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http://dx.doi.org/10.5352/JLS.2018.28.2.207

Socheongja and Socheong 2 Extracts Suppress Lipopolysaccharide-induced Inflammation and Oxidative Stress in RAW 264.7 Macrophages through Activating Nrf2/HO-1 Signaling and Suppressing MAPKs Pathway  

Kwon, Da Hye (Open Laboratory for Muscular & Skeletal Disease Control and Department of Biochemistry, Dongeui University College of Korean Medicine)
Choi, Eun Ok (Open Laboratory for Muscular & Skeletal Disease Control and Department of Biochemistry, Dongeui University College of Korean Medicine)
Hwang, Hye-Jin (Department of Food and Nutrition, College of Nursing, Healthcare Sciences & Human Ecology, Dongeui University)
Kim, Kook Jin (Genomine Advanced Biotechnology Research Institute, Genomine Inc.)
Hong, Su Hyun (Open Laboratory for Muscular & Skeletal Disease Control and Department of Biochemistry, Dongeui University College of Korean Medicine)
Lee, Dong Hee (Genomine Advanced Biotechnology Research Institute, Genomine Inc.)
Choi, Yung Hyun (Open Laboratory for Muscular & Skeletal Disease Control and Department of Biochemistry, Dongeui University College of Korean Medicine)
Publication Information
Journal of Life Science / v.28, no.2, 2018 , pp. 207-215 More about this Journal
Abstract
Inflammatory response and oxidative stress play critical roles in the development and progression of many human diseases. Therefore, a great deal of attention has been focused on finding functional materials that can control inflammation and oxidative stress simultaneously. The purpose of this study was to investigate the effects of Socheongja and Socheong 2, Korean black seed coat soybean varieties, on the inflammatory and oxidative stress induced by lipopolysaccharide (LPS) in RAW 264.7 macrophages. Our data indicated that the extracts of Socheongja (SCJ) and Socheong 2 (SC2) significantly suppressed LPS-induced production of nitrite oxide (NO) and prostaglandin $E_2$, key pro-inflammatory mediators, by suppressing the expression of inducible NO synthase and cyclooxygenase-2. It was also found that SCJ and SC2 reduced the LPS-induced secretion of pro-inflammatory cytokines, such as tumor necrosis $factor-{\alpha}$ and $interleukin-1{\beta}$, which was concomitant with a decrease in the protein levels. In addition, SCJ and SC2 markedly diminished LPS-stimulated intracellular reactive oxygen species accumulation, and effectively enhanced nuclear factor erythroid 2-related factor 2 (Nrf2) and heme oxygenase (HO)-1 expression. Furthermore, LPS-induced activation of mitogen-activated protein kinases (MAPKs) was abrogated by SCJ and SC2. Taken together, these data suggest that SCJ and SC2 may offer protective roles against LPS-induced inflammatory and oxidative responses in RAW 264.7 macrophages through attenuating MAPKs pathway, and these effects are mediated, at least in part, through activating Nrf2/HO-1 pathway. Given these results, we propose that SCJ and SC2 have therapeutic potential in the treatment of inflammatory and oxidative disorders caused by over-activation of macrophages.
