Journal of Chitin and Chitosan (한국키틴키토산학회지)

The Korean Society for Chitin and Chitosan (한국키틴키토산학회)
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Radio-protective Effect of a Polysaccharide from Ishige okamurae against Gamma Ray-irradiated Mouse Immune Cells

방사선을 조사한 면역 세포에 대한 패 다당류의 보호 효과

  • Lee, WonWoo (Department of Marine Life Sciences, Jeju National University) ;
  • Ahn, Ginnae (Department of Marine Bio-Food, Chonnam National University) ;
  • Kang, Nalae (Department of Marine Life Sciences, Jeju National University) ;
  • Kim, Eun-A (Department of Marine Life Sciences, Jeju National University) ;
  • Jee, Youngheun (Department of Veterinary Medicine, Jeju National University) ;
  • Jeon, You-Jin (Department of Marine Life Sciences, Jeju National University)
  • 이원우 (제주대학교 해양생명과학과) ;
  • 안긴내 (전남대학교 해양바이오식품학과) ;
  • 강나래 (제주대학교 해양생명과학과) ;
  • 김은아 (제주대학교 해양생명과학과) ;
  • 지영흔 (제주대학교 수의학과) ;
  • 전유진 (제주대학교 해양생명과학과)
  • Received : 2015.08.11
  • Accepted : 2015.10.12
  • Published : 2015.12.31
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Abstract

In this study, we prepared a crude polysaccharide from a Celluclast enzymatic extract of Ishige okamurae (IOP) and evaluated its radio-protective effects in immune cells of gamma ray-irradiated mice. First, the extraction yield of IOP was approximately 14.5% and contained major contents of galactose (20.8%), glucose (18.1%), and mannose (14.8%). Also, IOP dose-dependently increased the proliferation of splenocytes without cytotoxicity. In addition, IOP significantly enhanced the proliferation of 2 Gy-irradiated splenocytes whereas reduced the intracellular ROS production. In further study, IOP improved the ratio of spleen weight/body weight by increasing the number and proliferation of splenocytes, compared to only 2 Gy-irradiated mice. Especially, IOP increased the population of $CD8^+$ cytolytic T cells, whereas reduced the population of Gr-1 granulocytes. Interestingly, IOP recovered the ratio of $CD4^+$ helper T cells/$CD8^+$ cytolytic T cells, compared to the only 2 Gy-irradiated mice. According to these results, we suggest that IOP protected mice as improving the peripheral immune system damaged by gamma ray irradiation in mice.

본 연구는 방사선이 조사된 마우스 면역 세포와 마우스의 면역 기능에 대한 패의 효소적 추출물로부터 제조된 다당류 성분의 방사선 방호 효능을 확인하였다. 패로부터 효소적 추출 기법을 이용한 경우, 높은 수율과 탄수화물 함량을 나타내었고, 에탄올 침전법을 이용한 다당류 성분 분리시 주로 glucose, galactose와 mannose의 단당으로 이루어진 패 다당류 성분(IOP)를 얻을 수 있었고, 이것은 더 높아진 탄수화물 함량을 보였다. 분리된 IOP는 마우스 면역 세포의 증식을 세포 독성 없이 유의적으로 유도하였고, 흥미롭게도 이러한 IOP의 면역 세포 증식 효능은 방사선 조사가 야기한 세포 생존율과 증식 감소 및 세포 내 ROS 생성 증가를 억제하는 데에도 영향을 끼쳤다. 뿐만 아니라, 방사선이 조사된 마우스로부터 얻어진 말초면역기관인 비장 조직의 축소, 수와 증식능의 감소가 IOP의 경구 투여에 의해 회복된다는 것을 확인할 수 있었다. 게다가 IOP의 처리는 방사선 조사에 의해 야기된 cytolytic T lymphocyte, monocytes와 granulocytes의 수적 감소를 회복시켰다. 이와 같이 실험을 종합하여 볼 때, IOP는 방사선 조사에 의해 야기되는 면역 세포의 수적 및 기능적 저하를 회복시킴으로서 방사선 방호 효능을 가진다는 것을 제시할 수 있고, 차후 천연 방사선 방호를 위한 소재로서 이용 가치가 있다고 사료된다.

