Journal of Ginseng Research

  • 제46권1호
  • /
  • Pages.23-32
  • /
  • 2022
  • /
  • 1226-8453(pISSN)
  • /
  • 2093-4947(eISSN)
고려인삼학회 (The Korean Society of Ginseng)
권호 표지
DOI QR코드

DOI QR Code

A review of the immunomodulatory activities of polysaccharides isolated from Panax species

  • Hu, Yeye (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • He, Yang (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Niu, Zhiqiang (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Shen, Ting (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Zhang, Ji (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Wang, Xinfeng (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Hu, Weicheng (Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Huaiyin Normal University) ;
  • Cho, Jae Youl (Department of Integrative Biotechnology, Sungkyunkwan University)
  • 투고 : 2021.05.06
  • 심사 : 2021.06.01
  • 발행 : 2022.01.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Panax polysaccharides are biopolymers that are isolated and purified from the roots, stems, leaves, flowers, and fruits of Panax L. plants, which have attracted considerable attention because of their immunomodulatory activities. In this paper, the composition and structural characteristics of purified polysaccharides are reviewed. Moreover, the immunomodulatory activities of polysaccharides are described both in vivo and in vitro. In vitro, Panax polysaccharides exert immunomodulatory functions mainly by activating macrophages, dendritic cells, and the complement system. In vivo, Panax polysaccharides can increase the immune organ indices and stimulate lymphocytes. In addition, this paper also discusses the membrane receptors and various signalling pathways of immune cells. Panax polysaccharides have many beneficial therapeutic effects, including enhancing or activating the immune response, and may be helpful in treating cancer, sepsis, osteoporosis, and other conditions. Panax polysaccharides have the potential for use in the development of novel therapeutic agents or adjuvants with beneficial immunomodulatory properties.

키워드

과제정보

This study was financially supported by Natural Science Foundation of Jiangsu Province (BK20201480).

