Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Immune Enhancement Effects of Codium fragile Anionic Macromolecules Combined with Red Ginseng Extract in 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 Marine Food Science and Technology, Gangneung-Wonju National University) ;
  • You, Sang-Guan (Department of Marine Food Science and Technology, Gangneung-Wonju National University) ;
  • Lee, Sang-min (Department of Marine Biotechnology, Gangneung-Wonju National University) ;
  • Park, Woo Jung (Department of Wellness-Bio Industry, Gangneung-Wonju National University)
  • Received : 2019.05.09
  • Accepted : 2019.08.06
  • Published : 2019.09.28
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Abstract

Codium fragile is an edible seaweed in Asian countries that has been used as a thrombolytic, anticoagulant, antioxidant, anti-inflammatory, and immune-stimulatory agent. Ginseng has also been known to maintain immune homeostasis and to regulate the immune system via enhancing resistance to diseases and microorganisms. In this study, anionic macromolecules extracted from C. fragile (CFAM) were orally administered with red ginseng extract (100 mg/kg body weight) to cyclophosphamide-induced immunosuppressed male BALB/c mice to investigate the immune-enhancing cooperative effect of Codium fragile and red ginseng. Our results showed that supplementing CFAM with red ginseng extract significantly increased spleen index, T- and B-cell proliferation, NK cell activity, and splenic lymphocyte immune-associated gene expression compared to those with red ginseng alone, even though a high concentration of CFAM with red ginseng decreased immune biomarkers. These results suggest that CFAM can be used as a co-stimulant to enhance health and immunity in immunosuppressed conditions.