Keywords

Acknowledgement

Supported by : 한국연구재단

References

  1. Park, E. J., Jeon, S. M., Joo, H. G., Hwang, K. K., and Jee, Y.: Radioprotective effect of fucoidan against hematopoietic and small intestinal stem cells of ${\gamma}$-ray irradiated mice. Korean J. Vet. Res. 2008, 48, 393-399.
  2. Lee, S. H., Kang, M. C., Moon, S. H., Jeon, B. T., and Jeon, Y. J.: Potential use of ultrasound in antioxidant extraction from Ecklonia cava. Algae., 2013, 28, 371-378. https://doi.org/10.4490/algae.2013.28.4.371
  3. Kim, A., Bing, S. J., Cho, J., Ahn, G., Lee, J. H., Jeon, Y. J., Lee, B. G., and Jee, Y.: Protective effect of Hizikia fusiforme on radiation-induced damage in splenocytes. Korean J. Vet. Res. 2015, 55, 21-30. https://doi.org/10.14405/kjvr.2015.55.1.21
  4. Park, E., Ahn, G. N., Lee, N. H., Kim, J. M., Yun, J. S., Hyun, J. W., Jeon, Y. J., Wie, M. B., Lee, Y. J., Park, J. W., and Jee, Y.: Radioprotective properties of eckol against ionizing radiation in mice. FEBS Lett. 2008, 582, 925-930. https://doi.org/10.1016/j.febslet.2008.02.031
  5. Chen, T., Burke, K. A., Zhan, Y., Wang, X., Shibata, D., and Zhao, Y.: IL-2 facilitates both recovery of endogenous hematopoiesis and the engraftment of stem cells after ionizing radiation. Exp. Hematol. 2007, 35, 203-213. https://doi.org/10.1016/j.exphem.2006.10.002
  6. Neta, R., Douches, S., and Oppenheim, J. J.: Interleukin 1 is a radioprotector. J. Immunol. 1986, 136, 2483-2485.
  7. Goel, H. C., Prasad, J., Singh, S., Sagar, R. K., Agrawala, P. K., Bala, M., Sinha, A. K., and Dogra, R.: Radioprotective potential of an herbal extract of Tinospora cordifolia. J. Radiat Res. 2004, 45, 61-68. https://doi.org/10.1269/jrr.45.61
  8. Bogo, V., Jacobs, A. J., and Weiss, J. F.: Behavioral Toxicity and efficacy of WR-2721 as a radioprotectant. Radiat. Res. 1985, 104, 182-190. https://doi.org/10.2307/3576614
  9. MacVittie, T. J., Monroy, R. L., Patchen, M. L., and Souza, L. M.: Therapeutic use of recombinant human G-CSF (rhG-CSF) in a canine model of sublethal and lethal wholebody irradiation. Int. J. Radiat. Biol. 1990, 57, 723-736. https://doi.org/10.1080/09553009014550891
  10. Neta, R.: Role of cytokines in radioprotection. Pharmacol. Ther. 1988, 39, 261-266. https://doi.org/10.1016/0163-7258(88)90070-8
  11. Neta, R., Douches, S., and Oppenheim, J. J.: Interleukin 1 is a radioprotector. J. Immunol. 1986, 136, 2483-2485.
  12. Utley, J. F., Phillips, T. L., and Kane, L. J.: Protection of normal tissues by WR2721 during fractionated irradiation. Int. J. Radiat. Oncol. Biol. Phys. 1976, 1, 699-703. https://doi.org/10.1016/0360-3016(76)90152-8
  13. Shin, T., Ahn, M., Hyun, J. W., Kim, S. H., and Moon, C.: Antioxidant marine algae phlorotannins and radioprotection: A review of experimental evidence. Acta Histochem. 2014, 116, 669-674. https://doi.org/10.1016/j.acthis.2014.03.008
  14. Park, E., Lee, N. H., Joo, H. G., and Jee, Y.: Modulation of apoptosis of eckol against ionizing radiation in mice. Biochem. Biophys. Res. Commun. 2008, 372, 792-797. https://doi.org/10.1016/j.bbrc.2008.05.140
  15. Moon, C., Kim, S. H., Kim, J. C., Hyun, J. W., Lee, N. H., Park, J. W., and Shin, T.: Protective effect of phlorotannin components phloroglucinol and eckol on radiation-induced intestinal injury in mice. Phytother. Res. 2008, 22, 238-242. https://doi.org/10.1002/ptr.2298