Keywords
Anti-inflammation; antioxidant; RAW 264.7 macrophages; Socheongja; Socheong 2;
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1 Barnes, S. 1998. Evolution of the health benefits of soy isoflavone. Proc. Soc. Exp. Biol. Med. 217, 386-392.   DOI
2 Brue, B., Dehne, N., Grossmann, N., Jung, M., Namgaladze, D., Schmid, T., von Knethen, A. and Weigert, A. 2013. Redox control of inflammation in macrophages. Antioxid. Redox. Signal. 19, 595-637.   DOI
3 Cho, B. O., Ryu, H. W., So, Y., Lee, C. W., Jin, C. H., Yook, H. S., Jeong, Y. W., Park, J. C. and Jeong, I. Y. 2014. Anti-inflammatory effect of mangostenone F in lipopolysaccharidestimulated RAW 264.7 macrophages by suppressing $NF-{\kappa}B$ and MAPK activation. Biomol. Ther. 22, 288-294.   DOI
4 Choung, M. G., Baek, I. Y., Kang, S. T., Han, W. Y., Shin, D. C., Moon, H. P. and Kang, K. H. 2001. Isolation and determination of anthocyanins in seed coats of black soybean (Glycine max (L.) Merr.). J. Agric. Food Chem. 49, 5848-5851.   DOI
5 Dinarell, C. A. 2000. Proinflammatory cytokines. Chest 118, 503-508.   DOI
6 Golden, B. D. and Abramson, S. B. 1999. Selective cyclooxygenase-2 inhibitors. Rheum. Dis. Clin. North. Am. 25, 359-378.   DOI
7 Huang, B. P., Lin, C. H., Chen, H. M., Lin, J. T., Cheng, Y. F. and Kao, S. H. 2015. AMPK activation inhibits expression of proinflammatory mediators through downregulation of PI3K/p38 MAPK and $NF-{\kappa}B$ signaling in murine macrophages. DNA Cell Biol. 34, 133-141.   DOI
8 Gong, G. L. 2001. Studies on the standardization of manufacture and cancer protection and anti-obesity effects of Kochujang, Master Degree dissertation, Pusan National University, Busan, Korea.
9 Guo, S., Qiu, P., Xu, G., Wu, X., Dong, P., Yang, G., Zheng, J., McClements, D. J. and Xiao, H. 2012. Synergistic anti-inflammatory effects of nobiletin and sulforaphane in lipopolysaccharide-stimulated RAW 264.7 cells. J. Agric. Food Chem. 60, 2157-2164.   DOI
10 Higuchi, M., Hisgahi, N., Taki, H. and Osawa, T. 1990. Cytolytic mechanisms of activated macrophages: Tumor necrosis factor and L-arginine-dependent mechanisms act synergistically as the major cytolytic mechanisms of activated macrophages. J. Immunol. 144, 1425-1431.
11 Huang, Y., Li, W., Su, Z. Y. and Kong, A. N. 2015. The complexity of the Nrf2 pathway: beyond the antioxidant response. J. Nutr. Biochem. 26, 1401-1413.   DOI
12 Kang, K. A. and Hyun, J. W. 2017. Oxidative stress, Nrf2, and epigenetic modification contribute to anticancer drug resistance. Toxicol. Res. 33, 1-5.   DOI
13 Lee, D. H., Park, J. S., Lee, Y. S., Sung, S. H., Lee, Y. H. and Bae, S. H. 2017. The hypertension drug, verapamil, activates Nrf2 by promoting p62-dependent autophagic Keap1 degradation and prevents acetaminophen-induced cytotoxicity. BMB Rep. 50, 91-96.   DOI
14 Kasahara, E., Sekiyama, A., Hori, M., Hara, K., Takahashi, N., Konishi, M., Sato, E. F., Matsumoto, S., Okamura, H. and Inoue, M. 2011. Mitochondrial density contributes to the immune response of macrophages to lipopolysaccharide via the MAPK pathway. FEBS Lett. 585, 2263-2268.   DOI
15 Kauppinen, A., Suuronen, T., Ojala, J., Kaarniranta, K. and Salminen, A. 2013. Antagonistic crosstalk between $NF-{\kappa}B$ and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal. 25, 1939-1948.   DOI
16 Korea seed & Variety service, https://www.seed.go.kr
17 Lee, T. S. and Chau, L. Y. 2002. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8, 240-246.   DOI
18 Lim, B. O., Jeong, Y. J., Park, M. H., Kim, J. D., Hwang, S. J. and Yu, B. P. 2007. Immunoregulatory effects of Saengshik on DSS-induced inflammatory bowel disease in mouse model system. J. Kor. Soc. Food Sci. Nutr. 36, 32-42.   DOI
19 Loboda, A., Damulewicz, M., Pyza, E., Jozkowicz, A. and Dulak, J. 2016. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell. Mol. Life Sci. 73, 3221-3247.   DOI
20 Maines, M. D. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554.   DOI
21 Mann, J. R., Backlund, M. G. and DuBois, R. N. 2005. Mechanism of disease: Inflammatory mediators and cancer prevention. Nat. Clin. Pract. Oncol. 2, 202-210.
