DOI QR코드

DOI QR Code

Structural analysis, anti-inflammatory activity of the main water-soluble acidic polysaccharides (AGBP-A3) from Panax quinquefolius L berry

  • Zhihao Zhang (Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Huijiao Yan (Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Hidayat Hussain (Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry) ;
  • Xiangfeng Chen (Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Jeong Hill Park (College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Sung Won Kwon (College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Lei Xie (Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Bowen Zheng (Biological Engineering Technology Innovation Center of Shandong Province, Heze Branch of Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Xiaohui Xu (Department of Genetics and Cell Biology, Basic Medical College, Qingdao University) ;
  • Daijie Wang (Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Jinao Duan (Jiangsu Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, and Jiangsu Key Laboratory for High Technology Research of TCM Formulae, College of Pharmacy, Nanjing University of Chinese Medicine)
  • Received : 2024.01.13
  • Accepted : 2024.05.04
  • Published : 2024.09.01

Abstract

Background: Panax quinquefolius L, widely recognized for its valuable contributions to medicine, has aroused considerable attention globally. Different from the extensive research has been dedicated to the root of P. quinquefolius, its berry has received relatively scant focus. Given its promising medicinal properties, this study was focused on the structural characterizations and anti-inflammatory potential of acidic polysaccharides from the P. quinquefolius berry. Materials and methods: P. quinquefolius berry was extracted with hot water, precipitated by alcohol, separated by DEAE-52-cellulose column to give a series of fractions. One of these fractions was further purified via Sephadex G-200 column to give three fractions. Then, the main fraction named as AGBP-A3 was characterized by methylation analysis, NMR spectroscopy, etc. Its anti-inflammatory activity was assessed by RAW 264.7 cell model, zebrafish model and molecular docking. Results: The main chain comprised of α-L-Rhap, α-D-GalAp and β-D-Galp, while the branch consisted mainly of α-L-Araf, β-D-Glcp, α-D-GalAp, β-D-Galp. The RAW264.7 cell assay results showed that the inhibition rates against IL-6 and IL-1β secretion at the concentration of 625 ng/mL were 24.83 %, 11.84 %, while the inhibition rate against IL-10 secretion was 70.17 % at the concentration of 312 ng/mL. In the zebrafish assay, the migrating neutrophils were significantly reduced in number, and their migration to inflammatory tissues was inhibited. Molecular docking predictions correlated well with the results of the anti-inflammatory assay. Conclusion: The present study demonstrated the structure of acidic polysaccharides of P. quinquefolius berry and their effect on inflammation, providing a reference for screening anti-inflammatory drugs.

Keywords

Acknowledgement

We gratefully acknowledge the Science, Education and Industry Integration Innovation Pilot Project from Qilu University of Technology (Shandong Academy of Sciences) (2022JBZ02-06), Key R&D Program of Shandong Province (2023TZXD068, 2023TZXD083), the Science and Technology smes Innovation Ability Improvement Project of Shandong Province (2022TSGC2439), the Key R&D and transformation plan of Qinghai Province (2023-SF-112), and the assistance of Yangzhou BoRui Saccharide Biotech Co. Ltd. (www.polyscilife.com) in experiments design and data analysis.

