Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Hexane fraction from the ethanolic extract of Sargassum serratifolium suppresses cell adhesion molecules via regulation of NF-κB and Nrf2 pathway in human umbilical vein endothelial cells

  • Gwon, Wi-Gyeong (Department of Food Science and Nutrition, Pukyong National University) ;
  • Lee, Sang-Gil (Department of Food Science and Nutrition, Pukyong National University) ;
  • Kim, Jae-Il (Department of Food Science and Nutrition, Pukyong National University) ;
  • Kim, Young-Mog (Department of Food Technology, Pukyong National University) ;
  • Kim, Seon-Bong (Department of Food Technology, Pukyong National University) ;
  • Kim, Hyeung-Rak (Department of Food Science and Nutrition, Pukyong National University)
  • Received : 2018.11.22
  • Accepted : 2019.02.18
  • Published : 2019.03.31
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Abstract

Sargassum serratifolium ethanolic extract has been known for strong antioxidant and anti-inflammatory properties. We prepared hexane fraction from the ethanolic extract of S. serratifolium (HSS) to improve biological activities. In this study, we investigated the effects of HSS on the inhibition of tumor necrosis factor (TNF)-${\alpha}$-induced monocyte adhesion to human umbilical vein endothelial cells (HUVECs). We found that HSS suppressed the production of cell adhesion molecules such as intracellular adhesion molecule-1 and vascular cell adhesion molecule-1 in TNF-${\alpha}$-induced HUVECs. Moreover, TNF-${\alpha}$-induced production of monocyte chemoattractant protein 1 and keratinocyte chemoattractant was inhibited by HSS treatment. HSS suppressed TNF-${\alpha}$-induced nuclear factor kappa B ($NF-{\kappa}B$) activation via preventing proteolytic degradation of inhibitor ${\kappa}B-{\alpha}$. HSS induced the production of heme oxygenase 1 via translocation of Nrf2 into the nucleus in TNF-${\alpha}$-treated HUVECs. Overall, HSS alleviated vascular inflammation through the downregulation of $NF-{\kappa}B$ activation and the upregulation of Nrf2 activation in TNF-${\alpha}$-induced HUVECs. These results indicate that HSS may be used as therapeutic agents for vascular inflammatory disorders.