참고문헌

  1. Attele AS, Wu JA, Yuan CS. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 1999;58:1685-93. https://doi.org/10.1016/S0006-2952(99)00212-9
  2. Chen F, Huang G. Antioxidant activity of polysaccharides from different sources of ginseng. Int J Biol Macromol 2019;125:906-8. https://doi.org/10.1016/j.ijbiomac.2018.12.134
  3. Wang J, Li S, Fan Y, Chen Y, Liu D, Cheng H, et al. Anti-fatigue activity of the water-soluble polysaccharides isolated from Panax ginseng C. A. Meyer. J Ethnopharmacol 2010;130:421-3. https://doi.org/10.1016/j.jep.2010.05.027
  4. Cheng H, Li S, Fan Y, Gao X, Hao M, Wang J, et al. Comparative studies of the antiproliferative effects of ginseng polysaccharides on HT-29 human colon cancer cells. Med Oncol 2011;28:175-81.
  5. Sun C, Chen Y, Li X, Tai G, Fan Y, Zhou Y. Anti-hyperglycemic and anti-oxidative activities of ginseng polysaccharides in STZ-induced diabetic mice. Food Funct 2014;5:845-8. https://doi.org/10.1039/c3fo60326a
  6. Sun Y, Guo M, Feng Y, Zheng H, Lei P, Ma X, et al. Effect of ginseng polysaccharides on NK cell cytotoxicity in immunosuppressed mice. Exp Ther Med 2016;12:3773-7. https://doi.org/10.3892/etm.2016.3840
  7. Lim TS, Na K, Choi EM, Chung JY, Hwang JK. Immunomodulating activities of polysaccharides isolated from Panax ginseng. J Med Food 2004;7:1-6. https://doi.org/10.1089/109662004322984626
  8. Li S, Qi Y, Chen L, Qu D, Li Z, Gao K, et al. Effects of Panax ginseng polysaccharides on the gut microbiota in mice with antibiotic-associated diarrhea. Int J Biol Macromol 2019;124:931-7. https://doi.org/10.1016/j.ijbiomac.2018.11.271
  9. Lim DS, Bae KG, Jung IS, Kim CH, Yun YS, Song JY. Anti-septicaemic effect of polysaccharide from Panax ginseng by macrophage activation. J Infect 2002;45:32-8. https://doi.org/10.1053/jinf.2002.1007
  10. Ghosh R, Bryant DL, Arivett BA, Smith SA, Altman E, Kline PC, et al. An acidic polysaccharide (AGC3) isolated from North American ginseng (Panax quinquefolius) suspension culture as a potential immunomodulatory nutraceutical. Curr Res Food Sci 2020;3:207-16. https://doi.org/10.1016/j.crfs.2020.07.002
  11. Sun Y. Structure and biological activities of the polysaccharides from the leaves, roots and fruits of Panax ginseng C.A. Meyer: an overview. Carbohydr Polym 2011;85:490-9. https://doi.org/10.1016/j.carbpol.2011.03.033
  12. Zhao B, Lv C, Lu J. Natural occurring polysaccharides from Panax ginseng C. A. Meyer: a review of isolation, structures, and bioactivities. Int J Biol Macromol 2019;133:324-36. https://doi.org/10.1016/j.ijbiomac.2019.03.229
  13. Ji X, Hou C, Shi M, Yan Y, Liu Y. An insight into the research concerning Panax ginseng C. A. Meyer polysaccharides: a review. Food Rev Int 2020:1-17. 00.
  14. Guo M, Shao S, Wang D, Zhao D, Wang M. Recent progress in polysaccharides from Panax ginseng C. A. Meyer. Food Funct 2021;12:494-518. https://doi.org/10.1039/D0FO01896A
  15. Loh SH, Park JY, Cho EH, Nah SY, Kang YS. Animal lectins: potential receptors for ginseng polysaccharides. J Ginseng Res 2017;41:1-9. https://doi.org/10.1016/j.jgr.2015.12.006
  16. Cui L, Chen L, Yang G, Li Y, Qiao Z, Liu Y, et al. Structural characterization and immunomodulatory activity of a heterogalactan from Panax ginseng flowers. Food Res Int 2020:109859. https://doi.org/10.1016/j.foodres.2020.109859
  17. Zhang SD, Yin YX, Wei Q. Immunopotentiation on murine spleen lymphocytes induced by polysaccharide fraction of Panax ginseng via upregulating calcineurin activity. Apmis 2010;118:288-96. https://doi.org/10.1111/j.1600-0463.2010.02589.x
  18. Hwang SH, Shin MS, Yoon TJ, Shin KS. Immunoadjuvant activity in mice of polysaccharides isolated from the leaves of Panax ginseng C. A. Meyer. Int J Biol Macromol 2018;107:2695-700. https://doi.org/10.1016/j.ijbiomac.2017.10.160
