Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Co-immunomodulatory Activities of Anionic Macromolecules Extracted from Codium fragile with Red Ginseng Extract on Peritoneal Macrophage of Immune-Suppressed Mice

  • Kim, Ji Eun (Department of Wellness-Bio Industry, Gangneung-Wonju National University) ;
  • Monmai, Chaiwat (Department of Marine Food Science and Technology, Gangneung-Wonju National University) ;
  • Rod-in, Weerawan (Department of Marine Food Science and Technology, Gangneung-Wonju National University) ;
  • Jang, A-yeong (Department of Wellness-Bio Industry, Gangneung-Wonju National University) ;
  • You, Sang-Guan (Department of Wellness-Bio Industry, Gangneung-Wonju National University) ;
  • Lee, Sang-min (Department of Wellness-Bio Industry, Gangneung-Wonju National University) ;
  • Jung, Seok-Kyu (Department of Horticulture, Daegu Catholic University) ;
  • Park, Woo Jung (Department of Wellness-Bio Industry, Gangneung-Wonju National University)
  • Received : 2019.10.10
  • Accepted : 2019.12.24
  • Published : 2020.03.28
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Abstract

In this study we investigated the immune effects of oral administration of anionic macromolecules extracted from Codium fragile (CFAM) and red ginseng extract mixture on the peritoneal macrophage cells in immune-suppressed mice. Cyclophosphamide (CY) induces the immune-suppressed condition. CY-treated mice were orally fed with different concentrations of CFAM supplemented with red ginseng extract and the peritoneal macrophages collected. CY treatment significantly decreased the immune activities of peritoneal macrophages, compared to the normal mice. The administration of CFAM mixed with red ginseng extract significantly boosted the viability of macrophage cells and nitric oxide production of peritoneal macrophages. Further, the oral administration of CFAM mixed with red ginseng extract up-regulated the expression of iNOS, COX-2, and TLR-4 as well as cytokines such as IL-1β, IL-6, TNF-α, and IFN-γ more than the red ginseng-treated group. This study showed that CFAM enhanced the immune activity of red ginseng extract in the peritoneal macrophage cells of immune-suppressed mice. Furthermore, CFAM might be used as a co-stimulant of red ginseng extract through the regulation of macrophage cells for the enhancement of human health and immunity.