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References

  1. Ayer A, Zarjou A, Agarwal A, Stocker R. Heme oxygenases in cardiovascular health and disease. Physiol Rev. 2016;96:1449-508. https://doi.org/10.1152/physrev.00003.2016
  2. Azam MS, Joung EJ, Choi J, Kim HR. Ethanolic extract from Sargassum serratifolium attenuates hyperpigmentation through CREB/ERK signaling pathways in ${\alpha}$-MSH-stimulated B16F10 melanoma cells. J Appl Phycol. 2017;29:2089-96. https://doi.org/10.1007/s10811-017-1120-8
  3. Catalan U, Hazas ML, Rubio L, Fernandez-Castillejo S, Pedret A, de la Torre R, Motilva MJ, Sola R. Protective effect of hydroxytyrosol and its predominant plasmatic human metabolites against endothelial dysfunction in human aortic endothelial cells. Mol Nutri Food Res. 2015;59:2523-36. https://doi.org/10.1002/mnfr.201500361
  4. Catapano AL, Pirillo A, Norata GD. Vascular inflammation and low-density lipoproteins: is cholesterol the link? A lesson from the clinical trials. Br J Pharmacol. 2017;174:3973-85. https://doi.org/10.1111/bph.13805
  5. Chen YM, Chiang WC, Lin SL, Wu KD, Tsai TJ, Hsieh BS. Dual regulation of tumor necrosis factor-${\alpha}$-induced CCL2/monocyte chemoattractant protein-1 expression in vascular smooth muscle cells by nuclear factor-${\kappa}B$ and activator protein-1: modulation by type III phosphodiesterase inhibition. J Pharmacol Exp Ther. 2004;309:978-86. https://doi.org/10.1124/jpet.103.062620
  6. Choi ES, Yoon JJ, Han BH, Jeong DH, Lee YJ, Kang DG, Lee HS. Ligustilide attenuates vascular inflammation and activates Nrf2/HO-1 induction and, NO synthesis in HUVECs. Phytomedicine. 2018;38:12-23. https://doi.org/10.1016/j.phymed.2017.09.022
  7. De Filippo K, Henderson RB, Laschinger M, Hogg N. Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J Immunol. 2008;180:4308-15. https://doi.org/10.4049/jimmunol.180.6.4308
  8. Gwon WG, Joung EJ, Kwon MS, Lim SJ, Utsuki T, Kim HR. Sargachromenol protects against vascular inflammation by preventing TNF-${\alpha}$-induced monocyte adhesion to primary endothelial cells via inhibition of NF-${\kappa}B$ activation. Int Immunopharmacol. 2017;42:81-9. https://doi.org/10.1016/j.intimp.2016.11.014
  9. Gwon WG, Joung EJ, Shin T, Utsuki T, Wakamatsu N, Kim HR. Meroterpinoid-rich fraction of the ethanol extract from Sargassum serratifolium suppresses TNF-${\alpha}$-induced monocytes adhesion to vascular endothelium and vascular inflammation in high cholesterol-fed C57BL/6J mice. J Func Foods. 2018;46:384-93. https://doi.org/10.1016/j.jff.2018.05.013
  10. Gwon WG, Lee B, Joung EJ, Choi MW, Yoon N, Shin T, Oh CW, Kim HR. Sargaquinoic acid inhibits TNF-${\alpha}$-induced NF-${\kappa}B$ signaling, thereby contributing to decreased monocyte adhesion to human umbilical vein endothelial cells (HUVECs). J Agric Food Chem. 2015;63:9053-61. https://doi.org/10.1021/acs.jafc.5b04050
  11. Huang W, Huang M, Ouyang H, Peng J, Liang J. Oridonin inhibits vascular inflammation by blocking NF-${\kappa}B$ and MAPK activation. Eur J Pharmacol. 2018;826:133-9. https://doi.org/10.1016/j.ejphar.2018.02.044
  12. Huo Y, Weber C, Forlow SB, Sperandio M, Thatte J, Mack M, Jung S, Littman DR, Ley K. The chemokine KC, but not monocyte chemoattractant protein-1, triggers monocyte arrest on early atherosclerotic endothelium. J Clin Invest. 2001;108:1307-14. https://doi.org/10.1172/JCI12877
  13. Ishikawa K, Sugawara D, Wang X, Suzuki K, Itabe H, Maruyama Y, Lusis AJ. Heme oxygenase-1 inhibits atherosclerotic lesion formation in ldl-receptor knockout mice. Circ Res. 2001;88:506-12. https://doi.org/10.1161/01.RES.88.5.506
  14. Joung EJ, Gwon WG, Shin T, Jung BM, Choi J, Kim HR. Anti-inflammatory action of the ethanolic extract from Sargassum serratifolium on lipopolysaccharidestimulated mouse peritoneal macrophages and identification of active components. J Appl Phycol. 2017;29:563-73. https://doi.org/10.1007/s10811-016-0954-9
  15. Joung EJ, Lee B, Gwon WG, Shin T, Jung BM, Yoon NY, Choi JS, Oh CW, Kim HR. Sargaquinoic acid attenuates inflammatory responses by regulating NF-${\kappa}B$ and Nrf2 pathways in lipopolysaccharide-stimulated RAW 264.7 cells. Int Immunopharmacol. 2015;29:693-700. https://doi.org/10.1016/j.intimp.2015.09.007