  16. Guiry, M. D. and Bulunden, G.: Seaweed resource in europe: Uses and potential. wiley, chichester west sussex, U.K. (1991).
  17. Ahn, M. J., Yoon, K. D., Kim, C. Y., Kim, J. H., Shin, C. G., and Kim, J.: Inhibitory activity on HIV-1 reverse transcriptase and integrase of a carmalol derivative from a brown alga, Ishige okamurae. Phytother. Res. 2006, 20, 711-713. https://doi.org/10.1002/ptr.1939
  18. Heo, S. J., Kim, J. P., Jung, W. K., Lee, N. H., Kang, H. S., Jun, E. M., Park, S. H., Kang, S. M., Lee, Y. J., Park, P. J., and Jeon, Y. J.: Identification of chemical structure and free radical scavenging activity of diphlorethohydroxycarmalol isolated from a brown alga, Ishige okamurae. J. Microbiol. Biotechnol. 2008, 18, 676-681.
  19. Kim, B. K. and Kim, M. H.: The Effect of Ishige okamurae extracts on antioxidant activity and serum lipid content in ovariectomized rats. J. Life Sci. 2013, 23, 1501-1508. https://doi.org/10.5352/JLS.2013.23.12.1501
  20. Heo, S. J., Cha, S. H., Kim, K. N., Lee, S. H., Ahn, G., Kang, D. H., Oh, C., Choi, Y. U., Affan, A., Kim, D., and Jeon, Y. J.: Neuroprotective effect of phlorotannin isolated from Ishige okamurae against $H_2O_2$-induced oxidative stress in murine hippocampal neuronal cells, HT22. Appl. Biochem. Biotechnol. 2012, 166, 1520-1532. https://doi.org/10.1007/s12010-012-9545-7
  21. Ahn, M., Moon, C., Yang, W., Ko, E. J., Hyun, J. W., Joo, H. G., Jee, Y., Lee, N. H., Park, J. W., Ko, R. K., Kim, G. O., and Shin, T.: Diphlorethohydroxycarmalol, isolated from the brown algae Ishige okamurae, protects against radiationinduced cell damage in mice. Food Chem. Toxicol. 2011, 49, 864-870. https://doi.org/10.1016/j.fct.2010.12.008
  22. Heo, S. J., Lee, K. W., Song, C. B., and Jeon, Y. J.: Antioxidant activity of enzymatic extracts from brwon seaweeds. Algae 2003, 18, 71-81. https://doi.org/10.4490/ALGAE.2003.18.1.071
  23. Xu, H. S., Wu, Y. W., Xu, S. F., Sun, H. X., Chen, F. Y., and Yao, L.: Antitumor and immunomodulatory activity of polysaccharides from the roots of Actinidia eriantha. J. Ethnopharmacol. 2009, 125, 310-317. https://doi.org/10.1016/j.jep.2009.06.015
  24. Desai, V. R., Ramkrishnan, R., Chintalwar, G. J., and Sainis, K. B.: G1-4A, an immunomodulatory polysaccharides from Tinospora cordifolia, modulates macrophage responses and protects mice against lipopolysaccharides induced endotoxic shock. Int. Immunopharmacol. 2007, 7, 1375-1386. https://doi.org/10.1016/j.intimp.2007.06.004
  25. Guzmn, S., Gato, A., Lamela, M., Freire-Garabal, M., and Calleja, J. M.: Anti-inflammatory and immunomodulatory activities of polysaccharides from Chlorella stigmatophora and Phaeodactylum tricornutum. Phytother. Res. 2003, 17, 665-670. https://doi.org/10.1002/ptr.1227
  26. Hwang, H. J., Kwon, M. J., Kim, I. H., and Nam, T. J.: The effect of polysaccharide extracted from the marine alga Capsosiphon fulvescens on ethanol administration. Food Chem. Toxicol. 2008, 46, 2653-2647. https://doi.org/10.1016/j.fct.2008.04.027
  27. Shao, B. M., Xu, W., Dai, H., Tu, P., Li, Z., and Gao, X. M.: A study on the immune receptors for polysaccharides from the roots of Astragalus membranaceus, a chinese medicinal herb. Biochem. Biophys. Res. Commun. 2004, 320, 1103-1111. https://doi.org/10.1016/j.bbrc.2004.06.065
  28. Park, H. Y., Lim, C. W., Kim, Y. K., Yoon, H. D., and Lee, K. J.: Immunostimulating and anticancer activities of hot water extract from Capsosiphon fulvescens. J. Korean Soc. Appl. Biol. Chem. 2006, 49, 343-348.