Keywords

References

  1. de Veer MJ, Kemp JM, Meeusen EN. 2007. The innate host defence against nematode parasites. Parasite Immunol. 29: 1-9. https://doi.org/10.1111/j.1365-3024.2006.00910.x
  2. Zimmerman LM, Vogel LA, Bowden RM. 2010. Understanding the vertebrate immune system: insights from the reptilian perspective. J. Exp. Biol. 213: 661-671. https://doi.org/10.1242/jeb.038315
  3. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969. https://doi.org/10.1038/nri2448
  4. Ocana-Guzman R, Vazquez-Bolanos L, Sada-Ovalle I. 2018. Receptors that inhibit macrophage activation: mechanisms and signals of regulation and tolerance. J. Immunol. Res. 2018: 8695157.
  5. Arango Duque G, Descoteaux A. 2014. Macrophage cytokines: involvement in immunity and infectious diseases. Front. Immunol. 5: 491.
  6. Wang H, Wang M, Chen J, Tang Y, Dou J, Yu J, et al. 2011. A polysaccharide from Strongylocentrotus nudus eggs protects against myelosuppression and immunosuppression in cyclophosphamide-treated mice. Int. Immunopharmacol. 11: 1946-1953. https://doi.org/10.1016/j.intimp.2011.06.006
  7. Sistigu A, Viaud S, Chaput N, Bracci L, Proietti E, Zitvogel L. 2011. Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Semin. Immunopathol. 33: 369-383. https://doi.org/10.1007/s00281-011-0245-0
  8. Motoyoshi Y, Kaminoda K, Saitoh O, Hamasaki K, Nakao K, Ishii N, et al. 2006. Different mechanisms for anti-tumor effects of low- and high-dose cyclophosphamide. Oncol. Rep. 16: 141-146.
  9. Atsamo AD, Nguelefack TB, Datte JY, Kamanyi A. 2011. Acute and subchronic oral toxicity assessment of the aqueous extract from the stem bark of Erythrina senegalensis DC (Fabaceae) in rodents. J. Ethnopharmacol. 134: 697-702. https://doi.org/10.1016/j.jep.2011.01.023
  10. El-Abasy M, Motobu M, Nakamura K, Koge K, Onodera T, Vainio O, et al. 2004. Preventive and therapeutic effects of sugar cane extract on cyclophosphamide-induced immunosuppression in chickens. Int. Immunopharmacol. 4: 983-990. https://doi.org/10.1016/j.intimp.2004.01.019
  11. Wang J, Tong X, Li P, Cao H, Su W. 2012. Immunoenhancement effects of shenqi fuzheng injection on cyclophosphamide-induced immunosuppression in BALB/c mice. J. Ethnopharmacol. 139: 788-795. https://doi.org/10.1016/j.jep.2011.12.019
  12. Gunther F, Wabnitz GH, Stroh P, Prior B, Obst U, Samstag Y, et al. 2009. Host defence against Staphylococcus aureus biofilms infection: Phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol. Immunol. 46: 1805-1813. https://doi.org/10.1016/j.molimm.2009.01.020
  13. Park TY, Hong MG, Sung H, Kim SY, Suk KT. 2017. Effect of Korean red ginseng in chronic liver disease. J. Ginseng Res. 41: 450-455. https://doi.org/10.1016/j.jgr.2016.11.004
  14. Ernst E. 2010. Panax ginseng: An overview of the clinical evidence. J. Ginseng Res. 34: 259-263. https://doi.org/10.5142/jgr.2010.34.4.259
  15. Lee NH, Son CG. 2011. Systematic review of randomized controlled trials evaluating the efficacy and safety of ginseng. J. Acupunct. Meridian Stud. 4: 85-97. https://doi.org/10.1016/S2005-2901(11)60013-7
  16. Kim JE, Monmai C, Rod-In W, Jang AY, You SG, Lee SM, et al. 2019. Immune enhancement effects of Codium fragile anionic macromolecules combined with red ginseng extract in immunesuppressed mice. J. Microbiol. Biotechnol. 29: 1361-1368. https://doi.org/10.4014/jmb.1905.05017
  17. Helms S. 2004. Cancer prevention and therapeutics: Panax ginseng. Altern. Med. Rev. 9: 259-274.
  18. Kim S, Lee Y, Cho J. 2014. Korean red ginseng extract exhibits neuroprotective effects through inhibition of apoptotic cell death. Biol. Pharm. Bull. 37: 938-946. https://doi.org/10.1248/bpb.b13-00880
  19. Vuksan V, Sievenpipper J, Jovanovski E, Jenkins AL. 2010. Current clinical evidence for Korean red ginseng in management of diabetes and vascular disease: A Toronto's ginseng clinical testing program. J. Ginseng Res. 34: 264-273. https://doi.org/10.5142/jgr.2010.34.4.264
  20. Kim SK, Park JH. 2011. Trends in ginseng research in 2010. J. Ginseng Res. 35: 389-398. https://doi.org/10.5142/jgr.2011.35.4.389
  21. Jung CH, Seog HM, Choi IW, Choi HD, Cho HY. 2005. Effects of wild ginseng (Panax ginseng C.A. Meyer) leaves on lipid peroxidation levels and antioxidant enzyme activities in streptozotocin diabetic rats. J. Ethnopharmacol. 98: 245-250. https://doi.org/10.1016/j.jep.2004.12.030
  22. Joo SS, Won TJ, Lee DI. 2005. Reciprocal activity of ginsenosides in the production of proinflammatory repertoire, and their potential roles in neuroprotection in vivo. Planta. Med. 71: 476-481. https://doi.org/10.1055/s-2005-864145
  23. Moon SM, Lee SA, Han SH, Park BR, Choi MS, Kim JS, et al. 2018. Aqueous extract of Codium fragile alleviates osteoarthritis through the MAPK/NF-${\kappa}B$ pathways in IL-$1{\beta}$-induced rat primary chondrocytes and a rat osteoarthritis model. Biomed. Pharmacother. 97: 264-270. https://doi.org/10.1016/j.biopha.2017.10.130
  24. Kang CH, Choi YH, Park SY, Kim GY. 2012. Antiinflammatory effects of methanol extract of Codium fragile in lipopolysaccharide-stimulated RAW 264.7 cells. J. Med. Food 15: 44-50. https://doi.org/10.1089/jmf.2010.1540