  19. Wang Y, Huang M, Sun R, Pan L. Extraction, characterization of a Ginseng fruits polysaccharide and its immune modulating activities in rats with Lewis lung carcinoma. Carbohydr Polym 2015;127:215-21. https://doi.org/10.1016/j.carbpol.2015.03.070
  20. Li B, Zhang N, Feng Q, Li H, Wang D, Ma L, et al. The core structure characterization and of ginseng neutral polysaccharide with the immune-enhancing activity. Int J Biol Macromol 2019;123:713-22. https://doi.org/10.1016/j.ijbiomac.2018.11.140
  21. Cui L, Wang J, Huang R, Tan Y, Zhang F, Zhou Y, et al. Analysis of pectin from Panax ginseng flower buds and their binding activities to galectin-3. Int J Biol Macromol 2019;128:459-67. https://doi.org/10.1016/j.ijbiomac.2019.01.129
  22. Zhang X, Yu L, Bi H, Li X, Ni W, Han H, et al. Total fractionation and characterization of the water-soluble polysaccharides isolated from Panax ginseng C. A. Meyer. Carbohydr Polym 2009;77:544-52. https://doi.org/10.1016/j.carbpol.2009.01.034
  23. Zheng Y, Yang G, Zhao Z, Guo T, Shi H, Zhou Y, et al. Structural analysis of ginseng polysaccharides extracted by EDTA solution. RSC Adv 2016;6:2724-30. https://doi.org/10.1039/C5RA22751H
  24. Shin MS, Hwang SH, Yoon TJ, Kim SH, Shin KS. Polysaccharides from ginseng leaves inhibit tumor metastasis via macrophage and NK cell activation. Int J Biol Macromol 2017;103:1327-33. https://doi.org/10.1016/j.ijbiomac.2017.05.055
  25. Zhang X, Li S, Sun L, Ji L, Zhu J, Fan Y, et al. Further analysis of the structure and immunological activity of an RG-I type pectin from Panax ginseng. Carbohydr Polym 2012;89:519-25. https://doi.org/10.1016/j.carbpol.2012.03.039
  26. Ghosh R, Smith SA, Nwangwa EE, Arivett BA, Bryant DL, Fuller ML, et al. Panax quinquefolius (North American ginseng) cell suspension culture as a source of bioactive polysaccharides: immunostimulatory activity and characterization of a neutral polysaccharide AGC1. Int J Biol Macromol 2019;139:221-32. https://doi.org/10.1016/j.ijbiomac.2019.07.215
  27. Ridley BL, O'Neill MA, Mohnen D. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 2001;57:929-67. https://doi.org/10.1016/S0031-9422(01)00113-3
  28. Perez S, Rodriguez-Carvajal MA, Doco T. A complex plant cell wall poly-saccharide: rhamnogalacturonan II. A structure in quest of a function. Biochimie 2003;85:109-21. https://doi.org/10.1016/S0300-9084(03)00053-1
  29. Kim H, Kim HW, Yu KW, Suh HJ. Polysaccharides fractionated from enzyme digests of Korean red ginseng water extracts enhance the immunostimulatory activity. Int J Biol Macromol 2019;121:913-20. https://doi.org/10.1016/j.ijbiomac.2018.10.127
  30. Ferreira SS, Passos CP, Madureira P, Vilanova M, Coimbra MA. Structure-function relationships of immunostimulatory polysaccharides: a review. Carbohydr Polym 2015;132:378-96. https://doi.org/10.1016/j.carbpol.2015.05.079
  31. Li H, Yin M, Zhang Y. Advances in research on immunoregulation of macrophages by plant polysaccharides. Front Immunol 2019;10:145. https://doi.org/10.3389/fimmu.2019.00145
  32. Sun L, Peng X, Sun P, Shi J, Yuan X, Zhu J, et al. Structural characterization and immunostimulatory activity of a novel linear 𝛼-(1→6)-D-glucan isolated from Panax ginseng C. A. Meyer. Glycoconj J 2012;29:357-64. https://doi.org/10.1007/s10719-012-9403-4
  33. Wang L, Yu X, Yang X, Li Y, Yao Y, Lui EMK, et al. Structural and anti-inflammatory characterization of a novel neutral polysaccharide from North American ginseng (Panax quinquefolius). Int J Biol Macromol 2015;74:12-7. https://doi.org/10.1016/j.ijbiomac.2014.10.062