References

  1. Zhang J, Fan S, Qin J, Dai J, Zhao F, Gao L, Lian X, Shang W, Xu X, Hu X. Changes in the microbiome in the soil of an American ginseng continuous plantation. Front Plant Sci 2020;11:572199.
  2. Ma Xiu-li HC-y, Shi -xiang LU, Yun-xiu SUN, Ju-zheng LIU, Shu-ying LIU. Isolation and characterization of a bioactive polysaccharide from Panax quinquef olium L. Chem Res Chin Univ 1998;14(2):143-6.
  3. Assinewe VA, Arnason JT, Aubry A, Mullin J, Lemaire I. Extractable polysaccharides of Panax quinquefolius L. (North American ginseng) root stimulate TNFa production by alveolar macrophages. Phytomedicine 2002;9(5):398-404.
  4. Lemmon HR, Sham J, Chau LA, Madrenas J. High molecular weight polysaccharides are key immunomodulators in North American ginseng extracts: characterization of the ginseng genetic signature in primary human immune cells. J Ethnopharmacol 2012;142(1):1-13.
  5. Xie JT, Wu JA, Mehendale S, Aung HH, Yuan CS. Anti-hyperglycemic effect of the polysaccharides fraction from American ginseng berry extract in ob/ob mice. Phytomedicine 2004;11(2-3):182-7.
  6. Wang C, Song W. Steamed American ginseng berry: ginsenoside analyses and anticancer activities. J Agric Food Chem 2006;54:9936-42.
  7. Xie J, Wang C, Zhang B. In vitro and in vivo anticancer effects of American ginseng berry: exploring representative compounds. Biol Pharm Bull 2009;32(9):1552-8.
  8. Mehendale SR, Wang CZ, Shao ZH, Li CQ, Xie JT, Aung HH, Yuan CS. Chronic pretreatment with American ginseng berry and its polyphenolic constituents attenuate oxidant stress in cardiomyocytes. Eur J Pharmacol 2006;553(1-3):209-14.
  9. Wang C, Sun S. American ginseng berry enhances chemopreventive effect of 5-FU on human colorectal cancer cells. Oncol Rep 2009;22(4):943-52.
  10. Xu XY, Wang Z, Ren S, Leng J, Hu JN, Liu Z, Chen C, Li W. Improved protective effects of American ginseng berry against acetaminophen-induced liver toxicity through TNF-alpha-mediated caspase-3/-8/-9 signaling pathways. Phytomedicine 2018;51(7):128-38.
  11. Li J, Huang G. Extraction, purification, separation, structure, derivatization and activities of polysaccharide from Chinese date. Process Biochem 2021;110(9):231-42.
  12. Fan H, Sun M, Li J, Zhang S, Tu G, Liu K, Xia Q, Jiang Y, Liu B. Structure characterization and immunomodulatory activity of a polysaccharide from Saposhnikoviae Radix. Int J Biol Macromol 2023;233:123502.
  13. Zhang H, Zou P, Zhao H, Qiu J, Regenstein JM, Yang X. Isolation, purification, structure and antioxidant activity of polysaccharide from pinecones of Pinus koraiensis. Carbohydr Polym 2021;251:117078.
  14. Bai Y, Zhou Y, Zhang R, Chen Y, Wang F, Zhang M. Gut microbial fermentation promotes the intestinal anti-inflammatory activity of Chinese yam polysaccharides. Food Chem 2023;402:134003.
  15. Qiu WL, Lo HC, Lu MK, Lin TY. Significance of culture period on the physiochemistry and anti-cancer potentials of polysaccharides from mycelia of Ganoderma lucidum. Int J Biol Macromol 2023;242(4):125181.
  16. Mallavadhani UV, Chandrashekhar M, Nayak VL, Ramakrishna S. Synthesis and anticancer activity of novel fused pyrimidine hybrids of myrrhanone C, a bicyclic triterpene of Commiphora mukul gum resin. Mol Divers 2015;19(4):745-57.
  17. Chandrashekhar M, Nayak VL, Ramakrishna S, Mallavadhani UV. Novel triazole hybrids of myrrhanone C, a natural polypodane triterpene: synthesis, cytotoxic activity and cell based studies. Eur J Med Chem 2016;114:293-307.
  18. Li G, Chen P, Zhao Y, Zeng Q, Ou S, Zhang Y, Wang P, Chen N, Ou J. Isolation, structural characterization and anti-oxidant activity of a novel polysaccharide from garlic bolt. Carbohydr Polym 2021;267:118194.