  29. Volman, J. J., Helsper, J. P., Wei, S., Baars, J. J., van Griensven, L. J., Sonnenberg, A. S., Mensink, R. P., and Plat, J.: Effects of mushroom-derived beta-glucan-rich polysaccharide extracts on nitric oxide production by bone marrow-derived macrophages and nuclear factor-kappaB transactivation in Caco-2 reporter cells: can effects be explained by structure? Mol. Nutr. Food Res. 2010, 54, 268-276. https://doi.org/10.1002/mnfr.200900009
  30. Miura, Y.: Oxidative stress, radiation-adaptive responses, and aging. J. Radiat Res. 2004, 45, 357-372. https://doi.org/10.1269/jrr.45.357
  31. Baek, S., Choi, J. H., Ko, S. H., Lee, Y. J., Cha, D. S., and Park, E. Y.: Antioxidant and anti-inflammatory effect of nardostachys chinensis in IFN-${\gamma}$/LPS-stimulated peritoneal macrophage. Korean J. Orient. Physiol. Pathol. 2009, 23, 853-859
  32. Choi, W. H., Oh, Y. S., Ahn, J. Y., Kim, S. R., and Ha, T. Y.: Antioxidative and protective effects of Ulmus davidiana var. japonica extracts on glutamate-induced cytotoxicity in PC 12 Cells. Korean J. Food. Sci. Technol. 2005, 37, 479-483.
  33. Yoon, B. R., Cho, B. J., Lee, H. K., Kim, D. J., Rhee, S. K., Hong, H. D., Kim, K. T., Cho, C. W., Choi. H. S., Lee, B. Y., and Lee, O. H.: Antioxidant and anti-adipogenic effects of ethanolic extracts from Tartary and Common buckwheats. Korean J. Food Preserv. 2012, 19, 123-130. https://doi.org/10.11002/kjfp.2012.19.1.123
  34. Kim, S. S. and Son, S. M.: Oxidative stress and cell dysfunction in diabetes: Role of ROS produced by mitochondria and NAD(P)H oxidase. Korean Diabetes J. 2008, 32, 389-339. https://doi.org/10.4093/kdj.2008.32.5.389
  35. Bing, S. J., Kim, M. J., Ahn, G., Im, J., Kim, D. S., Ha, D., Cho, J., Kim, A., and Jee, Y.: Acidic polysaccharide of Panax ginseng regulates the mitochondria/caspase-dependent apoptotic pathway in radiation-induced damage to the jejunum in mice. Acta Histochem. 2014, 116, 514-521. https://doi.org/10.1016/j.acthis.2013.11.012
  36. Heo, S. J. and Jeon, Y. J.: Radical scavenging capacity and cytoprotective effect of enzymatic digests of Ishige okamurae. J. Appl. Phycol. 2008, 20, 1087-1095. https://doi.org/10.1007/s10811-008-9320-x
  37. Li, X., Wang, Z., and Wang, L.: Polysaccharide of Hohenbuehelia serotina as a defense against damage by whole-body gamma irradiation of mice. Carbohydr. Polym. 2013, 94, 829-835. https://doi.org/10.1016/j.carbpol.2013.02.015
  38. Kim, H. S., Choi, E. O., Park, C., Choi, Y. H., Hyun, S. K., and Hwang, H. J.: Effect of Hizikia fusiforme extracts on antioxidant enzyme activity and Vitamin E concentration in Rats. J. Kor. Soc. Food Sci. Nutr. 2011, 40, 1556-1561. https://doi.org/10.3746/jkfn.2011.40.11.1556
  39. Wilkins, R. C., Kutzner, B. C., Truong, M., and McLean, J. R.: The effect of the ratio of $CD4^+$ to $CD8^+$-cells on radiation-induced apoptosis in human lymphocyte subpopulations. Int. J. Radiat. Biol. 2002, 78, 681-688. https://doi.org/10.1080/09553000210144475
  40. Lee, W., Ahn, G., Lee, B. J., Wijesinghe, W. A., Kim, D., Yang, H., Kim, Y. M., Park, S. J., Jee, Y., and Jeon, Y. J.: Radio-protective effect of polysaccharides isolated from Lactobacillus brevis-fermented Ecklonia cava. Int. J. Biol. Macromol. 2013, 52, 260-266. https://doi.org/10.1016/j.ijbiomac.2012.10.004