  34. Choi HS, Kim KH, Sohn E, Park JD, Kim BO, Moon EY, et al. Red ginseng acidic polysaccharide (RGAP) in combination with IFN-𝛾 results in enhanced macrophage function through activation of the NF-κB pathway. Biosci Biotechnol Biochem 2008;72:1817-25. https://doi.org/10.1271/bbb.80085
  35. Jiang MH, Zhu L, Jiang JG. Immunoregulatory actions of polysaccharides from Chinese herbal medicine. Expert Opin Ther Targets 2010;14:1367-402. https://doi.org/10.1517/14728222.2010.531010
  36. Schepetkin IA, Quinn MT. Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol 2006;6:317-33. https://doi.org/10.1016/j.intimp.2005.10.005
  37. Ghosh R, Bryant DL, Farone AL. Panax quinquefolius (North American Ginseng) polysaccharides as immunomodulators: current research status and future directions. Molecules 2020;25:5854. https://doi.org/10.3390/molecules25245854
  38. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nunez G, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005;307:731-4. https://doi.org/10.1126/science.1104911
  39. Byeon SE, Lee J, Kim JH, Yang WS, Kwak YS, Kim SY, et al. Molecular mechanism of macrophage activation by red ginseng acidic polysaccharide from Korean red ginseng. Mediators Inflamm 2012;2012:7-9.
  40. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001;106:255-8. https://doi.org/10.1016/S0092-8674(01)00449-4
  41. Steinman RM. Dendritic cells: understanding immunogenicity. Eur J Immunol 2007;37:53-60. https://doi.org/10.1002/eji.200737400
  42. Liu YJ. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001;106:259-62. https://doi.org/10.1016/S0092-8674(01)00456-1
  43. Liu S, Yang Y, Qu Y, Guo X, Yang X, Cui X, et al. Structural characterization of a novel polysaccharide from Panax notoginseng residue and its immunomodulatory activity on bone marrow dendritic cells. Int J Biol Macromol 2020;161:797-809. https://doi.org/10.1016/j.ijbiomac.2020.06.117
  44. Meng J, Meng Y, Liang Z, Du L, Zhang Z, Hu X, et al. Phenotypic and functional analysis of the modification of murine bone marrow dendritic cells (BMDCs) induced by neutral ginseng polysaccharides(NGP). Hum Vaccines Immunother 2013;9:233-41. https://doi.org/10.4161/hv.22612
  45. Kim MH, Byon YY, Ko EJ, Song JY, Yun YS, Shin T, et al. Immunomodulatory activity of ginsan, a polysaccharide of Panax ginseng, on dendritic cells. Korean J Physiol Pharmacol 2009;13:169-73. https://doi.org/10.4196/kjpp.2009.13.3.169
  46. Lambris JD, Reid KBM, Volanakis JE. The evolution, structure, biology and pathophysiology of complement. Immunol Today 1999;20:207-11. https://doi.org/10.1016/S0167-5699(98)01417-0
  47. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010;11:785-97. https://doi.org/10.1038/ni.1923
  48. Fujita T. Evolution of the lectin - complement pathway and its role in innate immunity. Nat Rev Immunol 2002;2:346-53. https://doi.org/10.1038/nri800
  49. Zhu Y, Pettolino F, Mau SI, Shen YC, Chen CF, Kuo YC, et al. Immunoactive polysaccharide-rich fractions from Panax notoginseng. Planta Med 2006;72:1193-9. https://doi.org/10.1055/s-2006-947222
  50. Gao H. Immunostimulating polysaccharides from Chinese medicinal herbs: Panax notoginseng and Viola yedoensis. University of Southern California; 1995.
  51. Gao H, Wang F, Lien EJ, Trousdale MD. Immunostimulating polysaccharides from Panax notoginseng. Pharm Res 1996;13:1196-200. https://doi.org/10.1023/A:1016060119425
  52. Zhang J, Li C, Li J, Guo R, Wang H, Pan J, et al. Immunoregulation on mice of low immunity and effects on five kinds of human cancer cells of Panax japonicus polysaccharide. Evid Based Complement Alternat Med 2015;2015:839697.
  53. Ni W, Zhang X, Wang B, Chen Y, Han H, Fan Y, et al. Antitumor activities and immunomodulatory effects of ginseng neutral polysaccharides in combination with 5-Fluorouracil. J Med Food 2010;13:270-7. https://doi.org/10.1089/jmf.2009.1119