  19. Chen W, Zhu X, Ma J, Zhang M, Wu H. Structural elucidation of a novel pectin-polysaccharide from the petal of saussurea laniceps and the mechanism of its anti-HBV activity. Carbohydr Polym 2019;223:115077.
  20. Zhang M, Wang G, Lai F, Wu H. Structural characterization and immunomodulatory activity of a novel polysaccharide from lepidium meyenii. J Agric Food Chem 2016;64(9):1921-31.
  21. Zhou Y, Wang S, Feng W, Zhang Z, Li H. Structural characterization and immunomodulatory activities of two polysaccharides from Rehmanniae Radix Praeparata. Int J Biol Macromol 2021;186:385-95.
  22. Song H, Han L, Zhang Z, Li Y, Yang L, Zhu D, Wang S, He Y, Liu H. Structural properties and bioactivities of pectic polysaccharides isolated from soybean hulls. LWT - Food Sci Technol (Lebensmittel-Wissenschaft -Technol) 2022;170:114079.
  23. Brahmi F, Hadj-Ahmed S, Zarrouk A, Bezine M, Nury T, Madani K, Chibane M, Vejux A, Andreoletti P, Boulekbache-Makhlouf L, Lizard G. Evidence of biological activity of Mentha species extracts on apoptotic and autophagic targets on murine RAW264.7 and human U937 monocytic cells. Pharmaceut Biol 2017;55(1):286-93.
  24. Li JJ, Zhang Y, Han LW, Tian QP, He QX, Wang XM, Sun C, Han J, Liu KC. Tenacissoside H exerts an anti-inflammatory effect by regulating the nf-kappab and p38 pathways in zebrafish. Fish Shellfish Immunol 2018;83:205-12.
  25. Filipponi E, Cecchetti V, Fravolini A. Chemometric rationalization of the structural and physicochemical basis for selective cyclooxygenase-2 inhibition: toward more specific ligands. J Comput Aided Mol Des 2000;14:277-91.
  26. Li Q, Li J, Li H, Xu R, Yuan Y, Cao J. Physicochemical properties and functional bioactivities of different bonding state polysaccharides extracted from tomato fruit. Carbohydr Polym 2019;219:181-90.
  27. Wang W, Ma X, Jiang P, Hu L, Zhi Z, Chen J, Ding T, Ye X, Liu D. Characterization of pectin from grapefruit peel: a comparison of ultrasound-assisted and conventional heating extractions. Food Hydrocolloids 2016;61:730-9.
  28. Yang B, Luo Y, Sang Y, Kan J. Isolation, purification, structural characterization, and hypoglycemic activity assessment of polysaccharides from Hovenia dulcis (Guai Zao). Int J Biol Macromol 2022;208:1106-15.
  29. Wang S, Yang Y, Xiao D, Zheng X, Ai B, Zheng L, Sheng Z. Polysaccharides from banana (Musa spp.) blossoms: isolation, identification and anti-glycation effects. Int J Biol Macromol 2023;236:123957.
  30. Bhadja P, Tan C, Ouyang J, Yu K. Repair effect of seaweed polysaccharides with different contents of sulfate group and molecular weights on damaged HK-2 cells. Polymers 2016;8(5):188.
  31. Wei Q, Zhang YH. Ultrasound-assisted polysaccharide extraction from Cercis chinensis and properites, antioxidant activity of polysaccharide. Ultrason Sonochem 2023;96:106422.
  32. Kim M, Kim SR, Park J, Mun SH, Kwak M, Ko HJ, Baek SH. Structure and antiviral activity of a pectic polysaccharide from the root of Sanguisorba officinalis against enterovirus 71 in vitro/vivo. Carbohydr Polym 2022;281:119057.
  33. Ye J, Zhang C, Lyu X, Hua X, Zhao W, Zhang W, Yang R. Structure and physicochemical properties of arabinan-rich acidic polysaccharide from the byproduct of peanut oil processing. Food Hydrocolloids 2021;117:106743.
  34. Makarova EN, Shakhmatov EG. Characterization of pectin-xylan-glucan-arabinogalactan proteins complex from Siberian fir Abies sibirica Ledeb. Carbohydr Polym 2021;260:117825.