Keywords

References

  1. 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
  2. Balogh P, Horvath G, Szakal AK. 2004. Immunoarchitecture of distinct reticular fibroblastic domains in the white pulp of mouse spleen. J. Histochem. Cytochem. 52: 1287-1298. https://doi.org/10.1177/002215540405201005
  3. Nolte MA, Hamann A, Kraal G, Mebius RE. 2002. The strict regulation of lymphocyte migration to splenic white pulp does not involve common homing receptors. Immunology 106: 299-307. https://doi.org/10.1046/j.1365-2567.2002.01443.x
  4. Lori A, Perrotta M, Lembo G, Carnevale D. 2017. The spleen: a hub connecting nervous and immune systems in cardiovascular and metabolic diseases. Int. J. Mol. Sci. 18: 1216. https://doi.org/10.3390/ijms18061216
  5. Mebius RE, Kraal G. 2005. Structure and function of the spleen. Nat. Rev. Immunol. 5: 606-616. https://doi.org/10.1038/nri1669
  6. Im SA, Kim K, Lee CK. 2006. Immunomodulatory activity of polysaccharides isolated from Salicornia herbacea. Int. Immunopharmacol. 6: 1451-1458. https://doi.org/10.1016/j.intimp.2006.04.011
  7. Montaldo E, Del Zotto G, Della Chiesa M, Mingari MC, Moretta A, De Maria A, et al. 2013. Human NK cell receptors/markers: a tool to analyze NK cell development, subsets and function. Cytometry A 83: 702-713.
  8. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510. https://doi.org/10.1038/ni1582
  9. Iida Y, Harashima N, Motoshima T, Komohara Y, Eto M, Harada M. 2017. Contrasting effects of cyclophosphamide on anti-CTL-associated protein 4 blockade therapy in two mouse tumor models. Cancer Sci. 108: 1974-1984. https://doi.org/10.1111/cas.13337
  10. Pass GJ, Carrie D, Boylan M, Lorimore S, Wright E, Houston B, et al. 2005. Role of hepatic cytochrome P450s in the pharmacokinetics and toxicity of cyclophosphamide: studies with the hepatic cytochrome P450 reductase null mouse. Cancer Res. 65: 4211-4217. https://doi.org/10.1158/0008-5472.CAN-04-4103
  11. Fishman P, Bar-Yehuda S, Barer F, Madi L, Multani AS, Pathak S. 2001. The A3 adenosine receptor as a new target for cancer therapy and chemoprotection. Exp. Cell Res. 269: 230-236. https://doi.org/10.1006/excr.2001.5327
  12. Dan D, Fischer R, Adler S, Forger F, Villiger PM. 2014. Cyclophosphamide: as bad as its reputation? Long-term single centre experience of cyclophosphamide side effects in the treatment of systemic autoimmune diseases. Swiss Med. Wkly. 144: w14030.
  13. Singh KP, Gupta RK, Shau H, Ray PK. 1993. Effect of ASTA-Z 7575 (INN Maphosphamide) on human lymphokine-activated killer cell induction. Immunopharmacol. Immunotoxicol. 15: 525-538. https://doi.org/10.3109/08923979309019729
  14. 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-kappaB pathways in IL-1betainduced rat primary chondrocytes and a rat osteoarthritis model. Biomed. Pharmacother. 97: 264-270. https://doi.org/10.1016/j.biopha.2017.10.130
  15. 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
  16. 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
  17. 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
  18. Ki Yeul N. 2005. The comparative understanding between red ginseng and white ginsengs, processed ginsengs (Panax ginseng C. A. Meyer). J. Ginseng Res. 29: 1-18. https://doi.org/10.5142/JGR.2005.29.1.001
  19. Babiker LB, Gadkariem EA, Alashban RM, ALjohar HI. 2014. Investigation of stability of Korean ginseng in herbal drug product. Am. J. Appl. Sci. 11: 160-170. https://doi.org/10.3844/ajassp.2014.160.170
  20. 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
  21. 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
  22. Huang GC, Wu LS, Chen LG, Yang LL, Wang CC. 2007. Immuno-enhancement effects of Huang Qi Liu Yi Tang in a murine model of cyclophosphamide-induced leucopenia. J. Ethnopharmacol. 109: 229-235. https://doi.org/10.1016/j.jep.2006.07.023
  23. Yu ZP, Xu DD, Lu LF, Zheng XD, Chen W. 2016. Immunomodulatory effect of a formula developed from American ginseng and Chinese jujube extracts in mice. J. Zhejiang Univ. Sci. B. 17: 147-157. https://doi.org/10.1631/jzus.B1500170
  24. 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
  25. 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
  26. Lee KC, Ladizinski B, Federman DG. 2012. Complications associated with use of levamisole-contaminated cocaine: an emerging public health challenge. Mayo Clin. Proc. 87: 581-586. https://doi.org/10.1016/j.mayocp.2012.03.010
  27. 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
  28. Park HR, Lee HS, Cho SY, Kim YS, Shin KS. 2013. Antimetastatic effect of polysaccharide isolated from Colocasia esculenta is exerted through immunostimulation. Int. J. Mol. Med. 31: 361-368. https://doi.org/10.3892/ijmm.2012.1224
  29. Chalamaiah M, Yu W, Wu J. 2018. Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: A review. Food Chem. 245: 205-222. https://doi.org/10.1016/j.foodchem.2017.10.087
  30. Chaplin DD. 2010. Overview of the immune response. J. Allergy Clin. Immunol. 125(2 Suppl 2): S3-S23. https://doi.org/10.1016/j.jaci.2009.12.980
  31. Ahlmann M, Hempel G. 2016. The effect of cyclophosphamide on the immune system: implications for clinical cancer therapy. Cancer Chemother. Pharmacol. 78: 661-671. https://doi.org/10.1007/s00280-016-3152-1
  32. Emadi A, Jones RJ, Brodsky RA. 2009. Cyclophosphamide and cancer: golden anniversary. Nat. Rev. Clin. Oncol. 6: 638-647. https://doi.org/10.1038/nrclinonc.2009.146
  33. 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
  34. Bronte V, Pittet MJ. 2013. The spleen in local and systemic regulation of immunity. Immunity 39: 806-818. https://doi.org/10.1016/j.immuni.2013.10.010
  35. Lai X, Pei Q, Song X, Zhou X, Yin Z, Jia R, et al. 2016. The enhancement of immune function and activation of NF-kappaB by resveratrol-treatment in immunosuppressive mice. Int. Immunopharmacol. 33: 42-47. https://doi.org/10.1016/j.intimp.2016.01.028
  36. Tu J, Sun H-X, Ye Y-P. 2008. Immunomodulatory and antitumor activity of triterpenoid fractions from the rhizomes of Astilbe chinensis. J. Ethnopharmacol. 119: 266-271. https://doi.org/10.1016/j.jep.2008.07.007
  37. 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
  38. Bloom BR. 1982. Natural killers to rescue immune surveillance? Nature 300: 214-215. https://doi.org/10.1038/300214a0
  39. Talmadge JE, Meyers KM, Prieur DJ, Starkey JR. 1980. Role of natural killer cells in tumor growth and metastasis: C57BL/6 normal and beige mice. J. Natl. Cancer Inst. 65: 929-935.
  40. Constant SL, Bottomly K. 1997. Induction of Th1 and Th2 CD4+ T cell responses: the alternative approaches. Annu. Rev. Immunol. 15: 297-322. https://doi.org/10.1146/annurev.immunol.15.1.297
  41. Mosmann TR, Coffman RL. 1989. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7: 145-173. https://doi.org/10.1146/annurev.iy.07.040189.001045
  42. Liu C, Li X, Li Y, Feng Y, Zhou S, Wang F. 2008. Structural characterisation and antimutagenic activity of a novel polysaccharide isolated from Sepiella maindroni ink. Food Chem. 110: 807-813. https://doi.org/10.1016/j.foodchem.2008.02.026

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