  54. Song YR, Sung SK, Jang M, Lim TG, Cho CW, Han CJ, et al. Enzyme-assisted extraction, chemical characteristics, and immunostimulatory activity of polysaccharides from Korean ginseng (Panax ginseng Meyer). Int J Biol Macromol 2018;116:1089-97. https://doi.org/10.1016/j.ijbiomac.2018.05.132
  55. Taneichi M, Naito S, Kato H, Tanaka Y, Mori M, Nakano Y, et al. T cell-independent regulation of IgE antibody production induced by surface-linked liposomal antigen. J Immunol 2002;169:4246-52. https://doi.org/10.4049/jimmunol.169.8.4246
  56. Huang L, Shen M, Morris GA, Xie J. Sulfated polysaccharides: immunomodulation and signaling mechanisms. Trends Food Sci Technol 2019;92:1-11. https://doi.org/10.1016/j.tifs.2019.08.008
  57. Bing SJ, Ha D, Hwang I, Park E, Ahn G, Song JY, et al. Protective effects on central nervous system by acidic polysaccharide of Panax ginseng in relapse-remitting experimental autoimmune encephalomyelitis-induced SJL/J mice. Am J Chin Med 2016;44:1099-110. https://doi.org/10.1142/s0192415x16500610
  58. Kim K-S, Pyo S, Sohn E-H. Immunomodulation of NK cell activity by red ginseng acidic polysaccharide (RGAP) in ovariectomized rats. J Ginseng Res 2009;33:99-103. https://doi.org/10.5142/JGR.2009.33.2.099
  59. Shu G, Jiang S, Mu J, Yu H, Duan H, Deng X. Antitumor immunostimulatory activity of polysaccharides from Panax japonicus C. A. Mey: roles of their effects on CD4+ T cells and tumor associated macrophages. Int J Biol Macromol 2018;111:430-9. https://doi.org/10.1016/j.ijbiomac.2018.01.011
  60. Ahn JY, Choi IS, Shim JY, Yun EK, Yun YS, Jeong G, et al. The immunomodulator ginsan induces resistance to experimental sepsis by inhibiting Toll-like receptor-mediated inflammatory signals. Eur J Immunol 2006;36:37-45. https://doi.org/10.1002/eji.200535138
  61. Zheng L, Wang M, Peng Y, Li X. Physicochemical characterization of polysaccharides with macrophage immunomodulatory activities isolated from red ginseng (Panax ginseng C. A. Meyer). J Chem 2017;2017:3276430.
  62. Park KM, Young Sook Kim, Jeong Tae Cheon, Joe CO, Han Jae Shin, You Hui Lee, et al. Nitric oxide is involved in the immunomodulating activities of acidic polysaccharide from Panax ginseng. Planta Med 2001;67:122-6. https://doi.org/10.1055/s-2001-11508
  63. Hwang I, Ahn G, Park E, Ha D, Song JY, Jee Y. An acidic polysaccharide of Panax ginseng ameliorates experimental autoimmune encephalomyelitis and induces regulatory T cells. Immunol Lett 2011;138:169-78. https://doi.org/10.1016/j.imlet.2011.04.005
  64. Zhu W, Han B, Sun Y, Wang Z, Yang X. Immunoregulatory effects of a glucogalactan from the root of Panax quinquefolium L. Carbohydr Polym 2012;87:2725-9. https://doi.org/10.1016/j.carbpol.2011.11.066
  65. Yu XH, Liu Y, Wu XL, Liu LZ, Fu W, Song DD. Isolation, purification, characterization and immunostimulatory activity of polysaccharides derived from American ginseng. Carbohydr Polym 2017;156:9-18. https://doi.org/10.1016/j.carbpol.2016.08.092
  66. Wang L, Yao Y, Sang W, Yang X, Ren G. Structural features and immunostimulating effects of three acidic polysaccharides isolated from Panax quinquefolius. Int J Biol Macromol 2015;80:77-86. https://doi.org/10.1016/j.ijbiomac.2015.06.007
  67. Yu X, Yang X, Cui B, Wang L, Ren G. Antioxidant and immunoregulatory activity of alkali-extractable polysaccharides from North American ginseng. Int J Biol Macromol 2014;65:357-61. https://doi.org/10.1016/j.ijbiomac.2014.01.046
  68. Li H, Gu L, Zhong Y, Chen Y, Zhang L, Zhang AR, et al. Administration of polysaccharide from Panax notoginseng prolonged the survival of H22 tumor-bearing mice. Onco Targets Ther 2016;9:3433-41.