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Biological Activity of Japanese Quince Extract and Its Interactions with Lipids, Erythrocyte Membrane, and Human Albumin

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Biological Activity of Japanese Quince Extract and Its Interactions with Lipids, Erythrocyte Membrane, and Human Albumin J Membrane Biol (2016) 249:393–410 DOI 10.1007/s00232-016-9877-2 Biological Activity of Japanese Quince Extract and Its Interactions with Lipids, Erythrocyte Membrane, and Human Albumin 1 1 1 Paulina Strugała • Sylwia Cyboran-Mikołajczyk • Anna Dudra • 2 2 3 1 Paulina Mizgier • Alicja Z. Kucharska • Teresa Olejniczak • Janina Gabrielska Received: 5 November 2015 / Accepted: 27 January 2016 / Published online: 10 February 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract The aim of the study was to determine in vitro with a slight decrease in mobility of the acyl chains. Lipid biological activity of fruit ethanol extract from membrane rigidification could hinder the diffusion of free Chaenomeles speciosa (Sweet) Nakai (Japanese quince, radicals, resulting in inhibition of oxidative damage JQ) and its important constituents (-)-epicatechin (EC) induced by physicochemical agents. JQ extract has the and chlorogenic acid (CA). The study also investigated the ability to quench the intrinsic fluorescence of human serum structural changes in phosphatidylcholine (PC) liposomes, albumin through static quenching. This report thus could be dipalmitoylphosphatidylcholine liposomes, and erythrocyte of huge significance in the food industry, pharmacology, membranes (RBC) induced by the extract. It was found that and clinical medicine. the extract effectively inhibits oxidation of RBC, induced by 2,20-azobis (2-amidinopropane) dihydrochloride Keywords Japanese quince Á Lipid peroxidation Á (AAPH), and PC liposomes, induced by UVB radiation and Erythrocyte and phosphatidylcholine membranes Á AAPH. Furthermore, JQ extract to a significant degree 1H-NMR and fluorometric study Á Human serum albumin inhibited the activity of the enzymes COX-1 and COX-2, involved in inflammatory reactions. The extract has more than 2 times greater activity in relation to COX-2 than Introduction COX-1 (selectivity ratio 0.48). JQ extract stimulated growth of the beneficial intestinal bacteria Lactobacillus In the scientific research of recent years, much attention casei and Lactobacillus plantarum. In the fluorimetric has been paid to the biological activity of natural com- method by means of the probes Laurdan, DPH and TMA- pounds of plant origin and their potential use in prevention DPH, and 1H-NMR, we examined the structural changes and therapy of several diseases, including civilizational induced by JQ and its EC and CA components. The results diseases. The Japanese quince (JQ) fruit (genus show that JQ and its components induce a considerable Chaenomeles, family Rosacea) is a rich source of increase of the packing order of the polar heads of lipids polyphenolic compounds, triterpenoids, saccharides, essential oils, and alkaloids (Xianfei et al. 2007). Japanese quince is distributed in Central, East, and Southwest China & Paulina Strugała [email protected] and is now cultivated worldwide. Chaenomeles speciosa has been used in traditional Chinese medicine for thou- 1 Department of Physics and Biophysics, Wrocław University sands of years to treat many diseases, including sunstroke, of Environmental and Life Sciences, C.K. Norwida 25, edema, arthralgia, enteritis, and migraine (Han et al. 2010; 50-375 Wrocław, Poland 2 Song et al. 2008). Moreover, in recent years, JQ has found Department of Fruit, Vegetable and Cereal Technology, application in the treatment of diarrhea, arthritis, and liver Wrocław University of Environmental and Life Sciences, Chełmon´skiego 37/41, 51-630 Wrocław, Poland ailments (Yao et al. 2013). Chaenomeles speciosa was proven to be effective in dopamine transporter (DAT) 3 Department of Chemistry, Wrocław University of Environmental and Life Sciences, C.K. Norwida 25, regulation and antiparkinsonism, as determined by in vitro 50-375 Wrocław, Poland and in vivo assays (Zhang et al. 2013). Also promising are 123 394 P. Strugała et al.: Biological Activity of Japanese Quince Extract and Its Interactions… research results that provide evidence for antitumor activity by some physicochemical factors (UVB radiation and of JQ. It has been demonstrated that ethanolic extract of C. AAPH compound). The biophysical studies, using fluori- speciosa H22 inhibits tumor growth in mice by direct metric and 1H-NMR techniques, were carried out to specify killing of tumor cells and enhancing immune function (Yao the sites of the interaction between JQ components and the et al. 2013). Other investigators have shown that JQ is an membrane. For the current study, three membrane models effective inhibitor of the enzymes, MMP-2 and MMP-9, were selected: DPPC liposome membranes (one-compo- secreted by human leukemia HL-60 cells. Gorlach and co- nent membrane to facilitate interpretation of results), PC authors showed that procyanidins isolated from JQ induce liposomes of egg phosphatidylcholine (their composition apoptosis in human adenocarcinoma cells, whereas resembling the natural cell bilayer lipid membrane), and Lewandowska and co-authors found a strong antiprolifer- red blood cell (RBC) membranes—natural lipid–protein ative effect against breast cancer cells (Gorlach et al. 2011; structures. An additional aim of the work was to determine Lewandowska et al. 2013). JQ’s ability to inhibit the enzymes (COX-1 and COX-2) Free radicals present in the body are an integral part of involved in inflammatory reactions, to bind to the blood physiology of the living organism (Wong et al. 2005). transport protein human serum albumin, and to examine the Their concentration increases under conditions of oxidative JQ-mediated increase in the bacteria Lactobacillus casei stress. Peroxidation of lipids as well as other biomolecules and L. plantarum of intestinal microflora. To our knowl- by reactive oxygen species results in disturbances in the edge, such comprehensive research on the biological structure and function of membranes, which in turn can activity of JQ and the proposed potential molecular cause serious diseases, such as atherosclerosis, stroke, mechanism of the observed effects/activity has not yet been cancer, and diseases of the circulatory system (Hendrich reported in the scientific literature. 2006). Biological activity of polyphenolic compounds is closely linked to their ability to interact with the bilayer lipid membrane. In the worldwide literature, there were Materials and Methods few reports of extensive biophysical studies aiming to explain the molecular mechanisms responsible for protec- Materials tion of the lipid bilayer against peroxidation. The amphi- philic properties of polyphenolic compounds are DPPHÁ, indomethacin, N,N,N0,N0-tetramethyl-p-phenylene- responsible for their interaction not only with the surface of diamine (TMPD), arachidonic acid from porcine liver, the lipid membrane (via the polar heads) but also with the cyclooxygenase 1 from sheep, cyclooxygenase 2 human deeper areas of the membrane in its hydrophobic part—the recombinant, trichloroacetic acid (TCA), 2-thiobarbituric acyl chains (Oteiza et al. 2005). acid (TBA), 1,2-dipalmitoyl-sn-glycero-3-phosphatidyl- The mechanisms of the therapeutic effects of polyphe- choline (DPPC), chlorogenic acid, (-)-epicatechin, deu- 0 nolic compounds are not yet sufficiently well understood. terium oxide (D2O), 2,2 -azobis (2-amidinopropane) One line of research is concerned with both the modulatory dihydrochloride (AAPH), and albumin from human serum impact of these substances on proteins, human serum (lyophilized powder, essentially fatty acid free) were pur- albumin in particular, and enzymes, including cyclooxy- chased from Sigma–Aldrich (Poznan´, Poland). Egg yolk genase and lipoxygenase, and with explaining such mod- phosphatidylcholine (PC) was obtained from Lipid Prod- ulatory effects. ucts, UK. The probes DPH, DPH-PA, TMA-DPH, and To determine the potential biological activity of a Laurdan were purchased from Molecular Probes (Eugene, polyphenolic compound in the body, it is important to Oregon). Tris (hydroxymethyl) aminomethane (Tris:HCl) know its interaction with bacteria of the intestinal micro- were obtained from ‘‘Chempur’’ Piekary S´la˛skie. Bacteria flora. There are numerous literature data on the activity of cultures (L. casei PCM 2639 and L. plantarum PCM 2675) polyphenolic compounds in fighting pathogenic bacteria were from the Polish Collection of Microorganisms (PCM, (Tzounis et al. 2008), whereas there are remarkably few Institute of Immunology and Experimental Therapy, Polish studies investigating the influence of polyphenols on the Academy of Science in Wrocław). composition and activity of the nonpathogenic gut micro- bial community. Preparation of Extract The aim of the study was to determine in vitro biological activity of fruit ethanol extract from C. speciosa (Sweet) The raw material for the study was Japanese quince [C. Nakai (JQ), and two important components present in JQ, speciosa (Sweet) Nakai]. The fruit of JQ was collected in i.e., (-)-epicatechin (EC) and chlorogenic acid (CA), with the Botanical Garden of Wrocław. It was frozen and then respect to membranes of phosphatidylcholine liposomes freeze-dried (ChRISTALPhA 1–4 LSC), and just before and erythrocyte membranes against peroxidation induced extraction it was disintegrated with an analytical mill (A11 123 P. Strugała et al.: Biological Activity of Japanese Quince Extract and Its Interactions… 395 basic of IKA-Werke, Germany). The process of obtaining Lh-1, collision energy 28–30 eV, source temperature the JQ extract was described in detail by Strugała and 100 °C,
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