22 Oh, G. S., Pae, H. O. and Chung, H. T. 2003. Nitric oxide priming protects nitric oxide-mediated apoptosis via heme oxygenase-1 induction. Free Radic. Biol. Med. 34, 1136-1145.   DOI
23 Masferrer, J. L., Zweifel, B. S., Manning, P. T., Hauser, S. D., Leahy, K. M., Smith, W. G., Isakson, P. C. and Seibert, K. 1994. Selective inhibition of inducible cyclooxygenase 2 in vivo is anti inflammatory and nonulcerogenic. Proc. Natl. Acad. Sci. USA. 91, 3228-3232.   DOI
24 Mills, E. L. and O'Neill, L. A. 2016. Reprogramming mitochondrial metabolism in macrophages as an anti-inflammatory signal. Eur. J. Immunol. 46, 13-21.   DOI
25 Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P. and Malik, A. B. 2014. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal. 20, 1126-1167.   DOI
26 Otterbein, L. E. and Chai, A. M. 2000. Heme oxygenase: colors of defense against cellular stress. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, 1029-1037.   DOI
27 Pearson, G., Robinson, F., Beers Gibson, T., Xu, B. E., Karandikar, M., Berman, K. and Cobb, M. H. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183.
28 Pittala, V., Salerno, L., Romeo, G., Modica, M. N. and Siracusa, M. A. 2013. A focus on heme oxygenase-1 (HO-1) inhibitors. Curr. Med. Chem. 20, 3711-3732.   DOI
29 Raingeaud, J., Whitmarsh, A. J., Barrett, T., Derijard, B. and Davis, R. J. 1996. MKK3- and MKK6-regulated gene expressionis is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell Biol. 16, 1247-1255.   DOI
30 Record, I. R., Dreosit, I. E. and Mclnerney, J. K. 1995. The antioxidant activity of genistein in vitro. J. Nutr. Biochem. 6, 481-485.   DOI
31 Sirisinha, S. 2011. Insight into the mechanisms regulating immune homeostasis in health and disease. Asian Pac. J. Allergy Immunol. 29, 1-14.
32 Rural Development Administration National Institute of Crop Science, Republic of Korea, www.nics.go.kr
33 Ryter, S. W. and Choi, A. M. 2016. Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Transl. Res. 167, 7-34.   DOI
34 Motterlini, R. and Foresti, R. 2014. Heme oxygenase-1 as a target for drug discovery. Antioxid. Redox Signal. 20, 1810-1826.   DOI
35 Stuehr, H. H., Kwon, N. S., Weise, M. and Nathan, C. 1991. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: and FAD- and FMN-containing flavoprotein. Proc. Natl. Acad. Sci. USA. 88, 7773-7777.   DOI
36 Tan, H. Y., Wang, N., Li, S., Hong, M., Wang, X. and Feng, Y. 2016. The reactive oxygen species in macrophage polarization: Reflecting its dual role in progression and treatment of human diseases. Oxid. Med. Cell. Longeva. 2016, 2795090.
37 Tomomatsu, H. 1994. Health effects of oligosaccharides. Food Technol. 48, 61-65.
38 Tsan, M. F. 2006. Toll-like receptors, inflammation and cancer. Semin Cancer Biol. 16, 32-37.   DOI
39 Wei, H., Cai, Q. and Rahn, R. 1996. Inhibition of UV light and fenton reaction-induced oxidative DNA damage by the soybean isoflacone genistein. Carcinogenesis 17, 73-77.   DOI
40 Willoughby, D. A. 1975. Human arthritis applied to animal models. Towards a better therapy. Ann. Rheum. Dis. 34, 471-478.   DOI
41 Yang, J. L., Jang, J. H., Radliakrishnan, V., Kim, Y. H. and Song, Y. S. 2008. ${\beta}$-Glucan suppresses LPS-stimulated NO production through the down-regulation of iNOS expression and $NF-{\kappa}B$ transactivation in raw 264.7 macrophages. Food Sci. Biotechnol. 17, 106-113.