  25. Lee C, Park GH, Ahn EM, Kim BA, Park CI, Jang JH. 2013. Protective effect of Codium fragile against UVB-induced proinflammatory and oxidative damages in HaCaT cells and BALB/c mice. Fitoterapia 86: 54-63. https://doi.org/10.1016/j.fitote.2013.01.020
  26. Tabarsa M, Karnjanapratum S, Cho M, Kim JK, You S. 2013. Molecular characteristics and biological activities of anionic macromolecules from Codium fragile. Int. J. Biol. Macromol. 59: 1-12. https://doi.org/10.1016/j.ijbiomac.2013.04.022
  27. Monmai C, You S, Park WJ. 2019. Immune-enhancing effects of anionic macromolecules extracted from Codium fragile on cyclophosphamide-treated mice. PLoS One 14: e0211570. https://doi.org/10.1371/journal.pone.0211570
  28. Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P. 2014. Use of plant extracts in fish aquaculture as an alternative to chemotherapy: Current status and future perspectives. Aquaculture 433: 50-61. https://doi.org/10.1016/j.aquaculture.2014.05.048
  29. Sherif AH, Mahfouz ME. 2019. Immune status of Oreochromis niloticus experimentally infected with Aeromonas hydrophila following feeding with 1, 3 ${\beta}$-glucan and levamisole immunostimulants. Aquaculture 509: 40-46. https://doi.org/10.1016/j.aquaculture.2019.05.016
  30. Sevag M, Lackman D, Smolens J. 1938. The isolation of the components of streptococcal nucleoproteins in serologically active form. J. Biol. Chem. 124: 425-436. https://doi.org/10.1016/S0021-9258(18)74048-9
  31. Zhu XL, Chen AF, Lin ZB. 2007. Ganoderma lucidum polysaccharides enhance the function of immunological effector cells in immunosuppressed mice. J. Ethnopharmacol. 111: 219-226. https://doi.org/10.1016/j.jep.2006.11.013
  32. Ray A, Dittel BN. 2010. Isolation of mouse peritoneal cavity cells. J. Vis. Exp. (35): e1488.
  33. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. 1982. Analysis of nitrate, nitrite, and [$^{15}N$]nitrate in biological fluids. Anal. Biochem. 126: 131-138. https://doi.org/10.1016/0003-2697(82)90118-X
  34. Kim JK, Cho ML, Karnjanapratum S, Shin IS, You SG. 2011. In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from Enteromorpha prolifera. Int. J. Biol. Macromol. 49: 1051-1058. https://doi.org/10.1016/j.ijbiomac.2011.08.032
  35. Weeks BA, Keisler AS, Myrvik QN, Warinner JE. 1987. Differential uptake of neutral red by macrophages from three species of estuarine fish. Dev. Comp. Immunol. 11: 117-124. https://doi.org/10.1016/0145-305X(87)90013-9
  36. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-${\Delta}{\Delta}CT$ Method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  37. Manosroi A, Saraphanchotiwitthaya A, Manosroi J. 2003. Immunomodulatory activities of Clausena excavata Burm. f. wood extracts. J. Ethnopharmacol. 89: 155-160. https://doi.org/10.1016/S0378-8741(03)00278-2
  38. Yoo SA, Kim OK, Nam DE, Kim YJ, Baek HY, Jun WJ, et al. 2014. Immunomodulatory effects of fermented Curcuma longa L. extracts on RAW264.7 cells. J. Korean Soc. Food Sci. Nutr. 43: 216-223. https://doi.org/10.3746/jkfn.2014.43.2.216
  39. Hirayama D, Iida T, Nakase H. 2017. The phagocytic function of macrophage-enforcing innate immunity and tissue homeostasis. Int. J. Mol. Sci. 19: 92-105. https://doi.org/10.3390/ijms19010092
  40. Rahat MA, Hemmerlein B. 2013. Macrophage-tumor cell interactions regulate the function of nitric oxide. Front. Physiol. 4: 144. https://doi.org/10.3389/fphys.2013.00144
  41. Sotolongo J, Ruiz J, Fukata M. 2012. The role of innate immunity in the host defense against intestinal bacterial pathogens. Curr. Infect. Dis. Rep. 14: 15-23. https://doi.org/10.1007/s11908-011-0234-4
  42. Navegantes KC, de Souza Gomes R, Pereira PAT, Czaikoski PG, Azevedo CHM, Monteiro MC. 2017. Immune modulation of some autoimmune diseases: the critical role of macrophages and neutrophils in the innate and adaptive immunity. J. Transl. Med. 15: 36-56. https://doi.org/10.1186/s12967-017-1141-8
  43. Zhu Q, Liao C, Liu Y, Wang P, Guo W, He M, Huang Z. 2012. Ethanolic extract and water-soluble polysaccharide from Chaenomeles speciosa fruit modulate lipopolysaccharide-induced nitric oxide production in RAW264.7 macrophage cells. J. Ethnopharmacol. 144: 441-447. https://doi.org/10.1016/j.jep.2012.09.042
  44. Hu SS, Bradshaw HB, Chen JS, Tan B, Walker JM. 2008. Prostaglandin E2 glycerol ester, an endogenous COX-2 metabolite of 2-arachidonoylglycerol, induces hyperalgesia and modulates $NF{\kappa}B$ activity. Br. J. Pharmacol. 153: 1538-1549. https://doi.org/10.1038/bjp.2008.33
  45. Lee JH, Moon SH, Kim HS, Park E, Ahn DU, Paik HD. 2017. Immune-enhancing activity of phosvitin by stimulating the production of pro-inflammatory mediator. Poult. Sci. 96: 3872-3878. https://doi.org/10.3382/ps/pex205
  46. Xia Y, Zhai Q. 2010. IL-$1{\beta}$ enhances the antibacterial activity of astrocytes by activation of NF-${\kappa}B$. Glia 58: 244-252. https://doi.org/10.1002/glia.20921
  47. Seo SH, Webster RG. 2002. Tumor necrosis factor alpha exerts powerful anti-influenza virus effects in lung epithelial cells. J. Virol. 76: 1071-1076. https://doi.org/10.1128/JVI.76.3.1071-1076.2002
  48. van Horssen R, Ten Hagen TL, Eggermont AM. 2006. TNF-${\alpha}$ in cancer treatment: molecular insights, antitumor effects, and clinical utility. Oncologist 11: 397-408. https://doi.org/10.1634/theoncologist.11-4-397

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