  35. Shen Y, Liang J, Guo YL, Li Y, Kuang HX, Xia YG. Ultrafiltration isolation, structures and anti-tumor potentials of two arabinose- and galactose-rich pectins from leaves of Aralia elata. Carbohydr Polym 2021;255:117326.
  36. Huang W, Zhao M, Wang X, Tian Y, Wang C, Sun J, Wang Z, Gong G, Huang L. Revisiting the structure of arabinogalactan from Lycium barbarum and the impact of its side chain on anti-ageing activity. Carbohydr Polym 2022;286:119282.
  37. Rakhmanberdyeva RK, Shashkov AS, Bobakulov KM, Azizov DZ, Malikova MK, Ogay DK. The structure and prebiotic activity of arabinogalactan from Ferula Kuhistаnica. Carbohydr Res 2021;505:108342.
  38. Liu Q, Fang J, Wang P, Du Z, Li Y, Wang S, Ding K. Characterization of a pectin from LonicerajaponicaThunb and its inhibition effect on AF06242 aggregation and promotion of neuritogenesis. Int J Biol Macromol 2018;107:112-20.
  39. Liu W, Li W, Sui Y, Li XQ, Liu C, Jing H, Zhang H, Cao W. Structure characterization and anti-leukemia activity of a novel polysaccharide from Angelica sinensis (Oliv.) Diels. Int J Biol Macromol 2019;121:161-72.
  40. Zheng ZH, Tu JL, Li XH, Hua Q, Liu WZ, Liu Y, Pan BX, Hu P, Zhang WH. Neuroinflammation induces anxiety- and depressive-like behavior by modulating neuronal plasticity in the basolateral amygdala. Brain Behav Immun 2021;91:505-18.
  41. Zhang H, Guo Q, Liang Z, Wang M, Wang B, Sun-Waterhouse D, Waterhouse GIN, Wang J, Ma C, Kang W. Anti-inflammatory and antioxidant effects of Chaetoglobosin V(b) in LPS-induced RAW264.7 cells: achieved via the MAPK and NF-kappaB signaling pathways. Food Chem Toxicol 2021;147:111915.
  42. Pereira TC, Campos MM, Bogo MR. Copper toxicology, oxidative stress and inflammation using zebrafish as experimental model. J Appl Toxicol 2016;36(7):876-85.
  43. Zhang Q, Ding A, Yue Q, Li W, Zu Y, Zhang Q. Dynamic interaction of neutrophils and RFP-labelled Vibrio parahaemolyticus in zebrafish (Danio rerio). Aquaculture and Fisheries 2017;2(6):269-77.
  44. Li H, Rod-in W, Surayot U, You S, Park WJ. Inhibitory effects of polysaccharides from Korean ginseng berries on LPS-induced RAW264.7 macrophages. PLoS One 2023;18(11).
  45. Talapphet N, Rod-in W, Monmai C, Jang Ay, You S, Park WJ. Immune enhancement effects of Korean ginseng berry polysaccharides on RAW264.7 macrophages through MAPK and NF-κB signalling pathways. Food Agric Immunol 2021;32(1):298-309.
  46. Ye J, Chen D, Ye Z, Huang Y, Zhang N, Lui EMK, Xue C, Xiao M. Fucoidan isolated from Saccharina japonica inhibits LPS-induced inflammation in macrophages via blocking NF-κB, MAPK and JAK-STAT pathways. Mar Drugs 2020;18(6).
  47. Gong G, Dang T, Deng Y, Han J, Zou Z, Jing S, Zhang Y, Liu Q, Huang L, Wang Z. Physicochemical properties and biological activities of polysaccharides from Lycium barbarum prepared by fractional precipitation. Int J Biol Macromol 2018;109:611-8.
  48. Sanjeewa KKA, Fernando IPS, Kim S-Y, Kim H-S, Ahn G, Jee Y, Jeon Y-J. In vitro and in vivo anti-inflammatory activities of high molecular weight sulfated polysaccharide; containing fucose separated from Sargassum horneri: short communication. Int J Biol Macromol 2018;107:803-7.
  49. Sadiq A, Mahnashi MH, Alyami BA, Alqahtani YS, Alqarni AO, Rashid U. Tailoring the substitution pattern of Pyrrolidine-2,5-dione for discovery of new structural template for dual COX/LOX inhibition. Bioorg Chem 2021;112:104969.
  50. Lee YR, Moon GH, Shim D, Kim JC, Lee KJ, Chung KH, An JH. Neuroprotective effects of fermented tea in MPTP-induced Parkinson's disease mouse model via MAPK signaling-mediated regulation of inflammation and antioxidant activity. Food Res Int 2023;164:112133.