  16. Kato H, Amersi F, Buelow R, Melinek J, Coito AJ, Ke BBRW, Kupiec-Weglinski JW. Heme oxygenase-1 overexpression protects rat livers from ischemia/reperfusion injury with extended cold preservation. Am J Transplantation. 2001;1:121-8. https://doi.org/10.1034/j.1600-6143.2001.10205.x
  17. Kawamura K, Ishikawa K, Wada Y, Kimura S, Matsumoto H, Kohro T, Itabe H, Kodama T, Maruyama Y. Bilirubin from heme oxygenase-1 attenuates vascular endothelial activation and dysfunction. Arterioscler Thromb Vasc Biol. 2005;25:155-60. https://doi.org/10.1161/01.ATV.0000148405.18071.6a
  18. Kim JH, Na HJ, Kim CK, Kim JY, Ha KS, Lee H, Chung HT, Kwon HJ, Kwon YG, Kim YM. The non-provitamin A carotenoid, lutein, inhibits NF-${\kappa}B$-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-${\kappa}B$-inducing kinase pathways: role of $H_2O_2$ in NF-${\kappa}B$ activation. Free Rad Biol Med. 2008;45:885-96. https://doi.org/10.1016/j.freeradbiomed.2008.06.019
  19. Kleinbongard P, Heusch G, Schulz R. TNF${\alpha}$ in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther. 2010;127:295-314. https://doi.org/10.1016/j.pharmthera.2010.05.002
  20. Kwon M, Lim SJ, Joung EJ, Lee B, Oh CW, Kim HR. Meroterpenoid-rich fraction of an ethanolic extract from Sargassum serratifolium alleviates obesity and nonalcoholic fatty liver disease in high fat-fed C57BL/6J mice. J Func Foods. 2018;47:288-98. https://doi.org/10.1016/j.jff.2018.05.063
  21. Lim S, Choi AH, Kwon M, Joung EJ, Shin T, Lee SG, Kim NG, Kim HR. Evaluation of antioxidant activities of various solvent extract from Sargassum serratifolium and its major antioxidant components. Food Chem. 2019;278:178-84. https://doi.org/10.1016/j.foodchem.2018.11.058
  22. Lim S, Kwon M, Joung EJ, Shin T, Oh CW, Choi JS, Kim HR. Meroterpenoid-rich fraction of the ethanolic extract from Sargassum serratifolium suppressed oxidative stress induced by tert-butyl hydroperoxide in HepG2 cells. Mar Drugs. 2018;16:374. https://doi.org/10.3390/md16100374
  23. Liu L, Heinrich M, Myers S, Dworjanyn SA. Towards a better understanding of medicinal uses of the brown seaweed Sargassum in traditional Chinese medicine: a phytochemical and pharmacological review. J Ethnopharmacol. 2012;142:591-619. https://doi.org/10.1016/j.jep.2012.05.046
  24. Madge LA, Pober JS. TNF signaling in vascular endothelial cells. Exp Mol Pathol. 2001;70:317-25. https://doi.org/10.1006/exmp.2001.2368
  25. Nallasamy P, Si H, Babu PV, Pan D, Fu Y, Brooke EA, Shah H, Zhen W, Zhu H, Liu D, Li Y, Jia Z. Sulforaphane reduces vascular inflammation in mice and prevents TNF-${\alpha}$-induced monocyte adhesion to primary endothelial cells through interfering with the NF-${\kappa}B$ pathway. J Nutr Biochem. 2014;25:824-33. https://doi.org/10.1016/j.jnutbio.2014.03.011
  26. Namiki M, Kawashima S, Yamashita T, Ozaki M, Hirase T, Ishida T, Inoue N, Hirata K, Matsukawa A, Morishita R, Kaneda Y, Yokoyama M. Local overexpression of monocyte chemoattractant protein-1 at vessel wall induces infiltration of macrophages and formation of atherosclerotic lesion: synergism with hypercholesterolemia. Arterioscler Thromb Vas Biol. 2002;22:115-20. https://doi.org/10.1161/hq0102.102278
  27. Oh SJ, Joung EJ, Kwon MS, Lee B, Utsuki T, Oh CW, Kim HR. Anti-inflammatory effect of ethanolic extract of Sargassum serratifolium in lipopolysaccharidestimulated BV2 microglial cells. J Med Food. 2016;19:1023-31. https://doi.org/10.1089/jmf.2016.3732
  28. Packard RR, Libby P. Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin Chem. 2008;54:24-38. https://doi.org/10.1373/clinchem.2007.097360
  29. Rao RM, Yang L, Garcia-Cardena G, Luscinskas FW. Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ Res. 2007;101:234-47. https://doi.org/10.1161/CIRCRESAHA.107.151860b
  30. Zhang H, Park Y, Wu J, Chen X, Lee S, Yang J, Dellsperger KC, Zhang C. Role of TNF-${\alpha}$ in vascular dysfunction. Clin Sci. 2009;116:219-30. https://doi.org/10.1042/CS20080196

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