Polysaccharides isolated from Lycium barbarum L. by integrated tandem hybrid membrane technology exert antioxidant activities in mitochondria
Graphical abstract
Introduction
Lycium barbarum L. (wolfberry, Goji berries) have been recognized and used as a valuable traditional Chinese herbal medicine and functional food for 2500 years. The earliest record of these berries is found in the oracle bone script (Jiaguwen) of the Shang Dynasty (1600–1040 BE). The medicinal properties of Lycium barbarum L. have been appreciated by numerous medical scientists throughout the history of China. Medical and pharmaceutical knowledge regarding L. barbarum, which are categorized among the top class of medicines and contribute to longevity, have been recorded and summarized in Shennong’s Root and Herbal Classic (Shennong bencao jing). Li Shizhen also summarized the health and tonic effects of Goji berries in the Compendium of Materia Medica (Wu et al., 2018; Li, 2007; Chiu et al., 2010).
The most important active ingredients in Lycium barbarum L. are complexes of polysaccharides and glycoproteins, followed by flavonoids, carotenoids, saponins and others (Zhou et al., 2017; Pires et al., 2018; Kan et al., 2020). Polysaccharides with a molecular weight (MW) of 10–2300 kDa comprise 5%–8% of the dried fruits and possess hypoglycemic, hypolipidemic, immuno-modulatory, antioxidant, anti-aging, neuroprotective, and anti-Alzheimer’s disease properties (Tian et al., 2019; Yao et al., 2018; Masci et al., 2018; Kwok et al., 2019). The varied MW of polysaccharides may lead to different pharmacological functions. Zhou et al. degraded extracellular polysaccharides (EPS) with MW of 6.53, 256, 606, 802.6, 903.3, and 1002 kDa by hermetical–microwave and H2O2 under ultrasonic waves, and observed notable differences among their activities; in particular, the 6.53 kDa fraction had the most potent immune enhancing activity (Sun et al., 2012). Sun et al. obtained four low molecular polysaccharides derivatives (CPA-1, CPA-2, CPA-3 and CPA-4) by adding increased proportions of hydrogen peroxide, and have confirmed that high MW polysaccharides could scavenge free DPPH radicals and possess significant reducing ability, whereas the low MW polysaccharides exhibit relatively more potent free radical scavenging activity, especially for hydroxyl radicals (Sheng and Sun, 2014). Gu et al. successively fractionated the following polysaccharides using ethanol: SPC-60 (52.0 kDa), SPC-70 (294.9 kDa), SPC-80 (230.6 kDa), and SPC-90 (229.4 kDa); among these, SPC-70 was the most potent scavenger of DPPH, ABTS, and hydroxyl radicals, whereas SPC-60 exhibited the strongest immunomodulatory effects in terms of phagocytosis, proliferation activity, and nitric oxide (NO) release (Gu et al., 2019).
At present, the hierarchical alcohol precipitation method is the main method that can separate polysaccharides into different fragments. Polysaccharides fractions with different average molecular weight can be precipitated by different concentrations of ethanol. When ethanol is added to a solution containing polysaccharide, the polysaccharide molecules begin to dehydrate, followed with conformation transforming and assembling, caused by the enhancement of intramolecular hydrogen bonding. This may make it difficult to study the biological activity of polysaccharides themselves (Jiang et al., 2019; Wang et al., 2019). Membrane separation technology has rapidly advanced over the past few years. High separation efficiency, low energy consumption, rapid procedure, simple operation, and no contamination are critical to maintaining the original chemical structures and bioactivities of the extracted components, and membrane techniques have proven efficient for separating carbohydrates (Córdova et al., 2017). Zhang et al. isolated soybean oligosaccharides using two nanofiltration (NF) membranes with a yield and purity of 83.2 % and 77.9 %, respectively (Zhao et al., 2017). Nabarlatz et al. achieved optimal isolation of xylooligosaccharides from amylopectin acidification products using a 1000 Da membrane (Nabarlatz et al., 2007). Sun et al. used integrated membrane technology with nanofiltration, ultrafiltration, and microfiltration membranes to fractionate crude oligosaccharides from Hericium erinaceus (Cai et al., 2019). However, membrane separation technology has not yet been applied to separate polysaccharides from L. barbarum.
This work developed and applied a novel integrated tandem hybrid membrane technology (ITHMT) to separate L. barbarum polysaccharides having different MW. Four polysaccharides fractions (LBP1, LBP2, LBP3, and LBP4) were successfully isolated from L. barbarum. Further, the structures and antioxidant capacities of the isolated polysaccharides were preliminarily analyzed.
Section snippets
Materials and chemicals
Dried fruits of Lycium barbarum were gathered from Ningxia Zhongqi Wolfberry Trading Group Co., Ltd. on 1 May 2017, kept dry, and ventilated and were discerned by Dr. Xiao-Dong Luo from Kunming Institute of Botany, CAS. A specimen was stored at the Lanzhou Institute of Chemical Physics, CAS, with a serial number of 20170501. The test report from Alex Stewart Agriculture LTD showed that the specimen contained 4.01 % polysaccharides, 5.75 % water, 46.5 % carbohydrates, 13.5 % protein and 3.0 %
Preparation of crude L. barbarum polysaccharides
Goji berries contain abundant pigments such as carotenoids, which must be removed before extracting L. barbarum polysaccharides. The pigments were removed from Goji berries using subcritical extraction technology. The advantages of this procedure include a high extraction yield, rapid processing, and simple operation; moreover, since heat and radiation are not required in this procedure, the original chemical structures and bioactivities of the extracted components are retained, and so, this
Conclusions
The study established a novel ITHMT method for the separation of polysaccharides based on the principle of molecular exclusion. As a result, four polysaccharide fractions (LBP1, LBP2, LBP3 and LBP4) with different physiochemical properties were successfully isolated from L. barbarum L. All of them concentration-dependently scavenged superoxide anion radicals, and increased reducing power in vitro, as well as reduced the level of superoxide anions in mitochondria. This indicated that the
CRediT authorship contribution statement
Jianfei Liu: Data curation, Writing - original draft. Qiaosheng Pu: Writing - review & editing. Hongdeng Qiu: Software, Validation. Duolong Di: Supervision, Conceptualization, Methodology.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (No. 21904130) and the Science and Technology Program of Gansu Province (20CX9FG238). The authors also are grateful to Meng Jiao from National Laboratory of Biomacromolecules (CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences) for their support about Effect of Lycium barbarum polysaccharide on ROS in different organelles and anonymous reviewers for their
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