts from the 'Nadorcott' mandarin slightly prevailed overall, due, at least in part, to its high content of β-cryptoxanthin. This study depicts some of the antioxidant interactions between citrus fruit carotenoids and ascorbic acid in models of animal cell membranes and reinforces the contribution of them in promoting health benefits for humans.

References

Mano C, Guaratini T, Cardozo K, Colepicolo P, Bechara E, Barros M . Astaxanthin Restrains Nitrative-Oxidative Peroxidation in Mitochondrial-Mimetic Liposomes: A Pre-Apoptosis Model. Mar Drugs. 2018; 16(4). PMC: 5923413. DOI: 10.3390/md16040126. View

Martinez A, Stinco C, Melendez-Martinez A . Free radical scavenging properties of phytofluene and phytoene isomers as compared to lycopene: a combined experimental and theoretical study. J Phys Chem B. 2014; 118(33):9819-25. DOI: 10.1021/jp503227j. View

Nithila S, Anandkumar B, Vanithakumari S, George R, Mudali U, Dayal R . Studies to control biofilm formation by coupling ultrasonication of natural waters and anodization of titanium. Ultrason Sonochem. 2013; 21(1):189-99. DOI: 10.1016/j.ultsonch.2013.06.010. View

Esterbauer H . Estimation of peroxidative damage. A critical review. Pathol Biol (Paris). 1996; 44(1):25-8. View

Sandmann G . Antioxidant Protection from UV- and Light-Stress Related to Carotenoid Structures. Antioxidants (Basel). 2019; 8(7). PMC: 6680902. DOI: 10.3390/antiox8070219. View

Mortensen A, Skibsted L, Truscott T . The interaction of dietary carotenoids with radical species. Arch Biochem Biophys. 2001; 385(1):13-9. DOI: 10.1006/abbi.2000.2172. View

Spector A, Yorek M . Membrane lipid composition and cellular function. J Lipid Res. 1985; 26(9):1015-35. View

Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M . Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol. 2004; 134(2):824-37. PMC: 344557. DOI: 10.1104/pp.103.031104. View

Aune D, Keum N, Giovannucci E, Fadnes L, Boffetta P, Greenwood D . Dietary intake and blood concentrations of antioxidants and the risk of cardiovascular disease, total cancer, and all-cause mortality: a systematic review and dose-response meta-analysis of prospective studies. Am J Clin Nutr. 2018; 108(5):1069-1091. PMC: 6250988. DOI: 10.1093/ajcn/nqy097. View

10.

Rodrigo M, Alquezar B, Alos E, Medina V, Carmona L, Bruno M . A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments. J Exp Bot. 2013; 64(14):4461-78. PMC: 3808326. DOI: 10.1093/jxb/ert260. View

11.

Rodrigo M, Marcos J, Zacarias L . Biochemical and molecular analysis of carotenoid biosynthesis in flavedo of orange (Citrus sinensis L.) during fruit development and maturation. J Agric Food Chem. 2004; 52(22):6724-31. DOI: 10.1021/jf049607f. View

12.

Rodrigo M, Cilla A, Barbera R, Zacarias L . Carotenoid bioaccessibility in pulp and fresh juice from carotenoid-rich sweet oranges and mandarins. Food Funct. 2015; 6(6):1950-9. DOI: 10.1039/c5fo00258c. View

13.

Sujak A, Gabrielska J, Milanowska J, Mazurek P, Strzalka K, Gruszecki W . Studies on canthaxanthin in lipid membranes. Biochim Biophys Acta. 2005; 1712(1):17-28. DOI: 10.1016/j.bbamem.2005.03.010. View

14.

Gensure R, Zeidel M, Hill W . Lipid raft components cholesterol and sphingomyelin increase H+/OH- permeability of phosphatidylcholine membranes. Biochem J. 2006; 398(3):485-95. PMC: 1559473. DOI: 10.1042/BJ20051620. View

15.

Huang Y, Li W, Su Z, Kong A . The complexity of the Nrf2 pathway: beyond the antioxidant response. J Nutr Biochem. 2015; 26(12):1401-13. PMC: 4785809. DOI: 10.1016/j.jnutbio.2015.08.001. View

16.

Di Mascio P, Kaiser S, Sies H . Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys. 1989; 274(2):532-8. DOI: 10.1016/0003-9861(89)90467-0. View

17.

Grudzinski W, Nierzwicki L, Welc R, Reszczynska E, Luchowski R, Czub J . Localization and Orientation of Xanthophylls in a Lipid Bilayer. Sci Rep. 2017; 7(1):9619. PMC: 5575131. DOI: 10.1038/s41598-017-10183-7. View

18.

Drummen G, van Liebergen L, Op den Kamp J, Post J . C11-BODIPY(581/591), an oxidation-sensitive fluorescent lipid peroxidation probe: (micro)spectroscopic characterization and validation of methodology. Free Radic Biol Med. 2002; 33(4):473-90. DOI: 10.1016/s0891-5849(02)00848-1. View

19.

Gruszecki W, Strzalka K . Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta. 2005; 1740(2):108-15. DOI: 10.1016/j.bbadis.2004.11.015. View

20.

Prabhu H, Krishnamurthy S . Ascorbate-dependent formation of hydroxyl radicals in the presence of iron chelates. Indian J Biochem Biophys. 1993; 30(5):289-92. View